J. Phyaiol. (1977), 266, pp. 471-498 With 15 text-figure8 Printed in Great Britain

471

EYE- AND HEAD MOVEMENTS IN FREELY MOVING RABBITS

BY H. COLLEWIJN From the Department of Physiology, Faculty of Medicine, Erasmus University, Rotterdam, The Netherlands

(Received 14 September 1976) SUMMARY

1. Eye- and head movements were recorded in unrestrained, spontaneously behaving rabbits with a new technique, based upon phase detection of signals induced in implanted coils by a rotating magnetic field. 2. Movements of the eye in space were exclusively saccadic. In the intersaccadic intervals the eyes were stabilized in space, even during vigorous head movements. Most of this stability was maintained in darkness, except for the occurrence of slow drift. 3. Many saccades were initiated while the head was stationary. They were accompanied by a similar, but slower head rotation with approximately the same amplitude. The displacement of the eye in space was a pure step without appreciable under- or over-shoot. The deviation of the eye in the head was mostly transient. 4. Other saccades were started while the head was moving and were possibly fast phases of a vestibulo-ocular reflex. The time course of the eye movement in space was identical for all saccades, whether the head was moving prior to the saccade or not. Eye movements without any head movement were not observed. 5. Saccades were mostly large (average 206 + 12.40 S.D.) and never smaller than 10. The relations of maximal velocity and duration to amplitude were similar to those reported for man. 6. Visual pursuit of moving objects, when elicited, was only saccadic and never smooth. 7. It is concluded that the co-ordination and dynamics of the rabbit's head- and eye movements are similar to those of primates. In the absence of foveal specialization, the eye movements are restricted to a rather global redirection of the visual field, possibly in particular of the binocular area.

472

H. COLLEWIJN INTRODUCTION

The control of the orientation of the eyes in space may be considered as a fundamental feature of guided visuo-motor behaviour. In a free situation, the position of the eye in space is the resultant of the positions of eye in orbit, head on body and body in space. The elimination of the latter two degrees of freedom by immobilizing the head, as is common practice in oculomotor research, might well distort normal oculomotor behaviour. The relatively few studies in which at least horizontal rotation of the head was allowed indicate a close correlation between eye- and head movements for monkey (Bizzi, Kalil & Tagliasco, 1971) and man (Mowrer, 1932; Bartz, 1966; Gresty, 1974). Such integrated eye- and head movements will demand a more complex structure of commands than eye movements alone and may involve feed-back loops such as the vestibuloocular and neck reflexes (Morasso, Bizzi & Dichgans, 1973). The resultant movements of the eye in space in a free animal might have other characteristics than those inferred from the situation with the head fixed. Also several sub-systems which have been distinguished such as fixation, smooth- and saccadic-pursuit, optokinetic and vestibulo-ocular reflexes have been usually studied in isolation and although plausible hypotheses about their functional meaning have been furnished (Robinson, 1968; Steinman, 1975), their actual integrated performance in real life can be only assessed in a freely behaving subject. For the rabbit, distortion of oculomotor performance by head fixation is even more likely than for man, monkey and cat. These latter species show a considerable amount of voluntary eye movements also with the head fixed (Dodge & Cline, 1901; Fuchs, 1967; Winterson & Robinson, 1975), but in the rabbit spontaneous eye movements are very rare under such conditions. Even the display of presumably 'interesting' visual objects does not induce fixation or pursuit, and for this reason the rabbit has proved highly suitable for the study of optokinetic- and vestibulo-ocular reflexes in isolation (Ter Braak, 1936; Brecher, 1936; Collewijn, 1969; Baarsma & Collewijn, 1974, 1975). Since a rabbit is prone to 'freeze' in any frightening or unusual condition, the lack of spontaneous eye movements with the head fixed might be entirely artifactual. In a freely moving rabbit saccadic eye movements can be easily observed, but since they are always accompanied by head movements, they could be merely fast components of a vestibulo-ocular reflex. Hughes (1971), using cinematographic recordings, has provided some evidence for intentional saccadic eye movements, not triggered by head movements. Obviously, cinematographic recording is not very suitable for a more detailed analysis of the dynamics of eye- and head movements

EYE MOVEMENTS IN UNRESTRAINED RABBITS 473 The present study is a first attempt to record continuously the normal, horizontal eye- and head movements in spontaneously behaving, unrestrained rabbits. These observations, made possible by the development of a new electromagnetic recording technique, show that free rabbits make frequent saccades, in close association with but often apparently not initiated by head movements. In the intersaccadic interval the eyes are stabilized in space, even when the head is moving erratically. METHODS

The principle of the measuring technique was suggested to us and recently published in a brief report by Hartmann & Klinke (1976). Two horizontal a.c. magnetic fields of equal magnitude, in spatial and phase quadrature, generate a magnetic vector of constant magnitude rotating with uniform angular velocity through 3600 during every period of the field frequency. The phase of the voltage induced in a sensor coil, placed in the field, will vary linearly with the angular orientation of the coil, and thus by phase detection the horizontal angular orientation of any object in the field can be measured.

