Progress in Neurobiology, 1975, Vol. 5, Part 2, pp. 127-166. Pergamon Press. Printed in Great Britain

VISUAL PROCESSING IN THE ROCK LOBSTER (CRUSTACEA) BARBARA YORK

Department of Physiology and Biochemistry, University of Southampton, Southampton S09 3TU and C. A. G. WIERSMA

Division of Biology, California Institute of Technology, Pasadena, Calif. 91109, U.S.A.

Contents Introduction

129

1. Optic interneurones 1.1. The structure of the decapod crustacean eye 1.2. The interneurones of the optic nerve 1.3. Fibre labelling 1.4. Identification of fibres 1.5. Interneurone inputs 1.6. Classes of interneurones 1.7. Possible information to be obtained from the preparation 1.8. Methods 1.9. Experimental procedure 1.10. Optic interneurones 1.10.1. Sustaining fibres 1.10.2. Dimming fibres 1.10.3. Jittery-movement fibres 1.10.4. Medium-movement fibres 1.10.5. Fast-movement fibres 1.10.6. Light-movement fibres 1.10.7. Space-constant fibres 1.10.8. Unidirectional movement fibres with and without space constant features 1.10.9. Multimodal mlidirectional fibres 1.10.10. Seeing fibres 1.10.11. Other fibre types

129 129 130 131 131 132 134 134 135 136 136 136 140 140 141 141 141 142 143 144 145 151

2.

Oculomotor fibres 2.1. Introduction 2.2. Recognition of motor fibres 2.3. Inputs on to the oculomotor fibres 2.4. Detailed account of the oculomotor fibres 2.4.1. Position-sensitive fibres 2.4.2. Eye withdrawal fibres 2.4.3. Optokinetic fibres (clockwise and anticlockwise)

151 151 152 152 153 153 156 157

General Discussion

163

References

165

127

VISUAL

PROCESSING IN THE ROCK LOBSTER (CRUSTACEA) BARBARA YORK

Department of Physiology and Biochemistry, University of Southampton, Southampton SO9 3TU

and C. A. G. WIERSMA Division of Biology, California Institute of Technology, Pasadena, Calif. 91109, U.S.A.

Introdnction Over the last 15 years Wiersma and his coworkers have made an extensive study of the visual systems of crustacea. These systems have been used to look at (a) how sensory information is integrated by interneurones, and (b) how integrated information is used to control eye movement and position. This review is mainly confined to findings in the rock lobster. The value of these studies has been expressed as follows: “More than in any other sense organ, eyes serve much the same purposes for all animals which have them. As a consequence, similar types of integration of input are indicated, and will result in output patterns which also show considerable similarities. To give one example of the latter; rapidly approaching large objects give rise to flight in many species. Even if such similarities are found to be based on quite different methods of central processing, which seems unlikely, solving the functional relationships in one group will contribute greatly to understanding the types of problems with which all systems have to deal” (Weirsma, 1967). The review is divided into two sections. Section 1 describes the interneurones of the optic nerve. Section 2 describes the oculomotor system. It is not intended to be a complete account of the crustacean visual system but focuses on the work carried out by Wiersma and his colleagues.

1. Optic Intemeuronea

Before describing the activity occurring in the optic nerve of the lobster, the structure of the eye will be described briefly. 1.1. THE STRUCTURE OF THE DECAPODCRUSTACEAN Eye The eyes of decapod crustacea are compound. In these eyes light is received by a large number of units called “ommatidia”. Figure 1 shows the structure of a single decapod ommatidium. Each ommatidium possesses a lens which is situated on the outer convex surface of the eye. The rest of the ommatidium consists of (a) a “light guide” system and (b) transducer cells which convert the light energy received to electrical energy. As shown in Fig. 1 there is a crystalline cone made up of four cells underlying the transparent lens. Under this is a crystalline thread of high refractive index. This thread ends on the rhabdomeres which make up the rod-like central rhabdom. Each rhabdomere is comprised of a number of projections from the inner surface of a retinula cell. The projections consist of a series of plates of parallel tubules containing the visual pigment. Their arrangement in the crab is shown in Fig. 2. There are seven retinula cells, arranged around the ommatidial axis, in decapod crustacea. Axons from each retinula cell lead down to the optic lamina where they make a multiple series of connections with the ganglion cell and other units in this layer. 129

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FIG. I. Ommatidium of a decapod crustacean in longitudinal section.

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Fro. 2. Structure of the rhabdom in a decapod crustacean retina.

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131

Light entering the lens probably passes via the cone, down the crystalline thread by internal reflection to reach the rhabdom. Because of the distance separating the cone and rhabdom these eyes are known as "superposition" eyes, as opposed to "apposition" eyes where the cone ends on the rhabdom. (It has been suggested by Horridge (1968a) that the advantage of the "superposition" eye, which is possessed mainly by nocturnal forms, is that the extended pathway caused by the crystalline thread allows an increase in the lightcatching area since cones placed at a greater radius from the rhabdomes can be larger.) Pigment cells surrounding the crystalline thread control the sensitivity of the eye. In the light-adapted eye the pigment migrates towards the thread and in the dark-adapted eye the pigment is withdrawn. The light arriving at the rhabdom is absorbed by the visual pigment arranged on the tubules of the rhabdomeres. The chemical processes following light absorption lead to a depolarization of the retinular cells from which the rhabdomeres project. Such a depolarization or "generator potential" has been measured, for example, in the retinular cells of the crayfish (Glantz, 1968). The visual information leaving the retinular cells is then processed by four optic ganglia: the optic lamina, medulla externa, medulla interna and medulla terminalis, as shown in Fig. 3. It is not yet known in crustacea whether transmission from the retinular cells to the lamina is by spike potentials or by electrotonic spread. A variety of synaptic connections existing in the optic ganglia have now been demonstrated. A detailed study of possible connections in the optic lamina of the lobster Homarus vulgaris has been made by Hamori and Horridge (1966 a, b) by morphological studies of the types of synapse present. A very complex network with many types of connections is suggested by these findings.

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FIG. 3. The optic ganglia of decapod crustacea.

1.2. THE INTERNEURONES OF THE OPTIC NERVE

The peripheral optic ganglia are connected to the protocerebral lobes or midbrain by the optic nerve, often called the optic peduncle. This nerve which runs along the eye stalk of stalk-eyed decapod crustacea is thus a central tract rather than a sensory one, consisting nearly completely of interneurones rather than primary sensory neurones. Some of these interneurones carry complex visual information from the optic ganglia to the midbrain. Others carry information to the optic ganglia from the rest of the body. Finally there are multimodal interneurones carrying information to and from the "midbrain" (see any of the many papers listed below) which includes both visual and other information (see summary Fig. 4). The great value of the decapod crustacean optic nerve for investigating information processing was discovered by Wiersma and his colleagues in 1955 during work on a number of species, although the first reports of the work were not published until much later (Waterman and Wiersma, 1963; Waterman et al., 1964; Wiersma et al., 1964; Bush et al., 1964). Besides providing such a variety of interneurones, the decapod optic nerve preparation has two other advantages:

BARBARAYORKAND C. A. G. WIERSMA

132

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(a) Recording techniques are simple. Good extracellular signals from single units can be obtained by introducing an insulated steel needle into the intact nerve by hand. Splitting the nerve is not necessary. (b) The hard carapace of these crustacea provides a good anchorage for attaching the base of a recording needle. This allows chronic implantation, and thus the activity of a single unit can be followed in the freely moving animal for several days or even weeks. 1.3. FIBRE LABELLING A systematic study of the optic nerve interneurones has shown that individual neurones are readily identifiable from animal to animal. Each neurone has its own unique properties in terms of behaviour and receptive field, and in its location in the nerve bundle. A system of code-numbering each fibre according to its type of response and receptive field has been developed for the crayfish, crabs and lobster. Thus, for example, a large fibre responding to jittery movements over the whole homolateral eye's field and to touch o f the whole homolateral body half in the lobster is known as LO 19. The observations made on LO 19 on various days and in different animals can then be compared to get an idea of the plasticity of the response of this fibre. It is certain that there is not a scattered group of LO 19 fibres, but only one, since the neighbouring units which appear in the same lead are fairly constant for any named fibre. New fibres are "established" after five good findings. 1.4. IDENTIFICATION OF FIBRES

The following criteria are used to identify each interneurone: (i) Types of input; e.g. visual: fast movement, jittery movement of a black target, sustained response to light, and mechano-receptors: hair responses, joint responses. (ii) Receptive fields of sensory inputs; excitatory (ERF) and inhibitory (IRF) receptive fields (see Fig. 5).

VISUALPROCeSS~GIN THERock LOeSTER(CRusTACEA)

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FIG. 5. Visual fields of (a) eight rim fibres and (b) three circular field fibres with twelve small mid-fieldfibres and four quadrant fields in the rock lobster. (iii) Habitation rate; phasic or tonic fibres. (iv) Fibre size, as indicated by signal size and ease with which the signal is lost. Figure 5 shows the shapes of the receptive fields found so far for lobster visual interneurones. Note how the fields are divided up along the horizontal and vertical axes of the eye, although the ommatidial lenses are aligned diagonally. Another interesting fact is that in the lobster there appears to be three rather than one "maculae", i.e. more detailed information from fibres with smaller receptive fields is obtained at the centre, midback and midfront areas than other parts of the eye. This is probably because the eye's surface receives input from a field of nearly 180 °. Rf size varies from 10° to the whole eye. 1.5. INTERNEURONEINPUTS These can be summarized as follows (see Fig. 4). (i) (ii) (iii) (iv) (v)

Visual; light level, target movement, stationary contrasting targets. Mechanical input: halts, joints. Statocyst input (see p. 142). Excited state. Other inputs reflecting the "state" of the animal.