Construction of the field To use this principle to its full advantage it is crucial that the two magnetic fields be homogeneous in direction and magnitude and truly orthogonal in space and phase. With an ordinary pair of coils the area of approximate homogeneity is quite small compared to the size of the coils. Robinson (1963), who introduced a similar field (but a different detection principle) in oculomotor research, estimated the approximately homogeneous area for two parallel circular coils with a diameter and distance of 2 ft. as a cube of no more than 2 in. on an edge. However, a simple arrangement for creating a more truly uniform, easily accessible magnetic field has been described by Rubens (1945). Five equally spaced coils, forming the surface of a cube, with the number of turns proportional to 19, 4, 10, 4 and 19, respectively, were connected in series. The magnetic field generated by such a coil proved to be homogeneous within 1 % in a cube concentric with and having half of the diameter of the coil. I constructed two such systems perpendicular to each other with a diameter of about 160 cm, which produced a homogeneous rotating field in a cube of 80 cm on an edge. This is enough space for a free rabbit to display some spontaneous behaviour. The coils were wound with insulated copper wire (diameter 158 mm) on a wooden frame, the numbers of turns used were 76, 16, 40, 16, and 76. The coils were connected to a sine and cosine constant current source with appropriate capacitors in series to tune them to the field frequency of 600 Hz. The peak current (about 850 mA) was adjusted for equal intensity (measured with a sensor coil) in both fields; the magnitude of the rotating vector was about 60 A. m-l (Fig. 1). Preparation of animal Scleral induction coils were chronically implanted as described by Fuchs & Robinson (1966) in adult Dutch belted rabbits. The coils consisted of 5 turns of Miniature Bioflex wire (type AS 632, Cooner Sales Company, Chatsworth, California), connected to a female miniature socket embedded in acrylic resin on top of the skull. This technique has been used in our laboratory for several years now in combination with the classical method of Robinson (1963) for measuring eye movements. The

474

H. COLLEWIJN

tolerance for these coils in the rabbits is excellent, no adverse effects have been noticed and previous observations indicate that eye movements remain perfectly normal. The typical life span of a coil before breakage is many months up to more than a year. Coils were implanted on one or both eyes. A coil for measuring head orientation was attached (in the sagittal plane) to the male connector through which the animal was connected with the detection equipment. This connexion was made with very flexible cables, which were elastically suspended upwards to remain out of reach of the rabbit's teeth, which are particularly prone to sever any cable at once. The load and drag on the rabbit's head by these leads was very minor. The rabbits were allowed to move freely on a square wooden platform (80 x 80 cm) bounded by vertical wooden edges (height 15 cm) within the homogeneous magnetic area.

IPhase detector

Fig. 1. Schematic drawing of the experimental apparatus. The two sets of five parallel coils, mounted perpendicular to each other, are indicated. The coils (numbers of turn 76, 16, 40, 16, and 76, respectively) are connected in series. The supporting structures (made of wood) are not shown.

Phase detection

Through the cables the head- and eye-coils were connected to differential amplifiers. Adequate magnetic screening and twisting of the leads and a high common mode rejection of the amplifiers proved essential to distortion-free con-

EYE MOVEMENTS IN UNRESTRAINED RABBITS

475

duction and processing of the rather weak magnetically induced signal (about 0;7 mV peak-to-peak). After amplification the sinusoidal signals from the head and eyes together with a reference signal from the current source were transformed into square-waves. To compare the phases of any two signals, the rising slopes of these square-waves were used to set and reset a bi-stable multivibrator. In this way a train of pulses was obtained with a frequency of 600Isec and a duration proportional to the phase angle between the two input sources. This pulse train was filtered through a low-pass filter (corner frequency 100Hz) to obtain an analogue voltage which was directly proportional to the angular orientation of the respective coil. Four signals and four phase angles could be processed simultaneously. The gain and DC offset of the output signals could be adjusted. An often used setting was 10 mV/0. Output voltages were reduced to a suitable level to be written out on a Grass Polygraph Model 7 curvilinear penrecorder. One possibility was to record the full 3600 of rotation absolutely, at a sensitivity of 10I/mm. For a better resolution signals were also written out at 1 or 20/mm. In this case an electronic circuit was used to reset the pens automatically to an arbitrary zero level whenever the pen deviation exceeded 20 mm. The whole system was tested and calibrated with an assembly of two dummy coils which could be rotated through calibrated angles, and a digital voltmeter. With optimal adjustments linearity was correct within 1 % over 360°. The output voltage typically increased by 10 mV/" for clockwise rotation of the sensor coil; near the 360°/0° transient point there was a small angle (1-2°) in which the output signal was unreliable and noisy. The maximal error in the measurement of the fixed angle between the two coils when the assembly was rotated through 3600 was + 1°. Translation of the assembly along straight trajectories through the 80 cm homogeneous cube did not affect the output signal. The noise level (for 5-turn coils) was about 12 min of arc peak-to-peak at an overall system bandwidth of 75 Hz (-6 dB); the latter was determined by the pen recorder. The rise time for steps in the input signal was typically 10- 15 msec (this is at least three times shorter than the briefest saccades recorded in the present experiments). In some of the experiments the position signals were differentiated in an operational circuit (limited at 70 Hz) to obtain the eye- and head-angular velocity. Since the noise level was about 20f/sec peak-to-peak only fast movements were well defined in this signal. A major advantage of the system is the absolute calibration, since the system measures phase angles and is insensitive to variations of the amplitude of the coil signals due to individual differences in the eye coils. One source of artifacts should be pointed out. Ideally one would measure the angle between the planes of any two coils (e.g. the two eyes). Actually, the system measures the angle of intersection of these two planes with the horizontal plane. This measured angle deviates from the true angle when the two coils are moved around a non-vertical axis. For instance, the apparent convergence angle between the eyes is changed by tilt of the head around the sagittal (roll) and transversal (pitch) axis. For a set of two coils intersecting with an angle a the measured angle a' is approximated by: cos /8 cos y

in which fi is the angle of pitch and y is the angle of roll. However, in the living animal this error may be much reduced by the action of compensatory vestibuloocular reflexes which tend to stabilize the position of the eyes in space. Therefore, the actual error is difficult to assess but probably not very large as long as pitch and roll are not excessive.

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H. COLLEWIJN

Pos8ible extension of the &y8tem In preliminary experiments it has been found to be feasible to combine the present phase-detection technique with the phase-locked amplitude detection technique as introduced by Robinson (1963). For this purpose, horizontal search coils can be mounted on the skull and the eye and connected to a lock-in amplifier, preferably of the dual phase type (e.g. Princeton Applied Research Model 129). In this way, roll and pitch of the head (and eye) can be measured simultaneously with yaw. If the output of the vertical head coil is used as the phase reference to the lock-in amplifier, roll and pitch of the head are measured independently of the position of the head in the field. The excellent homogeneity of the field guarantees a reliable measurement, but of course in this system the output is not proportional to the angle, but its sine (Robinson, 1963). For large head rotations this may make a correction (arc-sine) of the output desirable. H

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Fig. 2. Two examples of spontaneous, co-ordinated movements of eye (E) and head (H) relative to space in exploratory behaviour, recorded at low sensitivity over the full 360° of rotation. Downward displacement represents clockwise (rightward) rotation.

RESULTS

When a rabbit was placed on the platform and connected to the recording equipment, it usually showed a variety of active behaviour including active exploration of the surroundings (watching, sniffing, walking), grooming, gnawing at the wooden edges, some visual pursuit, quietly sitting, and freezing. The head cable allowed all motions including twisting and the animals did not pay any attention to it. All rabbits showed essen-

EYE MOVEMENTS IN UNRESTRAINED RABBITS 477 tially the same behaviour. In these new surroundings the animals were more active than in the cages where they normally stayed. Some typical examples of eye- and head-movements during exploratory behaviour are shown in Fig. 2, at low sensitivity, such that the pens cover the full 3600 of rotation. It should be emphasized that all recordings in this report reflect only the horizontal rotatory movements of eye and head and no rotations around other axes, nor any linear displacements. A

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Fig. 3. Examples of spontaneous movements of eye (E) and head (H) in space, and eye in head (E-H), at higher resolution than in Fig. 2. Triangles indicate an automatic resetting of the recording pen. Downward excursion represents clockwise (rightward) rotation for all traces in all illustrations. A-C, normal illumination; D, darkness.

It was consistently found that all movements of the eye in space were saccadic, and that in the interval between saccades the eye was stabilized in space. In all cases, the saccadic eye movements were accompanied by head movements. Often (Fig. 2) these head movements consisted mainly of smooth steps, in perfect co-ordination with the saccadic eye movements, and the head was nearly stable in the intervals. More detailed recordings at a higher sensitivity are shown in Fig. 3A-C. Positions of head in space (H) and eye in space (E) have been written out on self-resetting traces (see methods, resets indicated by triangles) and are therefore relative. The position of the eye in the head (E-H) is essentiallythe difference between

478 H. COLLEWIJN the other two traces but was synthesized directly from the phase angle between eye and head. The movements of the eye in space were exclusively saccadic. Saccades were made frequently (up to 4/sec) and many of them were started while the head was stationary. As is obvious from the E-H trace, the eye moved faster than the head, at least in the first half of the saccade, but eventually the head rotated over about the same angle as the eye. The displacement of the eye in the head was relatively small and mostly transient. At other moments, the head followed the eye somewhat more smoothly and gradually, and was not quite stable between saccades, particularly when saccades were made in rapid succession (Fig. 3A, B). In such cases many eye saccades started while the head was moving, but the movements of the eye in space remained strictly saccadic. The movements of the eye in the head could assume a nystagmoid character while the head was moving (Fig. 3A, B), but the amplitude remained limited. Obviously, recordings of eye position relative to the head alone, which might be recorded in a free animal with electro-oculography, would not reveal the true nature of eye- and head-movements in space. To investigate how essential vision was for this behaviour, Psome recordings were made in darkness (Fig. 3D). The coordination of eye- and head-movements and the general saccadic character of the movements of the eye in space was maintained, but in the inter-saccadic interval the ocular stability was slightly decreased, particularly when the head was moving. Presumably, this drift reflects the absence of optokinetic stabilization, which is particularly effective for low slip velocities, while sudden head movements will excite the vestibulo-ocular compensatory reflexes (Collewijn, 1969; Baarsma & Collewijn, 1974). In Fig. 4 the effect of darkness is shown in two rabbits in a quiet state. With the lights on (A, C) both head and eye were steady between the infrequent saccades. In darkness stability was sometimes maintained (D) but in another case (B) a slow drift of both head and eye occurred (about 1-8 0/sec). Such a drift, which is well within the range of the optokinetic reflex, was never observed under normal illumination. At the same time (Fig. 4B) fast head movements caused hardly any eye movements, presumably due to vestibulo-ocular