In cases (i)-(iii) inputs can be excitatory or inhibitory, and can arise from the homolateral, heterolateral or both sides of the animal. Some comment must be made on inputs (iv) and (v). "Excited state", which will frequently be mentioned, is recognized as a state of the animal in which motor activity suddenly increases. The legs and other parts of the body show movements for periods varying from a few seconds to some minutes. Such a state is accompanied by a large change in the reactivity of some optic interneurones. The excited state may occur spontaneously but can easily be triggered by mechanical or strong visual stimuli. Rowell (1971) has shown that in the locust, motor output is not necessary for the change in reactivity caused by excited state. As for input (v) it is certain that there are other inputs, besides excited state, which modify the activity of some optic interneurones. A fibre may suddenly become more active in the absence of excited state, for no apparent reason. At times the fibres could be said to he "paying more attention" to the stimuli presented. Units responsible for such modifications to the optic interneurones have not yet been found. They may well be too small for our recording techniques, but even if they were found, it would be difficult to prove their function. Circadian rhythms have been found in some visual fibres of crayfish (Arechiga and Wiersma, 1969), but probably such long-term changes are hormonally mediated.

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BARBARA YORK AND C. A. G. WIERSMA

1.6. CLASSESOF INTERNEURONES A general summary is given below of fibre classes found in the optic nerve of the rock lobster, together with their approximate relative size and habituation rate. (Relative size is estimated by signal size and by the ease with which the signal is lost on moving the recording needle.) In general members of each class, differing only in receptive field, run together in the nerve. (Figures in parentheses refer to detailed sections on these optic neurones, pp. 136-151.) (a) Primary hair fibres from the dorsal carapace. Size: medium-small. Habituation rate (for repetitive stimulation): absent. (1.10.11 (a)) (b) Sustaining fibres responding to light-intensity changes and levels. The firing rate increases with increasing light intensities. Size: medium-large. Habituation rate: slow. (1.10.1) (c) Dimming fibres responding to light-intensity changes and levels. The firing rate decreases with increasing light intensity. Size: small. Habituation rate:slow. (1.10.2) (d) Jittery-movementfibres responding to irregular movements of a black target. Size: medium-large. Habituation rate: medium. (1.10.3) (e) Medium-movement fibres responding to targets approaching the eye at a medium speed. Size: medium. Habituation rate: slow. (1.10.4) (f) Fast-movement fibres responding to very rapid, sudden movements of black targets. Size: large. Habituation rate: fast. (1.10.5) (g) Unidirectional movement fibres responding to black or white targets moving at moderate speeds in one direction only. Size: medium-small. Habituation rate: medium. (1.10.8) (h) Light-movement fibres responding to moving light sources travelling at medium speeds. Size: medium-small. Habit uation rate: medium. (1.10.6) (i) Space-constant fibres including members from groups (b) to (h) and possibly (j). The receptive field is such that only visual stimuli in the part of the eye's visual field which looks upward (relative to gravity) is effective (see later). (1.10.7) (j) Seeingfibres responding to both moving and stationary black and white targets. Size: medium-large. Habituation rate: medium-slow. (1.10.10) (k) Mechanoreceptorfibres responding to hair and/or joint stimulation on various parts of the body. No visual input. Size and habituati on rate are vari able. (1.10.11 (a)) (1) Multimodal fibres responding to both visual and mechanical inputs. Visual inputs can be identical to that of groups (d), (f), (g) and (j). (1.10.10; 1.10.1 l(b)) (m) Activity fibres responding to changes in the level of excited state in the animal. Onset of excited state increases firing. Crayfish and crabs have a similar set of optic fibre classes (see Table 4). (1.10.11 (c))

(i) (ii) (iii) (iv)

1.7. POSSIBLEINFORMATIONTO BE OBTAINED FROMTHE PREPARATION What types of visual and mechanical information are coded. How this information is coded. What types of inhibitory influences are present. How these inhibitory influences are used by the nervous system.

VISUAL PROCESSING IN THE R O C K LOBSTER (CRUSTACEA)

135

(v) What factors affect the reactivity of interneurones. (vi) How much computing is "in parallel" and how much "in series" (see Fig. 6). (vii) What are the possible outputs of the various interneurones. A fair amount of information has been obtained about points (i)-(vi). Further work is needed to get more information about point (vii). As far as (vi) is concerned, it would seem that in the decapod crustacean nervous system, most computing is in parallel. This means that a small field fibre does not serve as an input to a similar overlapping large field fibre. Instead they arise separately and run together in the optic nerve. Also there appears to be no relationship between the activity of a fibre which responds to jittery movements over the whole eye's field, and a fibre with the same visual behaviour but also mechanoreceptive input. Again it seems that these fibres arise separately. In contrast, from the work of Hubel and Wiesel (1965) on the cat's visual pathway, it appears that here computing is mainly in series (Fig. 6). Lobsfer

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(Panulirus interruptus Randall). These animals were stored in a holding tank kept at 14°C. Storage for more than a month appeared to have no detrimental effects. They were exposed to a 12-hr light/dark cycle. During recording the animal was suspended in air from a clamp, but kept moist by a cloth wrapped around it. Single unit activity was obtained from the optic nerve by inserting an insulated, electrolysed needle in one of three positions, as shown in Fig. 7. For a so-called "low" lead, the needle was pushed through the soft frontal membrane between the eyes. A peripheral lead was obtained by pushing the needle through a soft membrane on the eyestalk. Finally a high lead was occasionally obtained by pushing the needle downwards from the top of the frontal membrane. The eye was never immobilized but could move freely in its socket.

136

BARBARAYORK AND C. A. G. WIERSMA

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A wide variety of visual and mechanical stimuli were presented to the lobster. One way of presenting visual targets was to suspend the lobster in the centre of a rotating drum on the walls of which targets could be positioned at various heights. The drum could be rotated around the lobster at a wide variety of speeds. Black and white targets as well as black and white stripes were used. The drum interior was grey. Moving black and white hand-held targets were also used. Light-sensitive units were investigated with a hand-held light 1.7 mm in diameter and by altering the intensity of an overhead light continuously from 0 to 20 foot-candles. Mechanical stimulation to body hairs was applied with a horse-hair brush. Appendage joints were moved by hand. To carry out chronic implantation a hole was drilled through the carapace between the two large horns on the head. A recording needle was placed through this hole and adjusted by hand until it penetrated the optic nerve. It could then be fixed in position with a fast setting epoxy which also acted as insulation. After implantation the animal could move freely in a tank of sea water. This technique was useful for establishing whether fibre behaviour observed in restrained animals was physiological. It was also useful for observing if a fibre activity is associated with certain behaviour patterns. 1.9. EXPERIMENTALPROCEDURE Open-ended experiments were performed. That is, experiments were not designed such that only one type of fibre and one experimental procedure was used. Instead all good clear units obtained during recording were carefully studied with regard to their range of input, excitatory and inhibitory receptive fields, etc. In this way a picture was gradually formed of the types of information carried by a large cross-section of the larger fibres in the optic nerve.

1.10. OPTIC INTERNEURONES 1.10.1. Sustaining Fibres (SuF's) The behaviour of this group of fibres is the simplest shown by the visual fibres of the optic nerve. For a detailed account of these fibres in rock lobster see York 0972). They usually respond to a light source in their ERF by a maintained discharge roughly proportional in frequency to the intensity of the light. They give a high-frequency burst of spikes when the light is turned on but gradually adapt to a lower frequency with a maintained intensity change. Twenty-five homolateral and one heterolateral SuF's have now been established in the rock lobster. Their receptive fields vary in size from the whole eye to "small" fields approximately 10° across. (i) Response to a maintained change in light intensity The response of a sustaining fibre can be of two types in the rock lobster. In the first type the steady-state firing frequency is roughly proportional to the prevailing light intensity. A new firing rate is established rapidly after a change in light intensity, remaining stable for

137

VISUAL PROCESSING IN THE R O C K LOBSTER (CRUSTACEA)

30 min or more (Fig. 8a). This is the most common response. Such a response is also shown by SuF's of crayfish. However, in some cases there is a gradual continual drift towards a new firing level over a period lasting for many minutes (Fig. 8b) after the initial burst following an intensity change. Here the new stable rates are very similar over a wide range of light intensities. Thus such sustainers are poor indicators of light intensity. Both extreme types of response and a continuous spectrum of intermediate ones were shown by named fibres on different occasions. They therefore appear to be characteristic of the state of the animal or eye rather than representing differences between individual SuF's. ao- (a) IB 16 14

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(ii) Response to changes in light intensity All SuF's always show large changes in firing frequency when the light falling on their receptive field is changed (Fig. 8). An interesting property of these units is that in lobster, crabs and crayfish they "follow" shadowing of their receptive field, under conditions of diffuse light despite the very small changes in light intensity involved. Such shadowing is followed to frequencies of 15 to 20 per second, resulting in a series of short bursts (Fig. 9). It was of interest that in chronically implanted lobsters submerged in sea water, turbulence of the water's surface was a sufficient stimulus to cause a large response in SuF's, since this stimulus might frequently be present in the animal's natural habitat. Studies on these lobsters in the open sea showed that they avoided turbulent water; this is possibly a consequence of the resulting strong stimulation of the sustaining fibres (Lindberg, 1955).

BARBARAYORKANDC. A. G. WmRSMA

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(iii) Inhibitory input The SuF's are inhibited by light outside their receptive field. In the lobster, but not the crayfish, the distance between the inhibitory light source and the receptive field influences the magnitude of the inhibition (Fig. 10). (iv) Influence of excited state and circadian rhythms The firing frequency of the SuF's can be affected when excited state occurs. During "excited state" the animal makes movements of the legs and other appendages lasting from a few seconds to more than a minute. During these states the discharge frequency in response to light is increased. In the crayfish, but not in the lobster, the response of SuF's to a flash of light shows a clear circadian variation (Fig. 1 l). Probable hormonal influences are responsible (see also para. (vi)).

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FIG. 12. "Light bursting" discharges from the sustaining fibre LO 27 1 min after an increase in light intensity. (A) Response to 8 foot-candles after light adaptation. (B) Response to 8 foot-candles after dark adaptation. Time base: 1/I0 sec.

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FIG. 16. Response of a dimming fibre in crayfish to (A) light dimming (B) shadowing at 10/sec. Upper records: extracellular record, Lower record: light level. Time base: A 1 sec, B 1[60 sec.

FIG. 18. Discharges of a medium movement fibre to an object approaching the eye repeatedly at different speeds. (A) slow approach, (B) medium-fast approach, (C) Fast approach. Lower beam obtained by photocell. Time base: 1/60 see.

VISUAL PROCESSINGIN THE ROCK LOBSTER (CRUSTACEA)

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(vi) Dark discharges and dark bursting Although the SuF's signal information about light intensity, they often show discharges in total darkness. The frequency of these discharges can equal or even surpass that of firing in the light. However, they are not a permanent feature of any one fibre since a fibre was noted to show dark discharges on one day but nearly none a few days later. In the crayfish, but not the lobster, these dark discharges show a circadian rhythm (Fig. 14). The activity increases during the period of day which was dark during light/dark entrainment in both animals. It is probable that hormonal mechanisms control this rhythm. In the lobster the dark discharges can take the form of a remarkably regular bursting (Fig. 15A) at 8-9/see for all individuals. The bursting frequency is independent of the number of spikes per burst. In multi-fibre leads the SuF's often burst in phase. In contrast to light discharges the dark bursting can be inhibited by excited state for several seconds (Fig. 15B). Such dark bursting was never seen in implanted animals and thus may not normally occur in the unrestrained animal. '

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FIo. 14. Circadian rhythm of spontaneous activity in constant darkness of a sustaining fibre of crayfish. At left, hour at which 10-min sample was taken. (vii) Possible outputs Obviously the SuF's convey information about light intensity to the midbrain. However, owing to the variation in responses shown on different occasions, it is difficult to decide what features of the responses can be used by the nervous system and what is rejected as noise. In the lobster the SuF's do not appear to indicate the absolute level of the prevailing light intensity but only changes in light intensity. This is obvious from the fact that in some preparations the discharge rate in the dark can be equal to that in light, and that the steadystate firing rate was about the same over a wide range of intensities in some preparations. It is uncertain whether the dark discharges can be regarded as "noise". They are not restricted to SuF's but are also seen in movement fibres. Perhaps the pattern rather than frequency of impulses is important here in deciding how or if the information carried by the SuF's is used by the lobster. The functional significance of these fibres can be postulated. They may well serve as input sources for certain motor fibres to the eye muscles (York et al., 1972b). Experiments in the open field suggest that conditions which could lead to a high SuF firing frequency such as bright light or turbid water are avoided by rock lobsters (Lindberg, 1955). Also both rock lobster and crayfish in the laboratory show an excited state when the recorded SuF firing

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BARBARA YORK AND C. A. G. W m R S M A

frequency is high. Thus SuF input may well have an influence on locomotor activity. This correlates with behaviour during light exposure. When the light in the aquarium was of intermediate intensity, the lobsters clustered in groups in the corners of the tank, whereas the crayfish did not. At low light intensities the lobsters also remained dispersed.

1.10.2. Dimming fibres These fibres are inhibited by a light source in their receptive field. In contrast to SuF's their firing frequency is inversely related to the prevailing light intensity. It is highest in total darkness. On decreasing the light intensity there is a burst adapting to a new increased frequency (Fig. 16A). From studies on crayfish it appears that light outside the receptive field increases the firing frequency, as does excited state. Like SuF's they follow fast shadowing of the eye in diffuse light (Fig. 16B). However, findings of these fibres are comparatively rare. They appear to be of small diameter since their signals are small and are lost by very small movements of the recording needle. Also since they are rarely found without larger SuF signals being present they are very difficult to study.

1.10.3. Jittery movement fibres (i) Response to movement These fibres respond to black targets with a burst of impulses when the targets first enter the fibre's receptive field. Continued smooth movement in the same direction elicits no further response. However, if the direction of movement suddenly changes a renewed response is obtained. A fairly continuous series of spikes results from "jittery" uneven movements providing that the motion is not too fast or slow. Target size is also of importante. Targets subtending less than 8 ° at the eye are not well "seen" and very large targets also evoke no response. White objects and moving lights are not effective stimuli and may well be inhibitory. The fibres give a short burst when the light is turned off but the "off" response habituates very rapidly. Different parts of the receptive field of a jittery movement fibre habituate independently of others (Wiersma and Yanagisawa, 1971). Figure 17 shows the response of a jittery movement fibre to a series of three black targets subtending an angle of 15 ° at the eye. The targets are arranged in a diagonal row. Each one elicits a short burst when it enters the fibre's receptive field. When the targets re-enter 75 see later the response to each target is reduced. This illustrates that the habituation is limited to the exposed part of the field, each new target giving rise to a renewed response. Habituation of the fibre itself is not apparently involved. "T"

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VISUAL PROCESSINGIN THE ROCK LOBSTER(CRUSTACEA)

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(ii) Modulation of input Unlike the sustaining fibres these fibres are not greatly affected by the excited state. The responsiveness of any one fibre is very variable. Dishabituation appears to take place at certain times for no obvious reason. For example, a target may excite no response at all from a habituated jittery-movement fibre. Then suddenly the target becomes effective despite the fact that the stimulus has not changed. How this sudden increase in "attention" occurs is completely unknown. As mentioned later it is seen in many fibres. There is some evidence that jittery-movement fibres can be inhibited by input to the contralateral eye. For example, the ipsilateral space-constant jittery-movement fibre (see section 1.10.7) appears to be inhibited by activity in the space-constant fibre of the contralateral eye. A second type of inhibitory influence on jittery-movement fibres has been found in the crayfish (Yamaguchi, 1967). It may well exist in the lobster also. Jittery-movement fibres fail to respond to suitable stimuli during active or passive eye movement. Such a process would allow the animal to distinguish between movements of an object and movements of its eye which would lead to apparent motion of its surroundings. Some indication of where the inhibition takes place has also been obtained. If a small object is moved near the eye all the while that the eye is moving, it still elicits a strong reaction as soon as the eye movement stops. Normally the fibre would be habituated by such repeated stimulation. Hence the site of inhibition must be at or precede the locus where habituation occurs. 1.10.4. Medium-movement fibres Medium-movement fibres respond best to objects approaching the eye. Very little habituation is shown by these fibres to black and white objects repeatedly approaching the eye at medium speeds, as shown in Fig. 18. Receding objects do not elicit a response. Strangely enough the fibres usually respond rather poorly to similar targets moving parallel to their visual field. Fast and slowly approaching objects are also poor stimuli. The fibres show a response to large changes in illumination. However, they do not respond to an approaching light source. These units show no change in activity with the onset of excited state. However, they appear to be under central control of some type. Often when the response to a repeatedly approaching object has waned, it will suddenly become dishabituated again for no apparent reason. 1.10.5. Fast-movementfibres These are exceedingly difficult to study. This is not because of their size (they appear to have a very large diameter) but because of their extremely fast habituation rate. For this reason they can be termed "novelty" fibres. They respond to a rapid sudden motion of a large black target with one or a few spikes, after which they often show no further activity for several minutes. Thus determination of receptive field and the effect of excited state is very difficult. In view of their large diameter, which will allow fast conduction, and the specificity of their response, it seems likely that these fibres are involved in bringing about startle reactions. Experiments on chronically implanted animals support this view, e.g. LO 59 which responds to fast movement over the whole homolateral eye or sudden touch of the homolateral side. LO 59 always fired when the startle reaction was assumed, although its firing was not always accompanied by this reaction. 1.10.6. Light-movement fibres This group of fibres is specifically triggered by moving lights travelling at moderate speeds (around 4°/sec). Slow and rapid motions are not effective. White targets are also ineffective unless they are strongly illuminated. The fibres also respond with a short burst to "light on" and will "follow" a stroboscope light up to a high frequency (15-20/see). This "following" results in a higher discharge frequency than that elicited by a moving light. Above a frequency of 15 to 20/sec the firing pattern becomes disorganized.

142

BARBARAYORK AND C. A. G. WIERSMA

Excited state has no significant effect on these fibres. The fibres are small, however, and the total number of findings is low relative to many other fibre types. What useful information is carried by this group of units is hard to speculate. One stimulus situation to which they might react is moving light-giving organisms. 1.10.7. Space-eonstant fibres These fibres were first described in the crayfish (Yamaguchi and Wiersma, 1965). This is not really a separate class of fibre. Instead it includes members of various fibre classes (e.g. fast, jittery movement fibres, sustainers) which all have an unusual type of receptive field in common. They are located close together in the optic nerve, so that signals from more than one type of fibre, e.g. jittery and fast-movement fibres, may be found in the same lead. Their receptive field changes with the position of the animal's body. These changes are such that the fibres select information only from the direction of the sky, i.e. from a fixed direction in space. Some fibres have the whole eye as a potential receptive field. If the animal is tilted on its side so that the whole eye looks upwards towards the sky, then an appropriate stimulus will evoke a response anywhere in the eye's visual field. If, however, the animal is held so that its head is tilted downwards and its tail is in the air, then only the back (posterior) part of the eye looks towards the sky. Under these conditions only this posterior part of the eye is responsive to suitable stimuli, and the rest of the eye is not. The way in which the field changes as the animal's body position is changed is illustrated in Fig. 19. D

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Other fibres with space constant properties have been found with potential quadrant fields instead of whole eye fields. Since these display unidirectionality also, they will be described separately in the next section. Space-constancy is not due to the fact that the amount of light falling on the upward-looking part of the eye is usually greatest. Instead, at least in crayfish, there is good evidence that the receptive field is modified by inputs from the statocysts. The statocysts are organs located at the base of the antennules, which indicate body position relative to gravity. They consist of statoliths (calcium carbonate "stones") contained in sea-water-filled chambers lined with sensory hairs (Fig. 20). As the body position changes the statolith stimulates a new set of hairs since it stays at the lowest part of the chamber under the influence of gravity. For further information on this organ see Cohen (1960). If the statocysts are destroyed the space-constant fibres lose their inhibitory input from the statocysts. As a result the receptive field becomes the whole eye, regardless of body position. Few similar experiments have been performed in the rock lobster and their results are inconclusive. It is possible that clues of body position could come from the leg joints and antennal joints instead of the statocysts, or at least provide an accessory input. It is certain that such inputs are used by the oculomotor fibres to indicate body position (see p. 153).

VISUAL PROCESSING IN THE ROCK LOBSTER(CRUSTACEA)

143

Fio. 20. The statocyst of the lobster.