reflexes. Some examples of eye- and head movements during different states of behaviour are shown in Fig. 5. To reveal the degree of stability the rotational velocities are shown in addition to the angular positions. Fig. 5A represents alert exploration, similar to Fig. 2 and 3, with saccadic eye- and head movements. The eye velocity trace reflects the perfect ocular stability between saccades; the latter had a high velocity and short duration, so that the eye was stationary most of the time. Also the head was quite stable, but the stepwise head displacements were slower and

EYE MOVEMENTS IN UNRESTRAINED RABBITS 479 lasted longer than the ocular saccades. The velocity of the eye in the head typically followed a biphasic course. In Fig. 5B, the rabbit was sniffing around the platform and the head movements were smooth and erratic. The head velocity was fluctuating rapidly and rarely zero. Nevertheless, the eye movements in space remained saccadic and the eye velocity was still zero most of the time, even though saccades (possibly of vestibuloocular origin) were made frequently. In Fig. 5 C, the rabbit was gnawing at the wooden edge of the platform. The head movements were completely erratic, but ocular stability was still perfectly maintained. Fig. 5D shows a transition from violent head movements and very frequent saccades (which hardly left a stable interval) to a more quiet state with a few saccades and finally a state of complete rest (freezing). A

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200 1 sec Fig. 4. Recordings at increased sensitivity from two rabbits (A, B and C, D) in a quiet condition, to show the effect of darkness on long-term stability. A, C, normal illumination; B, D, darkness.

Some more examples of maintained ocular stability during rather violent head movements are shown in Fig. 6. Fig. 6A represents the typical head movements during grooming. The head was oscillating at a frequency of about 4 Hz and an amplitude of 5-10 peak-to-peak. The eye made the same movements in counterphase and with almost the same amplitude. As a result only a small part of the head oscillation was transferred to the eye. This stabilization was presumably due to the vestibulo-ocular reflex and equally effective in darkness. Fig. 6B shows another example of sniffing behaviour. Fig. 6 C shows some brief episodes of rapid headshaking, possible induced by the animal's awareness of the cable. The frequency was about 7 Hz and compensation was excellent. The most extreme case

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H. COLLEWIJN 480 of such headshaking recorded is shown in Fig. 7; the movement had a maximal frequency of 18 Hz. Eye movements were about three times smaller than head movements, thus compensation was still rather effective at this high frequency. A C H

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Fig. 5. Head- and eye-movements in different behavioural states. Position (p) and velocity (v) of head in space (H), eye in head (E-H) and eye in space (E). A, exploratory behaviour with co-ordinated fast eye and head movements. B, sniffing, with smooth head movements but saccadic eye movements. C, gnawing, with erratic head movements but strictly saccadic movements of the eye in space. D, transition from erratic head movements through co-ordinated saccades to a quiet state (freezing).

In the situations illustrated so far, locomotion occurred quite often but was not specifically identified in the figures. Some periods in which a rabbit was really walking some distance are marked in Fig. 8 (bars). The size of

EYE MOVEMENTS IN UNRESTRAINED RABBITS

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Fig. 6. Maintained ocular stability (eye in space) during erratic head movements. A, head movements typical for grooming behaviour; B, sniffing behaviour; C, periods of violent head shaking (indicated by bars).

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EYE MOVEMENTS IN UNRESTRAINED RABBITS 483 the platform limited the duration of this locomotion to 1 or 2 sec. Ocular stability was reasonable well maintained in walking, but apparently not as well as in the situations shown so far. On the other hand, visual stability during walking must be limited anyway, since the linear convection of the retinal projection is not compensated in the rabbit by a linear head nystagmus such as occurs in many birds. H

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Fig. 8. Stability of the eye during brief periods of walking (indicated by bars).

Fig. 9 illustrates some cases in which a rabbit was definitely watching with great interest. In Fig. 9A, a period (marked by bar) is shown during which a rabbit was standing erect on its hind legs and looking around attentively; this kind of behaviour is very common in rabbits. Again, the movements of the eye in space were purely saccadic. Fig. 9B, a mirror was slowly rotated (approximately sinusoidally) in front of the animal, in an attempt to elicit pursuit. This was definitely obtained but only for a short period, after which the animal lost interest. The pursuit was exclusively saccadic, and very coarse. Somewhat better pursuit was elicited by moving a hand slowly in front of the animal (Fig. 9C). The animal was clearly tracking the movements to the left and to the right with great interest. The head moved fairly smoothly (as the hand), but also in this case the ocular pursuit movement consisted only of large saccades without any smooth following. As shown in all previous examples, the eye- and head movements were always rather highly coordinated and the deviations of the eye in the head were limited and mostly transient. A more quantitative documentation of the excursions of the eye in the orbit is found in the dwell time histograms for four rabbits in Fig. 10. The zero point on the abscissa represents the average eye position but has no absolute meaning, since the orientation of the coil on the eye varied in different animals and no attempt was made to calibrate coil orientation with respect to the optical axis of the eye. Each histogram covers a period of 5 min of active behaviour; the four shown are representative for a larger number of similar diagrams. Close

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Fig. 9. Attentive looking behaviour. A, the animal was standing erect on its hind legs and looking around in the period marked by the bar. B, a mirror was oscillated slowly in front of the rabbit. After a brief period of saccadic pursuit of the mirror image, interest was lost. C, the hand of the observer was moved slowly in front of the animal and clearly tracked with great interest. The head followed the hand movements smoothly, but the eye movements in space were saccadic.