Space-constant fibres are the only ones found so far that indicate target positions in a fixed point in space rather than target position relative to the animal's body. Thus when the animal is climbing, it can tell what events are occurring "above". A possible output of the jittery-movement space constant fibre is nicely illustrated in the crayfish. The crayfish can be held in the hand and then tilted into various positions. If then a jittery movement is presented to that part of the eye which is looking "upwards" the crayfish raises its claws in a "defence" posture. Jittery motion below the horizon is ineffective. Thus it appears that one of the inputs initiating this reaction may be the jittery-movement space constant fibre for the whole eye. 1.10.8. Unidirectional movement fibres with and without space constant features (i) Simple unidirectional fibres Two fibres responding to horizontal movements have been found which show pronounced directional preference. Both have the total middle eye surface for their receptive field. One sees mainly back-to-front movements and the other front-to-back. They respond to both black and white targets. They also show a rather short after-discharge when a moving target is stopped in their field. The after-discharge is, however, much shorter than that shown by the seeing fibres (see section 1.10.10). They prefer moderate speeds of movement (about 4°/see) to slow or fast ones. Figure 21 shows the response of the unidirectional movement fibre LO 71 to movement of a black target. Figure 21 b illustrates the very slight after-discharge on stopping movement in the preferred direction.

5sec FIo. 21. Unidirectional movement response of a lobster interneurone. (A) Target movement from the front to back of eye (non-preferred direction). (B) Target movement from back to front of the eye (preferred direction). Target speed 4°/see. Time base: 5 sec. (Upper trace--target speed and position) Each dot represents a spike.

144

BARBARAYORK AND C. A. G. WIERSMA

(ii) Complex unidirectionalfibres Besides these relatively "simple" fibres, there are other unidirectional fibres whose behaviour is much more complex. All of these respond to vertical movements. Their fields lie to one side or the other of the horizontal midline of the eye. They all appear to have what could be called a "trigger zone" in the midline. This is demonstrated by their capacity to respond well to vertical target movements across their field only if a good response is elicited as the target crosses the midline. Once their "attention" is engaged, continued movement across the receptive field gives a continued response. If the target travels across the midline too fast or too slow and thus does not elicit a good response here, then continued movement into the field is relatively ineffective. Three of these fibres are excited by movements starting at the horizontal eye axis and see motions from the middle to the bottom of the eye. They are not space constant. A second set respond to upward motions and are space constant, i.e. the receptive field changes with the position of the animal's body. As described in the previous section, only that part of the field which looks upwards (away from gravity) is responsive. However, another interesting feature of these fibres is the change in the directional preference to movement with body position. The fibres respond only to movements away from the direction of gravity. Take, for example, a fibre with a potential receptive field of the back upper quadrant. When the animal is in a normal position, motions from the bottom to the top of the eye are effective stimuli. However, when the animal is in a "head-down" position with its tail in the air, only movements from the front to the back of the eye are effective, since this direction is now away from that of gravity. Thus the movement preference is fixed in space but not relative to the eye. Despite the complexity of these reactions, the behaviour of these fibres is very repeatable. 1.10.9. Multimodal unidirectionalfibres There are two interesting unidirectional fibres which are multimodal. Both have eye-half receptive fields. One responds only to movements in the front half of the eye when the target moves from the middle of the eye to the front rim. The other responds only to targets moving in the back half of the eye from the mid-eye to the back rim. This unidirectionality is shown in Fig. 22. The 15 ° black target first moves in the "null" direction which elicits a poor response. On reversing direction of movement a pronounced response is seen despite the fact that some habituation may have occurred. The mechnical input for both fibres is from the antennal joints. Even when the eye is capped, antennal movement stimulates both

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VISUAL PROCF~INO IN THE ROCK LOaSTn (CRusTACEA)

145

fibres. The front-eye-haif fibre responds best to antennal movements from back to front, while the back-eye'half fibre prefers movements in the opposite direction. These fibres habituate quite strongly to moving targets. It is interesting that a certain behavioural pattern disappears when habituation occurs; frequently the lobster points fairly accurately towards travelling targets with the tip of its antenna. This behaviour has been termed the "pointing reaction". This pointing habituates when the multimodal unidirectional fibres habituate. The possibility that these two fibres may be the command fibres for this reaction is considered in the discussion (see also p. 150). 1.10.I0. Seeing fibres (SeF's) A detailed account of these fibres has recently been published (Wiersma and York, 1972). They have been found only in the rock lobster so far, but may well be present in crayfish. The seeing fibres (SeF's) differ from all other known classes in that they show a prolonged response to stationary contrasting objects. (i) Receptivefields Although the most conspicuous part of a SeF's visual receptive field is excitatory, at least some fibres also have an inhibitory receptive field (1RF). The excitatory receptive field (ERF) can be divided into two areas. One area, the "seeing" area, responds to both moving and stationary objects. The less sensitive second area responds only to moving objects. In the horizontal plane at least, the fields of most fibres show a "seeing" area flanked on both sides by a "movement" area. For technical reasons vertical movements have been tested only roughly. The total ERF's of all the SeF's so far established are shown in Fig. 23. UNIMODAL HOMOLATERAL ~l~

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As shown by this figure, most fibres have no mechanoreceptor input (unimodal). Most of the fibres with mechanical input (multimodai) are bilateral. Input is mainly from the legs and head appendages. However, the response of the unimodal fibres is influenced by movements of the antennules and antennae as described later. (ii) General properties These fibres have a fairly large diameter and so they are easily found in most preparations. They respond to both black and white targets above a 2 ° angle. Size is not very important as long as the target is between about 4 ° and 15°. However, although black targets of 15°

146

BAI~ARA YORK AND C. A. G. WIERSMA

are generally more effective than 4 ° ones, the reverse is true for white targets. This will be discussed in para. (v). The shape of the target is definitely of no importance as, for example, a square and star shape of the same size and colour were equally effective. This means that one SeF alone cannot contribute to " f o r m " vision. Medium speeds of target movements are more effective than fast or slow ones, as shown in Fig. 24. Fast speeds give rise to a short burst of spikes (a), slow speeds elicit an irregular array of spikes (c), but medium speeds of about 4°/sec (b) cause a sustained discharge. Similar effects of target speed on response have been seen in certain neurones in the optic tectum of the toad (Ewert and Borchers, 1971). Although the SeF's respond fairly specifically to contrasting targets, they do also respond to large changes in background illumination. The fibres can give both " o n " and "off" responses, though the "off" response is stronger and shows less habituation. The SeF's, like most other fibres, show a background spontaneous discharge. This is more prominent in fibres with large receptive fields than those with small ones. Darkness sometimes increases this discharge, while sudden light inhibits it.

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(iii) Directionality SeF's can show some directionality in that target movement across their E R F in one direction may excite more impulses than movement in the opposite direction. The effect is much weaker than that shown by true unidirectional fibres (see sections 1.10.8 and 1.10.9). Only horizontal movements have been used so far. The number of observations of this directionality are limited. However, from these it appears that the preferred direction is constant for any one fibre, and does not change from animal to animal. In certain cases the difference in the number of impulses elicited for the two directions was as much as 25 %. (iv) Habituation Habituation to moving targets is much slower than that shown by jittery movement fibres. In general the "seeing" areas of the E R F habituate to movement more slowly than the less sensitive "movement" areas. Like the jittery-movement fibres, the habituation is limited to the exposed part of the field, i.e. it is not an habituation of the SeF itself. The reaction of a SeF to nine target presentations at three different heights is shown in Fig. 25. After three presentations of a mid-height target considerable habituation is seen. However, the other parts of the field show no habituation until they too have been exposed to repeated presentations. In multimodal SeF's with mechanical input from the body, the same was true. Habituation to touch of one leg did not affect the response to a second leg or the visual responsiveness of the fibre. (v) Inhibition and"distraction" There are several indications that SeF's are excited by contrasting edges and dark areas, but are inhibited by bright light and white areas. (a) As previously mentioned, the response of SeF's is best to small (4 °) white targets but to large 15 ° black targets. This could well be because the contrasting edge between the

VISUAL PROCF-SSlNG IN TIlE ROC~ LOBSTER (CRUSTACEA)

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A second type of inhibition is caused by target movement outside the ERF. The areas where such inhibition is evoked are termed the "inhibitory receptive field" or IRF. Such areas are much more difficult to define than the ERF. Also stronger stimuli are generally required to evoke an effect from the IRF than the ERF. The I R F of the lower front quadrant SeF appears to consist of the upper front quadrant. As illustrated in Fig. 29 the response of this SeF to a low moving target is inhibited by a "high" target. General visual stimulation of an IRF, e.g. by hand waving, was often very effective.