EYE MOVEMENTS IN UNRESTRAINED RABBITS 485 examination of these histograms reveals that the range of movement in all animals was about 50° (25° symmetrically on each side). In some animals, the distribution of the eye position over this range was rather flat I I I I

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H. COLLEWIJN 486 (Fig. 10 upper graph) while in others the eye stayed in the middle 200 of the range most of the time (Fig. 10, lower graph). The saccades, which apparently are the exclusive mode of movement of the eye in space, will now be examined in greater detail. The variety of combinations of eye- and head movement that may occur is illustrated in Fig. 11 with a faster time scale. In Fig. 11A for the first two saccades no fast head movement is present, and these might be interpreted as fast components of a compensatory movement of the eye in the skull of mainly vestibular origin. The third saccade of Fig. 11 A shows the addition of a fast and slow head movement, while in Fig. 1 B the head movements are predominantly fast. It is impossible to detect any essential difference between the movements of the eye in space between Fig. II A and B. A H E-H

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In Fig. 12 the time course of position and velocity of head in space, eye in head and eye in space are shown for a typical saccade with an amplitude of 200, initiated while the head was stationary. Several moments of interest have been marked by vertical lines, numbered 1-4. At t = 1, the eye started moving in the orbit and in space. The beginning of the saccade is well defined in the velocity traces. The head velocity started to increase at

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EYE MOVEMENTS IN UNRESTRAINED RABBITS 487 about the same moment, as far as can be distinguished, but the increase was much slower than that of the eye. The peak velocity of the eye in the orbit was reached soon (in this case 440'/sec after about 27 msec). The peak velocity of the eye in space was reached a little later and was slightly higher (in this case 460'/sec, after 40 msec), since head velocity is added to the velocity of the eye in the head. While the head velocity continued to increase, eye velocity declined sharply. At t = 2 (after 70 msec), the 1 2 3

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velocity of the eye in the orbit crossed the zero level. Frorn this moment the head was moving faster (with respect to space) than the eye. At t = 3, (after 125 msec) the eye reached its final position in space and was steady thereafter. The head continued to rotate around the stationary eye for another 105 msec until t = 4 (230 msec after the start of the saccade). The amplitudes of head rotation and eye rotation were approximately equal. The excursion of the eye in the head was transient and the course of the

H. COLLEWIJN 488 velocity of the eye in the orbit was biphasic. The main characteristics of a typical saccade can be summarized as follows: (1) head- and eyemovement start simultaneously; (2) head movement is much slower and lasts much longer than eye movement; (3) the amplitude of head- and eyemove-ment are very similar; (4) the movement of the eye in the orbit inverts before the eye has reached its final position in space. Various saccades of commonly occurring size and shape are shown in Fig. 13. Saccades A-K were initiated with the head stationary. A, B and C are straightforward single saccades, similar to that in Fig. 12. Also the smaller saccades were always accompanied by head movements, though for the smallest ones (which were relatively rare) head movements were often gradual and not stepwise, and for saccades in rapid succession the head movement became continuous and smooth (Fig. 3B). Saccades of the eye alone, with the head remaining stationary, were never clearly observed. The saccades illustrated in Fig. 12 and 13 A-C have a simple structure and are called 'single' because the velocity of the eye in space consists of a single peak. This type was very common, but other types occurred, particularly-among larger saccades. To retain the same structure with increasing size, eye velocity would have to increase, but apparently it cannot rise above a certain level, and either a broadening (Fig. 13D, J, K) or a splitting in two peaks (Fig. 13G, H) was seen. The latter are actually double saccades: they occurred quite frequently and intervals between the velocity peaks as short as 40 msec were seen. As a rule, the double character of the eye saccade was not reflected in the head movement, but in a few cases a splitting was indicated (Fig. 13 G). Another common variant was a velocity peak followed by a lower 'shoulder' (Fig. 13E, F). Less common variants showed multiple peaking of eye velocity and occasionally bizarre forms with up to four peaks have been observed. Many saccades were initiated while the head was moving, and some examples are shown in Fig. 13L, M and N. Apart from the more continuous head movement such saccades were often characterized by a nystagmic course of the displacement of the eye in the head (slow and fast component in opposite directions) instead of a transient deviation. Notwithstanding these differences, the movement of the eye in space (Fig. 13L, M, N) was indistinguishable from that in saccades initiated when the head was stationary (Fig. 13A, B, C). Since the motion of the eye in space is the only visually relevant parameter, a distinction between saccades started with stationary and moving head does not seem very meaningful. Such a distinction would be ambiguous anyway, since head velocities occur through a whole range from zero to many degrees/sec and no convincing criterion for a separation into two classes is evident. In the illustrations shown so far, the saccades are mostly fairly large.

EYE MOVEMENTS IN UNRESTRAINED RABBITS 489 This is in accordance with the actual distribution of the amplitudes of saccades which is shown in a histogram in Fig. 14, upper part. The sample consists of 5 x 125 consecutive saccades recorded in five active animals, without prolonged periods of freezing behaviour. All types of saccades were included; double saccades with an interval shorter than 041 sec were B

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Fig. 14. Histograms of the distribution of saccadic amplitude (above) and intersaccadic interval (below) for 625 saccades (5 x 125 saccades from five rabbits). Shaded: maximal deviation of eye in head; line: deviation of eye in space. Periods of prolonged inactivity (freezing) were not included in this sample.

EYE MOVEMENTS IN UNRESTRAINED RABBITS 491 treated as a single saccade. The solid line represents the distribution of the amplitudes of 625 saccades with respect to space. The modal and median values were 10 and 190, respectively. The shaded histogram represents the maximal excursion of the same saccades with respect to the head; the modal size was 60 and the median size 100. Obviously, eye movements in the head are smaller (apart from the transient nature of these excursions) than those in space, due to the accompanying head movements. Fig. 14 shows clearly that small saccades of the eye in space are rare in the rabbit. All saccades up to 60 in amplitude together form less than 10 % of the sample. The smallest saccades observed measured about 10 and these were very rare, although the noise level of the equipment would have allowed the distinction of smaller saccades. On the other hand saccades could be very large; the largest single one recorded was 90° (eye in space). The distribution of the duration of the intersaccadic intervals for the same sample is shown in Fig. 14, lower part. The modal and median values were 0 5 and 0 7 sec, respectively. In conclusion, saccades in the freely moving rabbit occurred frequently and were mostly large. The individual differences between the five rabbits were very minor. The maximal velocities (Vmax, in degrees/sec) and duration (d, in msec) as a function of the amplitude of the saccade in space (A, in degrees) are shown in Fig. 15 for a sample of 199 saccades, 193 of which were recorded from two rabbits which both showed a similar distribution. Six large saccades from other animals were added; they fitted well in the distribution. The relation between maximal eye velocity with respect to space and saccadic size is shown in Fig. 15A. Obviously, a positive correlation is present but the spread is considerable, and for the larger saccades a velocity saturation is seen. This effect has already been discussed in relation to Fig. 13. The maximal velocities (Vmax) observed were about 6250/sec. A linear regression was calculated for saccades up to 350 Vmax (eye-space) = 128 + 11-4 A (eye-space) '/sec. However, the correlation coefficient (r) was only 0 77. Fig. 15B shows the relation between the maximal eye velocity with respect to the head (the first velocity peak of the biphasic movement) as a function of A. The relation was somewhat similar to Fig. 15A, with lower velocities. The linear regression for saccades up to 350 was VMax (eye-head) = 93 + 90A (eye-space) '/sec. The correlation coefficient was only 0 73. Fig. 15C shows the relation between maximal head velocity and A. The relation seems to be straighter and no saturation effect is evident. For the larger saccades, head velocity

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492 H. COLLETTIJN also approaches 600'/sec. The linear regression (calculated for saccades of all sizes) was: Vmax (head-space) = 46 + 6-OA (eye-space) '/sec. In this case, the fit was considerably better (r = 0-84). Finally, Fig. 15D shows the relation between the duration d (measured between zero points in the velocity trace of the eye in space) and size of the same saccades. Again, the relation appeared to be rather linear and was calculated as: d = 52+2-OA msec. The correlation coefficient was 0-84.

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The average duration of saccades in this sample was 89 + 31 (S.D.) msec. In combination with the average intersaccadic interval of 1-16 sec it may be estimated that the eye was stationary in space for 93 % of the time, on average, during periods of activity. DISCUSSION

In contrast to the restrained rabbit, which is characteristically deficient in spontaneous eye movements, the free animal displays an active oculomotor behaviour. The present recordings support the earlier conclusions

EYE MOVEMENTS IN UNRESTRAINED RABBITS 493 of Hughes (1971), based upon cinematographic analysis. The crucial finding is the frequent occurrence of saccadic eye movements without previous head movement. Coordinated, visually triggered, saccades combined with head movements are well known in primates and have been investigated recently in detail in the monkey by Bizzi and his collaborators. In this type of movement the eye makes a fast saccade to the target, followed by a slower head movement in the same direction. The eye reaches the target when the head has just begun to move, and during the remaining part of the head movement the eyes perform a compensatory counter rotation to stabilize the retinal image (Bizzi, Kalil & Morasso, 1972). A similar close coordination has been reported for the guinea-pig (Gresty, 1975), in which the onset of a stepwise head movement was always synchronized with a saccadic eye movement in the same direction. The present recordings leave no doubt that the free rabbit makes coordinated eye- and head movements which are very similar to those of primates. As far as can be distinguished in the velocity traces eye- and head movements start simultaneously, but the head moves slower. An interesting detail is the timing of the compensatory backward movement of the eye in the skull. It does not start when the eye has reached the final position in space (or 'target'), but already before that moment. In this phase (t2 - t3 in Fig. 11) the eye is moving in the same direction as the head, but at lower velocity. Also in this detail of the eye-head co-ordination, which was consistently found, the rabbit is similar to man (Bartz, 1966). Morasso et al. (1973) and Dichgans, Bizzi, Morasso & Tagliasco (1973) have shown that the correct gaze shift is executed equally precisely in the monkey whether the head is free, restrained or unexpectedly arrested at the start of a saccade. They also demonstrated that vestibular afferents are of major importance in the adjustment of the amplitude of the saccadic eye movements and in the execution of the counter rotation of the eye in the latter part of the saccade. It would be of great interest to repeat the experiments with the unexpected arrest of the head in the rabbit, since a rabbit does not normally initiate saccades when the head is fixed. Experiments with labyrinthectomized rabbits would not be very informative since the latter are almost completely inactive and, recover poorly. Apart from this 'triggered' movement in which the head and eye start almost simultaneously from a stationary position, Bizzi et al. (1972) have described a second type, in which the head begins to move first, after which an eye saccade follows. This kind of movement was observed when the monkey anticipated the appearance of a target and was called 'predictive mode'. In this mode the head movements were slower, and the increase in