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The IRF can include specific areas of the carapace or appendages. An example is shown in Fig. 30. The back rim SeF LO 131 shows no response to a target travelling through its E R F if at the same time the head is stimulated with a brush. One minute later an identical stimulus evokes a good response in the absence of mechanical stimulation. For two frontward-looking SeF's touching the abdomen was inhibitory while touching the head was not. This second type of inhibition could be described as "distraction". Stimuli occurring in certain areas outside the E R F "distract the attention" of the SeF. Such inhibition would be useful for focusing the "attention" on one event or target at a time. Thus, for example, when a strong mechanical stimulation of the abdomen occurs, the animal will be more concerned with the environment behind than in front of it, so the forward-looking SeF's are "turned off". When the animal becomes obviously alarmed, all the SeF's appear to become completely inhibited. There is also some indication from the limited number of observations on inplanted SeF's that responsiveness is reduced while the animal is walking about. (vi) "Attention" If a SeF is to respond strongly, not only must it not be "distracted" but its "attention must be attracted". Unexpected or novel stimuli seem the most effective. For example, repeatedly presenting a target travelling in one direction to the E R F of a SeF results in

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BARBARAYORK AND C. A. G. WIERSMA

150

habituation. If the target direction but not the target path is then changed, a large dishabituated response is evoked by this unexpected stimulus. Also when a b l a c k target is continuously rotated across the ERF so that it loses its effectiveness, replacement with a white target can give an unexpectedly greater response. Very slowly moving targets do not "catch the attention" of the fibre. However, the sudden appearance of a stationary one does. If a black target is suddenly placed by hand into the unstimulated ERF, it will excite a good discharge from the SeF for up to 30 sec, after an initial silence. Placing a second target into the ERF may lead to a renewed response as shown in Fig. 31. It is uncertain how much the movement involved in placing the target quickly into the receptive field contributes to "catching the attention" of the fibre. However, such a movement is not necessary to obtain a response to a stationary stimulus. A good response may be obtained on reillumination of the room if a target is placed in the ERF of a SeF during darkness (see Fig. 32). It is as though the appearance of a target, which was not present before, has been noted. In the absence of a target slight inhibition is observed on reillumination (Fig. 32d). However, the period of darkness must not be longer than 30 sec. This period appears to be the "memory span" of the fibre during which it can remember that a change in the field has occurred. After longer periods of darkness there is no response to a new target on reillumination. (vii) Pointing reaction When a single target is moved around a lobster, the point of the antennal flagellum can follow this movement surprisingly accurately over a 90 ° arc or more. There appears to be antennal joint input to the SeF's since such a movement is accompanied by increased activity in the SeF's. However, there is also evidence that the SeF's serve as inputs for the antennal pointing reaction, e.g. habituation of the SeF's is accompanied by a parallel habituation of the pointing reaction. Thus a positive feedback loop may exist; a moving target excites the SeF's which stimulate pointing. The antennal movement then excites the SeF's further. Two multimodal unidirectional fibres described in section I. 10.9, pp. 144-145, might be the command fibres for the pointing reaction (Wiersma and Yanagisawa, 1971). Again the habituation of these fibres is often paralleled by habituation of the pointing reaction. The seeing fibres could then be a major modifying influence on these command fibres, p r o v i d i n g the accuracy shown in the pointing reaction (see Wiersma and York, 1972).

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FIG. 35. Statocyst input onto a tonic eye-down fibre with animal in a 45 ° eye-down position. Downward arrows: antennules are rotated along their length axis bringing the statocyst openings towards the eye cup (excitatory). Upward arrows: antennules are rotated in the reverse direction (inhibitory). Time base: 5 see.

Facing page 150

FIG. 38. Effect of shadowing the ipsilateral eye on the firing of a tonic head-down fibre. Regular background discharge becomes a bursting discharge as the bursts synchronize with the shadowing. Time base: 1 see.

FIG. 39. Ipsilateral antennal input onto a tonic eye-down fibre, v antennal base back, flapellum tip up. A antennal base forward, flapollum tip down. Time base: 5see.

FIG. 40. Input from the leg joints (mainly basi-ischio) on to a tonic eye-down fibre. (A) Manipulation of ipsilateral legs. (B) Manipulation of contralateral legs: A all legs fexed, v all legs extended. Time base: 5 see.

VISUALPROCESSINGIN THE ROCK LOBSTER (CRUSTACEA)

151

1.10.11 Other fibre types (a) Mechanoreceptor fibres As in the crayfish, there is a bundle of primary hair fibres running in the optic nerve. These supply the carapace. There are also many mechanoreceptor interneurones responding to hair and joint inputs from various parts of the body. The receptive fields of these fibres may include only one appendage or the entire body. Homo-, hetero- and bilateral fibres are present. (b) Multimodal fibres This group includes a very diverse selection of fibres with both visual and methanereceptor inputs. They have been described in appropriate previous sections, depending on their type of visual input. Most multimodal fibres have "jittery-movement" or "seeing" visual inputs. (c) Activity fibres These fibres have similar properties to certain mechanoreceptor fibres, in that sensory stimulation of any area of the body often causes firing. However, the firing is present only when an excited state occurs (see p. 133). Unlike the mechanoreceptor fibres, the activity fibre discharges can outlast the sensory stimulus. Both a tonic and phasic fibre are present. These are probably inputs on to the various visual interneurones whose firing activity is altered by the onset of the excited state.

2. Oculomotor Fibres

For details of the oculomotor systems of crayfish and crab, see Wiersma and Oberjat (1968) and Wiersma and Fiore (1971a, b). Some of the work to be described for rock lobster has already been reported (York et al., 1972a, York et al., 1972b). 2.1. INTRODUCTION The oculomotor fibres innervate the muscles which move the eye-stalks of stalk-eyed decapod crustacea. They provide interesting information on how a variety of sensory inputs interact and are used to control eye movement. Approximately twenty such fibres run along the optomotor nerve in the eye stalk of the rock lobster. There are three sets of muscles which move the eye in three planes, as well as the eye withdrawal fibres. Each set consists of two opposing members. In general, eye movements caused by these muscles excepting the eye-withdrawal fibres are such as to keep the position of the surrounding visual image on the eye stable. Thus the eyes will move if: (i) the animal moves relative to the surrounding visual image, or (ii) all or part of the visual image moves relative to the animal. The three sets of muscles are named: (a) head-up and head-down fibres. (b) eye-up and eye-down fibres. (c) clockwise and anticlockwise fibres. (a) and (b) are known as position-sensitive fibres, (c) are known as optokinetic fibres. They are named after the body position or body movement which activates them most. (i) Movement of the animal If the body moves in one direction, then the eyes must move in the opposite direction to keep "fixed" on the visual surround. The position sensitive fibres cause compensatory eye movements during body movements so that the eyes still "look" in the same direction.

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BARBARAYORK A N D C. A. G. WIERSMA

(ii) Movement of the visual image If the visual surround moves, the eyes move in the same direction to "follow" it. Rotating black and white vertical stripes are very effective in causing such eye movements. These "following" eye movements are known as the "optokinetic" response. Optokinetic fibres respond very strongly to rotating stripes. Position-sensitive fibres respond more weakly. 2.2. RECOGNITION OF MOTOR FIBRES

Recording techniques are identical to those described in section 1. The motor fibres can readily be separated from the optic interneurones which run parallel with them in the eyestalk. The motor fibres give much larger signals because of their greater diameter. The individual motor fibres can be identified by their reactions to changes in body position. As already mentioned, the fibres are named after the position in which they are most active. For example, the eye-down fibre is strongly stimulated when the lobster is tilted so that the homolateral eye faces downward. It is inhibited when this eye faces upwards. Movements in the two other planes are ineffective. Thus firing frequency is unchanged if the lobster is placed with its head pointing up or down. This is illustrated in Fig. 33. It should be emphasized here that the EYE-DOWNfibre moves the eye uP. The optokinetic fibres are stimulated if the animal is rotated in the horizontal plane in the presence of a varied visual surround.

"30

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-1:55

-90

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0 I

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FIG. 33. Activity in a position-sensitive oculomotor fibre during body movement. Plot of frequency of APs against angle of turning around length axis for eye-down fibres: - 9 0 ° = eye-down position; +90 ° = eye-up position (note hysteresis).

2.3. INPUTS ON TO TIlE OCULOMOTORFIBRES There are two main sorts of inputs on to the oculomotor fibres: (i) optokinetic (stripe movement, body stationary), (ii) inputs indicating body position. There appears to be no proprioceptive feedback from the eye on to the motor fibres indicating eye-up position. (i) Optokinetic input Rotation of the animal in front of the stripes is the main input on to the optokinetic fibres. Stripes rotating in the horizontal plane are usually equally effective. Optokinetic input on to the position sensitive input on to the position-sensitive fibres is weak and habituating. (ii) Inputs indicating bodyposition (a) Statocysts input indicating body position relative to gravity, (b) Sustainer (light-sensitive) optic interneurone input indicating daylight position. (c) Leg position indicating the tilt of the animal.

VISUAL PROCESSING IN THE ROCK LOBSTER (CRUSTACEA)

153

(d) Antennule joint input modifying input (a). (e) Antennal joint input probably involved in the pointing reaction (see p. 148). All inputs feed on to the motor fibres from both sides of the body, though the heterolateral input is always weaker, and if visual, may be absent. 2.4. DETAILEDACCOUNTOF THE OCULOMOTOR FIBRES 2.4.1. Position-sensitivefibres As described in the introduction, the position of the eye cups of stalk-eyed decapod crustacea is mainly determined by muscles innervated by the position-sensitive fibres. These muscles influence the angle at which the eyes are kept with regard to the proximal eye joint. As the animal's position changes this angle also changes in such a way as to keep the eyes in a horizontal plane, and as near as possible to their former position. Up to three fibres of one type have been found together in one lead (e.g. three head-up fibres). All fibres of each type respond similarly but with different thresholds and firing frequencies. There is a large phasic fibre with a high threshold and two smaller more tonic fibres with lower thresholds. All motor fibres are excited by the excited state (see p. 133). The other inputs on to these fibres are summarized above. They will now be described in more detail. (i) Statocysts As previously mentioned the statocysts are organs which indicate body position with respect to gravity. Their structure is shown in Fig. 20. They consist of a chamber filled with sea water and lined with sensory hairs. Embedded in the hairs is a calcium carbonate stone called the statolith. Body position relative to gravity is indicated by which set of hairs is stimulated by an increased shearing force, and thus which fibres in the antennular nerve are stimulated. Rotational acceleration is also detected by the statocysts. The. receptors responsible are very thin hairs which move as sea water swirls around the statocyst chamber. For more detail see Cohen (I 960). The influence of the statocyst input on the oculomotor nerves has been carefully studied in crayfish (Wiersma and Oberjat, 1968). Figure 33 shows the effect on firing of the eyedown fibre of rotating a crayfish around the length axis in the dark; --90 ° represents the eye-down position and +90 ° the eye-up position. A hysteresis is present. Most but not all the effects of rotation in the dark were removed on bilateral removal of the statocysts. Removal of the heterolateral statocysts greatly reduced the maximum firing frequency on rotation, as seen from Fig. 34. For the head-up and head-down fibres it made no difference which statocyst was removed. However, it made a difference as to which statocyst was removed for the eye-up and eye-down fibres, since stimulation of the two statocysts had opposite effects, one being excitatory and the other inhibitory. Removal of one should thus give lack of excitation while removal of the other should give lack of inhibition. As a result, the body position for maximum discharge should change from the 90 ° to the 60° one. This is suggested in Fig. 34 although more results are needed to prove that this is the case. Similar statocysts input on to the position-sensitive fibres was present in the rock lobster. Again pronounced hysteresis was present during rotation in the dark. (ii) Antennule joint input The statocysts are located at the base of the antennules which are very mobile in the rock lobster, in contrast to crayfish. Presumably as far as the statocysts are concerned, antennule movement could not be distinguished from entire body movement. However, there is good evidence that joint receptors at the base of the antennules modify the statocyst input when the antennule but not the body moves (Schfne and SchSne, 1967). Antennule movement certainly affected the activity of the eye-up and eye-down fibres. Of course, when the antennules are moved both statocysts and joint receptors can be activated. By turning both antennules along their length axis the statocysts will be rotated

154

BARBARAYORK AND C. A. G. WmRSMA

-30

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180

-135

-90

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FIG. 34. Effect of statocyst removal. Plot of frequency of APs against body rotationangle during rotation around length axis for eye-up fibres (in darkness). Solid line: statocysts intact. Dashed line: heterolateral statocyst removed. --90 ° = eye-down position. + 9 0 ° = eye-up position.

relative to gravity. The effects of such turning was as expected. Turning the ipsilateral antennule down towards the eye excites the eye-down fibre and inhibits the eye-up one, as shown in Fig. 35. If the antennules are moved in the horizontal plane only joint receptors should be stimulated and not the statocysts. It was found that bringing the antennules towards the ipsilateral eye in the horizontal plane increased the firing rate of the eye-up fibres and inlfibited the eye-down ones whereas movements in the opposite direction had the reverse effect. It is doubtful that statocyst acceleration receptors were involved since the effect continued after movement had ceased as long as the antennules were kept deflected. Large eye movements accompanied the changes in firing frequency. Antennule joint input on to the head-up and head-down fibres was also obvious. The effect of pulling the antennules up or down when the animal was held horizontal was due to the combined but antagonistic inputs from the statocysts and antennule joints. Unlike Sch~Sne and Schrne (1967), we found the effect was variable and that the two inputs were not perfectly matched. For seven head-down fibres pulling the antennules upwards inhibited the fibres, and pulling them down excited. Here the statocyst input was stronger than the joint input. However, in two cases the opposite effects were found. Here the joint receptor input overrode the statocyst one. Both cases are illustrated in Fig. 36. In intact animals the eyes were usually found to move upwards on bringing the antennules downwards in the horizontal animal, indicating that the head-down fibres were stimulated. (iii) Visual input Two types of visual input on to the position-sensitive fibres could be shown: optokinetic and light position. Optolcinetic input. The eye-up and eye-down muscles move the eyes down and up respectively around the longitudinal axis of the body. Thus, as would be expected, the fibres innervating these muscles are influenced by stripes rotated from the top to the bottom or the bottom to the top of the eye, i.e. in the vertical axis of the eye. To study such optokinetic influences the animal was mounted head-down within a rotating drum inside which were vertical black and white stripes. The stripes then travelled over the eye's surface in either direction with a large component in the vertical axis of the eye. In about one-third of the lobsters no optokinetic input was found on to the eye-up or eye-down fibres. In the rest it was usually weak and quickly habituated. However, Fig. 37 shows an example of a fairly strong optokinetic input on to a tonic eye-up fibre. Rotating

VISUALPROCESSINGIN" THE RocI~ LOBSTER(CRUSTACEA)

155

6,

A

V

===============================================

B

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A

V

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F1o. 36. Opposite effects of antennule movement in the vertical plane on two headdown fibres from two different animals (A) and (B). (A) Lifting the antermules excites. (13) Lifting antennules one by one inhibits. A --lifting antennule, v ---depressing. Time base: 1 see.

the animal was equally or more effective than rotating the drum, although animal rotation in the dark was ineffective. This input would be useful for tracing large interesting objects moving along the vertical axis of the eye. As found for the eye-up and eye-down fibres, the optokinetic input for the head-up and head-down fibres was again weak with pronounced habituation. It was also technically difficult to demonstrate in these fibres. The stimulus used was a white half-globe with eight black stripes arranged inside as spokes. These were rotated around the axis of the eye. Perhaps this input could again be used for tracking large moving targets. Light position. The influence of daylight position on the eye as an indication of body position was often as strong an influence as statocyst input. For the eye-down fibres, light anywhere on the ipsilateral eye was inhibitory while light anywhere in the contralateral eye was excitatory. The reverse was true for the eye-up fibres. In about 20 ~o of lobsters studied this input was absent, but when present it was usually bilateral. The head-up and head-down fibres were affected by light in the front and back rim areas. For example, the discharge rate of the head-down fibres was increased when light was shone in the back rim of the ipsi- or contralateral eye, and inhibited by light in the front rims. In 30 ~o of animals this input was absent.

A

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^ Fzo. 37. Optokinetic input onto a tonic eye-up fibre (animal mounted head downward in drum with vertical black and white stripes). (A) Preferred direction (top to bottom of eye). (B) Unpreferred direction (bottom to top of eye). Time base: 1 sec.

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BARBARAYORK AND C. A. G. WIERSMA

The visual interneurones acting as inputs for this response are almost certainly the sustainer fibres (see p. 136). As described in section 1 the sustainers are the only interneurones found so far which give a sustained response to an increase in light level and follow fast shadowing up to 20/see at fairly low light levels. It is significant that such fast shadowing was also expressed in the firing pattern of position-sensitive oculomotor fibres. However, the shadowing effect was limited to the input from the ipsilateral eye (Fig. 38). Therefore for eye-up fibres the excitatory effect was influenced, whereas in the eye-down fibres the inhibitory input was influenced. This probably means that the sustainer input from the contralateral eye had to pass through an extra synapse which obliterated such bursting. The sustainer input on to the eye-up and eye-down fibres must be from a "whole-eye" fibre, while sustainers with back and front rim receptive fields must act as inputs for the headdown and head-up fibres (see Fig. 9). (iv) Antennal joint input Weak inputs are present from the antennal joints on to the position-sensitive oculomotor fibres. For an eye-down fibre, bringing the base of the ipsilateral antenna back and pointing the flagellum upward was excitatory. Pointing the antenna down and forward was inhibitory. Such an effect is illustrated in Fig. 39. Any antennal input on to the head-up or head-down fibres was very weak. This input is probably related to the pointing reaction which is described on p. 136, where the lobster points the flagellum of its antennule towards objects of interest. The antennal input described here is such as to orientate the eye towards the direction in which the antenna points. (If in fact the same input exists for active movements as for the imposed movements used here.) For example, the eye-down fibre brings the eye upwards when excited. As pointing the antenna upwards excited the eye-down fibre, the eye will be brought upwards by this antennal movement. This will result in more of the eye's surface facing an interesting object towards which the lobster points. This antennal input is certainly not involved in indicating body position. For example, in the eye-down position, the heavy antenna tends to fall downwards, yet a passive movement in this direction inhibits the eye-down fibre. (v) Leg-position input Changes in leg position, which presumably indicate the tilt of the body, influence the firing of the position sensitive fibres. Indeed Dijkgraaf (1956a, b) has noted that leg position influences eye position. As can be seen from Fig. 40, flexing the ipsilateral legs and extending the contralateral legs excite an eye-down fibre, while leg movements in the opposite direction were inhibitory. (The former leg movements would bring the lobster into an eye-down position, if the animal were on level ground.) Manipulation of a single leg caused a change in frequency of the motor fibres. All appendages from the third maxilliped to the 5th leg were effective. The leg input was a fairly strong one. It affected the high threshold phasic fibres. It also overrode inhibitory light and statocyst inputs. Presumably the interneurones responsible for this input could well be the two "Sherrington" fibres described by Wiersma (1958) in crayfish, which run in the circumoesophageal connectives, and have input from the coxobasal joints. Leg position has a weak effect on the discharge rate of head-up and head-down fibres. Occasionally bringing all legs backwards resulted in a decreased discharge rate in the head-down fibre, and bringing them forward was excitatory. 2.4.2. Eye-withdrawalfibres In contrast with most stalk-eyed species, the rock lobster has only a feeble type of withdrawal reflex, with a high threshold. This brings the eye forward and downward through a maximum of less than 45 °. Protection of the eye under most circumstances is provided by the antennal segments. Relatively few recordings have been made of motor neurons involved in the eye-cup withdrawal. Here, as in other species, the fibres are inhibited by the presence of an excited state.

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Position-sensitive oculomotor fibres : Discussion In general the inputs on to the position-sensitive oculomotor fibres serve two purposes. One group of inputs indicate body position. These allow the eyes to make movements during changes in body position such that the visual image on the eye remains fairly stable. The second group of inputs allows the eye to follow the movement of interesting objects. Into this group fall the optokinetic input, and the antennal joint input which probably orientates the eye towards moving objects when the lobster points towards them with its antenna. It is interesting that more than one input is used to indicate body position. Presumably the reason for this is that the statocyst input is unreliable, owing to the fact that the statecysts are located on the mobile antennules. The antennule joint receptors compensate for antennule movement to some degree. Light position input reinforces statocyst input, and leg position also indicates body position. These extra inputs would also be useful if the antennules were lost or malformed after a moult. However, under certain conditions it would appear that the leg input could be in conflict with the statocyst input. The input would only agree with the statocyst input when the lobster was on level ground. What happens when the lobster climbs is not known. Interaction between gravity orientation and orientation to the ground has been shown in crayfish (Stein and SchSne, 1972). Clearly further work is needed to determine the interactions between the inputs on to the oculomotor fibres under various conditions. 2.4.3. Optokinetic fibres (clockwise and anticlockwise) The inputs on to the optokinetic fibres are not identical for crabs, crayfish and lobsters. In crab (Wiersma and Fiore, 1971b) three such fibres are found; one with input from the statocyst alone, one with input from the statocyst together with visual input, and one with only visual input. Crayfish and lobster optokinetic fibres have no statocyst input. Up to four optokinetic fibres of one type have been found together in one lead in the rock lobster. All the clockwise fibres, for example, behave similarly but their threshold varies with size. The largest, phasic fibre has a high threshold. The smallest most tonic fibre has a low threshold. The optokinetic fibres innervate the eye muscles which move the eyes in the horizontal plane. They are stimulated either when contrasting targets with vertical edges are rotated round the animal or when the animal moves relative to such targets. The eyes move in such a way as to keep the position of the edges on the eye constant. (i) Response to rotating stripes The activity of the optokinetic fibres is strongly influenced by vertical rotating black and white stripes. If the animal is placed in the centre of a drum whose walls are lined with such stripes, the eyes will follow the stripes as these are rotated. The eyes can move through an arc of about 15°. After they have reached an extreme position, the eyes flick backwards to their starting point, and start following again. The saccadic flicks are called "flip-backs". The optokinetic fibres show either a gradual build up of excitation or inhibition as the stripes rotate. Clockwise movement of the stripes (or anticlockwise movement of the animal) will excite the anticlockwise motor fibres (ACM). The reverse movement will excite the clockwise motor fibres (CM). During the flip-back, the excited fibres show a sudden silence, while the inhibited fibres show a sudden burst of activity. (ii) Inputs other than visual input All fibres are excited by excited state (see p. 133). No proprioceptive input on to the optokinetic fibres has been found. Also no statocyst input on to lobster or crayfish fibres (Wiersma and Oberjat, 1968) appears to be present. (In the crab optokinetic fibres are present which are excited by rotation of the animal in the dark. Presumably there is statocyst input on to these fibres from the floating hair acceleration receptors.)