494

H. COLLEIVIJN the activity of the agonist neck muscles was gradual, and not burst-like, as in the predictive mode. A related distinction was made by Gresty (1975) between 'voluntary' and 'passive' head displacements; in the latter the head is moving and the eye is counter-rotating before the eye-saccade. In the rabbit a similar division can be made between eye saccades starting with a stationary head (Fig. 13A-C) and a moving head (Fig. 13L-N). However, no systematic difference in the time course of the movement of the eye in space (gaze) was seen whether the head was moving or not. Apparently, the system that generates saccades (involving eye- and neck muscles) is capable of adjusting a saccade even during its execution on the basis of afferent information from the labyrinth and possibly neckproprioceptors, as has been inferred for the monkey (Morasso et al. 1973) and recently for the cat (Donaghy, 1975). The stability of the rabbit's eye in the last part of the saccadic head movement and in the intersaccadic intervals is excellent, even when the head is making vigorous and erratic movements (Figs. 5-7). These findings are at variance with a recent report by Gresty (1976), who recorded no compensatory eye movements during voluntary head movements in a rabbit with the body restrained, but in agreement with all findings in other species. Dichgans et al. (1973) have reported that ocular stability in the monkey was perfectly maintained in darkness, even during passive rotation of the head. All findings of Bizzi's group indicate that the monkey's vestibulo-ocular reflex is extremely effective and actually has unity gain. For man (Meiry, 1971) and rabbit (Baarsma & Collewijn, 1974) the gain of the vestibulo-ocular reflex for passive head movements was found to be only about 065. This raises some difficulties in the explanation of the perfect eye-head coordination in man and rabbit. However, recent observations (Barr, Schultheis & Robinson, 1976) show that human vestibulo-ocular gain may vary between 02 and 1-0 depending on the choice of the internal frame of reference. Thus, the performance of stabilizing reflexes may be much better during active behaviour, when spatial orientation is essential, than in a passive laboratory test. Atkin & Bender (1968) reported excellent ocular stability during active, self-regulated head movements in healthy human subjects, though severe defects (oscillopsia) were found in patients with labyrinthine lesions. Dichgans, Schmidt & Wist (1972) have recorded modulations of afferent and efferent unit activity in the vestibular nerve of the rabbit during ocular saccades. This may indicate a mechanism for a modulation of vestibulo-ocular gain during saccades. Most of the rabbit's ocular stability is maintained in darkness and thus not visually determined. The role of visual (optokinetic) stabilization may be most important during longer periods of relative inactivity (freezing). As shown in Fig. 4, a significant drift may occur under such circumstances

EYE MOVEMENTS IN UNRESTRAINED RABBITS 495 in darkness. As has been argued before (Baarsma & Collewijn, 1974), only the optokinetic reflex is able to suppress such slow, long-term drift. The lateral position of the eyes and the organization of the retina as visual streak type (Hughes, 1971) rather than as a foveal type may account for some quantitative differences with the oculomotor behaviour of primates. The nearly panoramic visual field (Hughes, 1971) and lack of a fovea preclude any simple optical definition of what the animal is looking at; 'fixation' is not a very useful concept in the study of rabbit's vision. The rarity of small eye movements (Fig. 14) and absence of microsaccades ( < 10' amplitude) may be an immediate consequence of this organization. Comparative investigations (Steinman, 1975) clearly show a correlation between the development of a fovea and the occurrence of small saccades. Cats never make microsaccades (Winterson & Robinson, 1975), monkeys do so only after special training (Skavenski, Robinson, Steinman & Timberlake, 1975), while humans make microsaccades all the time, although they are able to suppress them (Steinman, Cunitz, Timberlake & Herman, 1967). Small saccades in the rabbit could be even rarer than suggested by Fig. 14, since I recorded only the horizontal movements which could be the smaller part of a larger saccade with a main component in the vertical direction (Winterson & Robinson, 1975). The irrelevance of small saccades for the rabbit is also shown by the absence of any clear secondary corrective saccades after a main saccade, although these are prominent in human fixation (Becker, 1972). Behavioural evidence (Van Hof & Lagers-Van Haselen, 1973) suggests that the narrow frontal binocular area (about 30° wide, Hughes, 1971) may have a special significance, since it is preferentially used in a food-rewarded visual discrimination task. Also the saccadic pursuit (Fig. 9C) of an 'interesting' object moving in front of the animal indicates such a preference. A global redirection of this binocular area (which has a relatively large central representation, Hughes, 1971) might be the principal purpose of such saccades. The failure to elicit smooth pursuit even during attentive tracking could be also attributed to the absence of a fovea. Since the binocular zone is narrow, it would be compromised by any large movements of the eyes alone. This may be one reason for the head to follow the eyes so closely (Figs. 10 and 14). Whenever saccadic eye movements were accompanied by well defined stepwise head movements (as in Figs. 2 and 3 C) the amplitudes were similar within a few degrees. For man this relation is somewhat less tight; head movements have been reported to be about 75 0 of eye saccades on the average, for a continuously visible target (Gresty, 1974). A recent report by Bahill, Adler & Stark (1975) indicates that the large majority of saccades in freely walking subjects is no larger than 15° (eye in head). Human eye-head coordination may vary 20