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There is a weak input on to the lobster optokinetic fibres from the antennal joints. Turning both antennae in the horizontal plane in the clockwise direction causes the eyes to move clockwise and the ACM to be excited (Fig. 41). Thus this input is similar to that on to the position-sensitive fibres (p. 156). In both instances the eyes are oriented towards the direction in which the antennae point. This reflex is probably involved in the "pointing reaction" during which the lobster points its antenna towards objects of interest. This antennal movement will then cause the eyes to become oriented towards the interesting object and thus more of the eye's surface can react to the object.

A

V

A

FIG. 41. Antennal joint input onto a tonic anticlockwise fibre. ^ anticlockwise rotation of both antennae, v clockwiserotation of both antennae. Time base: 1 sec.

(iii) Visual input-pattern requirements Although visual interneurones of the lobster can respond to targets as small as 2 ° in visual angle, the optokinetic fibres do not respond to rotating stripes of less than 10 ° width. Thus stripe width is no indication of visual acuity. It would appear that the stripe pattern is not important for a good response. All that is needed is an array of contrasting vertical edges. It was found that equally good responses were obtained to a large number of black 15 ° targets whether they were arranged randomly in the drum or if they were arranged into a number of vertical stripes. Targets moving in exactly the vertical axis of the eye have no effect on the optokinetic fibres, but as soon as a horizontal vector of movement is present, the discharge rate is affected. (iv) Visual receptive fields It appears that the whole of both eye surfaces can provide input for all CMs and ACMs. However, the exact input areas vary from preparation to preparation. Sometimes parts of the ipsilateral eye are more effective than others. Also the relative effectiveness of optokinetic input from the ipsilateral and contralateral eye vary greatly. Out of fifty-two fibres tested, twenty-four showed no contralateral input, and only nine showed really strong contralateral input. The inputs from the two eyes are additive. A single stripe ~elicits the strongest response when it is in the fields of both eyes. The variation in the contralateral input means in practice that the degree of coupling between the movements of the two eyes is also varied. If the contralateral input is strong, this means that the ipsilateral eye will automatically move when the contralateral eye only is stimulated visually. However, when there is no contralateral input the two eyes can presumably follow objects quite independently of each other. (v) Fibre firing patterns in response to stripes As described in para. (i) of this section the optokinetic fibres show a gradual build-up of excitation or inhibition as stripes are rotated in front of the eyes (see Fig. 42). The tonic fibres respond first and then the more phasic ones. If the drum is rotated in the preferred direction, until the fibre firing rate is high, and then the drum is stopped there is often no immediate decline in firing frequency. Instead the fibre firing rate may continue at the same rate for many minutes. Such after-discharge is shown in Table 1. Once the drum is turned in the inhibitory direction the firing rate falls rapidly, usually much faster than it built up during excitation.

VISUAL PROCESSINGIN THE ROCK LOBSTER(CRUSTACEA)

159

~ I ~ ~ ~ ~ ~ ~ ~ ~ t ~ ~ ~ ~ t ~ : ~ ~ t t t t ~ t ~

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FIG. 42. Bursting discharge of a tonic anticlockwisemotor fibre in response to rotating stripes. (A) Rotation in preferred direction. (B) Rotation in unpreferred direction beginning at A and ending at v. Time base: 1 see. TABLE l. AFTER DISCHARGEIN AN ANTICLOCKWIS~MOTORFIBRE Time after stopping drum (rain) 0--5 10 15 20 25 30 35 40

Frequency impulses/see 50-60 45 40 38 36 33 31 30

The increase in firing frequency during excitation is not always smooth. In about 50 % of preparations it took the form of bursting which was masked at higher frequencies but reappeared as the firing frequency fell on reversing the drum. The frequency of bursting varied from 2-5/see and increased during excitation. It could also be present in the standing striped drum, as illustrated in Fig. 42. In a few preparations small fast eye movements could be seen to accompany the bursts. The reason for the bursting is uncertain. It is certainly not necessary since it was not always present, but when present it may prevent accommodation to visual input. (vi)

Flip-backs

As mentioned in para. (i) the eyes show saccadic flip-backs when they have reached an extreme position during following movements. The appearance of these flip-backs seems to be correlated with the attainment of a certain frequency level in the optokinetic fibres. However, it is certain that this is not the only factor involved since flip-backs did not always occur at adequate firing frequencies. It is possible that the mechanism shows habituation. If the required frequency was not reached, e.g. because the fibre had habituated, a flip-back might still occur if the frequency suddenly increased with the onset of excited state. The appearance of flip-backs is associated with characteristic changes in firing pattern o f the optokinetic fibres. During stripe rotations in the preferred direction, the high-frequency firing is suddenly interrupted. Then a gradual build up in frequency again occurs, at a speed proportional to but faster than the original build-up. The firing of both phasic and tonic fibres show a similar pattern, as shown in Fig. 43 where simultaneous records of both a phasic and tonic fibre are shown. During stripe rotation in the unpreferred direction, the

160

BARBARAYORKANDC. A. G. WmRSMA

A

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13

FIG. 43. Changes in fixing frequency during a flip-back in clockwise motor fibres. (A) Tonic and phasic fibres together. (B) Phasic fibre only (recorded simultaneously). Time base: 1 sec. inhibition is interrupted during a flip-back by a sudden burst, usually in both phasic and tonic fibres. The burst could last for up to 2 sec in the tonic fibres, but lasted on average for only 0.5 see. (vii) Speed of stripe rotation and habituation The speed at which stripes rotate relative to the lobster has a great influence on the firing pattern of the optokinetic fibres, and also on the frequency of flip-backs. The most significant effect of rotation speed is on the rate at which a fibre habituates to repeated stripe rotation. Habituation is usually not pronounced, but develops rapidly if the stripes are rotated at high speeds well above 2°/sec. Once habituation is present the fibre responds only to intermediate speeds of about 2°/see. At slow speeds the frequency does not rise above background, and at fast speeds it returns to background after an initial burst. The time in which the fibre builds up to a maximum firing rate when excited by stripe rotation is also dependent on the speed of this rotation. At very slow speeds of 0.06°/see firing frequency gradually increased, providing habituation was not present, over a period of about 5 min. With fast drum speeds of 10°/see or more, a maximum firing frequency was reached in less than a minute. For a given fibre the maximum frequency reached is fairly independent of drum speed, although owing to habituation, intermediate rotation speeds were most effective (see Table 2). TABLE 2. INFLUENCE OF DRUM SPEED ON THE MAXIMUM FIRING FREQUENCY OF A TONIC OPTOKINETIC FIBRE AND ON FLIP-BACK FREQUENCY Drum speed °/sec

0.06 0.7 2.0 10.0

Maximum tonic firing frequency spikes/see

Flip-backs[lO sees

35 50 41 20*

0 1.5 1.5 0

* Maximum frequency after initial early burst. The frequency of flip-backs, whose appearance depends on the attainment of a certain optokinetic firing frequency, also varied with speed. As frequency build-up was greatest at high speeds, flip-back frequency was also maximal at high speeds in fresh preparations. However, after habituation, intermediate speeds of rotation gave rise to the highest frequency of flip-backs (see Table 2).

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(viii) Dishabituation Turning the animal within the striped drum was sometimes even more effective than turning the stripes around the animal. In about 50 % of the animals there was no appreciable difference between the two. In other cases turning the animal gave a huge response while turning the drum was relatively ineffective. This result can be partly explained by the fact that the visual stimulus is strongest when the animal is turned. Here both the stripes and the surroundings above the striped drum will move in the same direction relative to the eye. When the stripes are rotated, however, the eye will follow the stripes so the stationary surroundings above the drum will move in the opposite direction to the stripes relative to the eye. The difference in visual stimulus is not enough to explain the greater effectiveness of rotating the animal. It would seem that a second difference is that unexpected rotation of the animal increases its "attention". This is illustrated in Fig. 44. Repeated stripe rotation I~rings about habituation of the optokinetic fibre. If the animal is then turned at the same speed as the stripes were previously rotated, the response is much greater. Stripe rotation immediately after animal rotation no longer causes a habituated response. It appears that the animal rotation dishabituates the fibre.

A

B

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C

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D

A A FIG. 44. Habituation to repeated drum rotation, and dishabituation by animal rotation, of tonic clockwise motor fibre. (A) Normal response to drum rotation. (B) Habituated response to drum rotation. (C) Response to animal rotation. (D) Dishabituated response to drum rotation. Time interval between experiments was 30 sec. Time base: 1 sec.

(ix) Optokinetic memory In para. (v) it is mentioned that a large after-discharge can remain for many minutes after drum rotation is stopped. In general the firing frequency of the optokinetic fibres attained during stripe rotation remains fairly constant for some time after the rotation ceases. Thus if the stripes had rotated in the unpreferred direction for a given fibre, the firing rate of this fibre would remain below resting levels for some time after stopping rotation. Of course, it follows that the eye remains in the same off-centre position for this length of time. If the light is turned off during the after-discharge and then turned on again, the afterdischarge rate falls to the resting level during darkness, but. then resumes the previous firing frequency when the light is turned back on (see Fig. 45). The resumption of firing frequency is not immediate but takes 15-30 se¢. How can this resumption of firing frequency after darkness be explained ? It seems that there is a memory of stripe position relative to the eye. This was shown by moving the stripes during the period of darkness. If a fibre was excited by stripe rotation, and the after-discharge on stopping rotation remained high, then after a short period of darkness this same high frequency, or at least nearly as high a frequency, would be resumed.

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However, if during the darkness the stripes were moved a few degrees in the unpreferred direction, then when the light was switched back on, the firing frequency assumed by the fibre would be lower than previously. If the stripes were rotated a few degrees in the preferred direction during darkness, the firing rate after darkness would be higher (see Fig. 45). It seems as though there is a system which "remembers" the positions on the eyes where the stripes fell, and causes these positions to be reassumed after the eye moves. During darkness the eye probably returns to a central "rest" position since the firing rate of the optokinetic fibres returns to resting levels. When visual input is present again the eye position is corrected, as long as the period of darkness does not exceed 2 min. A similar optokinetic memory has been very thoroughly studied in crabs (Horridge, 1966a,b, 1968b). Horridge has suggested that such an optokinetic memory can explain how insects and crabs can perceive movements down to angular speeds of one revolution per 3 days. Such behaviour reveals a persistent memory of target position on the eye. In crabs the duration of the memory seems longer than in lobsters. The presence and degree of memory shown by rock lobsters was in fact variable.

A Control

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Fxo. 45. Optokinetic memory. Changes in firing frequency of a tonic clockwise motor fibre in a stationary striped drum caused by movement of the stripes during 49 sec darkness (hatched areas). Stripe rotation in preferred direction stopped at arrows. (A) No movement (B) 8° in unpreferred direction caused inhibition. (C) 8° in preferred direction caused excitation.

Optokinetic fibres : Discussion The optokinetic fibres, like the position-sensitive fibres, seem to be involved in keeping the position of the visual image on the eye fixed when the image or the animal moves. In the optokinetic fibres a memory system allows the eye to return to its former position relative to the visual image even after fairly long interruptions. Just how the optokinetic reflex is actually used in the lobster is uncertain. According to Dijkgraaf (1956a) when the lobster makes a "planned" movement, the eyes swivel first in the turning direction. This makes the optokinetic reflex superfluous here. The reflexes would then only be used if the eye was moved passively, e.g. by water currents. For further details see Dijkgraaf (1956 a, b). Presumably the reflex can be used for tracking moving objects, though only very large single targets excite the optokinetic fibres. Habituation to single targets is considerable. Owing to the variable coupling between the two eyes, presumably the animal could track with its two eyes independently. The antennal pointing reaction and the optokinetic tracking seem to be largely independent of each other. The seeing fibres, which appear to partly control antennal pointing, do not respond to moving stripes, and can respond to 2 ° targets, while the optokinetic fibres respond only to large targets and 15 ° stripes. However, under certain circumstances they must mutually influence each other. For example, large single moving objects will elicit both pointing and optokinetic tracking.

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General Discussion The optic nerve of decapod crustacea is an intercentral tract connecting the optic ganglia to the midbrain. As illustrated by rock lobster unit classes described in this review, the fibres within the optic nerve vary in complexity from primary sensory hair fibres to highly complex visual multimodal interneurones. Just how the information carried by these interneurones is processed by the animal is largely unknown at present. O f the fibres passing towards the midbrain from the optic ganglia, some fibres appear to be "sensory" interneurones, while other more complex units may well be command fibres on the " o u t p u t " side of the nervous system. Some large-field, mainly bilateral visual interneurones are known to run in the circumoesophageal commissures of the crayfish which connect to the ventral nerve cord (Wiersma and Mill, 1965). Studies on crabs show that mechanoreceptive and visual information from the contralateral eye pass to the optic ganglia, presumably to be processed there. These fibres could provide inputs for multimodal and bilateral visual interneurones. Although the behaviour of numerous interneurones in the optic nerve of crayfish, crabs and rock lobster have been carefully analysed, in general their outputs are highly speculative. In a few cases behavioural patterns have been correlated with the firing of a particular interneurone or group of interneurones. It is obvious that for most behavioural patterns a large number of interneurones will be involved. However, possible interneurone roles can be postulated from the type of information which the fibre carries. Table 3 shows postulated outputs for some of the interneurones described in the previous pages. TABLE3. TABLE OF POSTULATED OUTPUTS FOR VISUAL INTERNEURONESOF ROCK LOBSTER Fibre class Sustaining fibres Fast-movement fibres (uni- and multimodal) Space-constant jittery movement fibre Unidirectional multimodal Seeing fibres Large field and multimodal fibres Dimming fibres Light movement fibres Medium movement fibres

Postulated output Input on to position-sensitive oculomotor fibres; effect on locomotor activity, excited state (see p. 139) Input for defence reaction-command fibre? (evidence from chronic implantation studies--see p. 141) Escape reaction (see Wiersma, 1970) Crayfish; input for defence reflex (see Wiersma, 1970) Input for pointing reaction--command fibres? Input onto "pointing reaction" command fibres (see pp. 144, 150), form vision (see Wiersma and York, 1972) Input onto activity fibres to increase alertness ?

To what extent is the visual processing carried out by lobster optic interneurones similar to that in the rest of the animal kingdom ? As would be expected, identical classes of fibres are found in the optic tracts of rock lobsters, crayfish and crabs, though some differences exist (see Table 4). Light-movement and seeing fibres have been found only in the rock TABLE4 Class of fibre

Crayfishes

Rock lobsters

Crabs

Sustaining Dimming Jittery movement Light movement Medium movement Fast movement Seeing Slow movement Space constant Unidirectional movement Multimodal

+ + +

q+ + + + + +

+ q+

+ + + +

+ + +

+ + ? + + + +

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lobster so far, and slow-movement fibres appear to be restricted to crabs (Brachyura). However, considerable similarities exist between the trigger features of lobster optic interneurones and visual interneurones of other animals. Features such as directionality of movement, fast or jittery movements are abstracted by interneurones of crustacea, insects and vertebrates. Table 5 groups visual interneurones found in various species whose trigger features show similarities to a lobster visual interneurone class. O f course, in several cases detailed behaviour varies. However, there is a marked similarity in the processing of sensory inputs throughout the animal kingdom. TABLE 5

Sustaining fibre

Dimming fibre

Jittery movement Light movement Fast movement Seeing fibres

Unidirectional movement fibres

Muitimodal jittery movement and seeing Space constant fibres

Lubber grasshopper optic lobes (Northrop and Guinon, 1970) Butterfly Heliconius erato, medulla externa, protocerebrum (Swihart, 1968) Dipteran first optic ganglion (Arnett, 1972) Limulus second optic ganglion (Snodderley, 1971) Goldfish retinal ganglion cell (Wagner et aL, 1960) Goldfish retinal ganglion cell (Wagner et aL, 1960) Lubber grasshopper optic lobes (Northrop and Guinon, 1970) Butterfly Heliconius erato, medulla externa (Swihart, 1968) Frog retinal ganglion cells dark detectors (Lettvin et aL, 1961) Butterfly Heliconius erato, medulla externa (Swihart, 1968) Frog optic tectum "newness" units (Lettvin et aL, 1961) Monkey striate cortex (Wurtz, 1969) Rabbit superior colliculus (Horn and Hill) Rabbit retinal ganglion cells (Barlow et al., 1964) Fly Calliphora phaenicia and domestica medulla lc units (McCann and Dill, 1969) Frog optic tectum "sameness" units (Lettvin et aL, 1961) Frog retinal ganglion cells sustained edge detectors or boundary detectors Lettvin et aL, 1961) Locust ventral nerve cord (Palka, 1967). Cricket ventral nerve cord (Palka, 1969) Butterfly Heliconius erato, medulla externa (Swihart, 1968) Rabbit retinal ganglion cells (Barlow and Hill, 1963) Squirrel retinal ganglion cells (Cooper and Robson, 1966); (Michael 1966). Cat lateral geniculate cells (Kozak et aL, 1965), cat cortex (Hubel and Wiesel, 1965; Baumgartner et aL, 1964) Fly Calliphora phaenicia (Bishop et al., 1968). N.B. No obvious optokinetic fibres are included Lubber grasshopper optic lobes (Northrop and Guinon, 1970) Locust tritocerebrum (Horn and Rowell, 1968) Monkey striate cortex (Wurtz, 1969) Cat visual cortex (Horn et al., 1972)

Several problems requiring further study arise from this work. It is necessary to investigate what role the various interneurones described in the review are playing. Further studies on behaviour correlation with the firing activity of chronically implanted units may contribute to this. Another possible approach is to study the destinations of certain interneurones using procion yellow (Stretton and Kravitz, 1968) or cobalt (Pitman et al., 1972) injection techniques. Perhaps simultaneous recordings from two or more levels of the nervous system would also help here. Another interesting problem which has arisen from these studies is the factors affecting the reactivity of various interneurones. There is evidence, for example, that the habituation rate of an auditory interneurone in the tettigniid H o m o r o c o r y l i u s is influenced by inputs from the thoracic ganglion which act synaptically within the prothoracic ganglion (McKay, 1970). In the rock lobster several fibres show "spontaneous" changes in reactivity. During walking the reactivity of the seeing fibres is greatly reduced. Also it is noteworthy that "novel" or unexpected targets reverse habituation in some fibres. The existence of bilateral fibres in the rock lobster is also interesting since binocular vision is not known to be important. Also it appears that the coupling of movements of the two eyes is very variable. In some optokinetic fibres there is a strong heterolateral input, i.e. the optokinetic movements of the two eyes will be strongly coupled. In other cases there is no heterolateral input, i.e. no coupling. The control of coupling and the significance of bilateral visual input could be further studied.

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