PHY 266

496 H. COLLEWIJN with the circumstances and no data on gaze shifts in free behaviour are available; nevertheless these data suggest that in man also all larger refixations are achieved with a combined head- and eye movement. Finally, the data on maximal velocity and duration of saccades in the free rabbit (Fig. 15) may be compared to other findings. Collewijn (1970) determined the maximal velocity-amplitude relationship for fast phases (< 200) of optokinetic nystagmus in encephale isolge rabbits. A rather linear relationship was found with maximal velocities around 200'/sec for amplitudes of 150. In the present conditions a steeper relationship was found, with velocities of about 300'/sec for saccades with an amplitude of 150 (eye in space). For larger saccades the relation was clearly non-linear and a saturation occurred at about 600'/sec. These data (for the movement of the eye in space) are not very different from most findings on human saccades (measured with the head fixed). Baloh, Sills, Kumley & Honrubia (1975), using electro-oculography with a bandwidth of 35 Hz (-6 dB), determined a normal range (their Fig. 7) which is very similar to the present data for the rabbit (Fig. 15A). Boghen, Troost, Daroff, dell'Osso & Birkett (1974) have presented similar findings. Fuchs (1967) found somewhat higher velocities in the monkey, and also in man velocities above 700'/sec have been reported to occur under certain conditions (Clark & Stark, 1974). For the duration-velocity relationship Baloh et at. (1975) found d = 37 + 2 7A, which is also close to the present findings for the rabbit (d= 52+2.0A). Thus, the dynamics of human and rabbit saccades appear to be fundamentally similar. The rather frequent occurrence of double saccades with a very short interval is also in agreement with findings in the human (Bahill, Bahill, Clark & Stark, 1975). In conclusion, it may be stated that the general pattern of eye- and head movements in the free rabbit is very similar to that of primates. The main differences are the lack of small saccades and of smooth pursuit of small objects; both may be accounted for by the absence of a foveal organization. Drs R. Hartmann and R. Klinke (Berlin) kindly communicated the principle of the measuring system to me at an early stage. The important technical contributions of Mr F. van der Mark are gratefully acknowledged. REFERENCES

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BAHILL, A. T., ADLER, D. & STARK, L. (1975). Most naturally occurring human saccades have magnitudes of 15 degrees or less. Invest. Ophthal. 14, 468469. BAHILL, A. T., BAHILL, K. A., CLARK, M. R. & STARK, L. (1975). Closely spaced saccades. Invest. Ophthal. 14, 317-320. BALOH, R. W., SILLS, A. W., KumT..Y, W. E. & HONRUBIA, V. (1975). Quantitative measurements of saccade amplitude, duration and velocity. Neurology, Minneap. 25, 1065-1070. BARR, C. C., SCHULTHEIS, L. W. & ROBINSON, D. A. (1976). Voluntary, non-visual control of the human vestibulo-ocular reflex. Acta oto-lar. 81, 365-375. BARTZ, A. E. (1966). Eye and head movements in peripheral vision: nature of compensatory eye movements. Science, N.Y. 152, 1644-1645. BECKER, W. (1972). The control of eye movements in the saccadic system. Biblthca ophthal. 82, 233-243. BIzzI, E., KALIL, R. E. & MoRAsso, P. (1972). Two modes of active eye-head co-ordination in monkeys. Brain Res. 40, 45-48. BIZZI, E., KALIL, R. E. & TAGLIASCO, V. (1971). Eye-head coordination in monkeys: evidence for centrally patterned organization. Science, N.Y. 173, 452-454. BOGHEN, D., TROOST, B. T., DAROFF, R. B., DELL'OSSO, L. F. & BIRKETT, J. E. (1974). Velocity characteristics of normal human saccades. Invest. Ophthal. 13, 619-623. BRECHER, G. A. (1936). Optisch ausgel6ste Augen- und Korperreflexe am Kaninchen. Z. vergl. Physiol. 23, 374-390. CLARK, M. R. & STARK, L. (1974). Control of human eye movements: III. Dynamic characteristics of the eye tracking mechanism. Mathem. Biosci. 20, 239-265. COLLEWIJN, H. (1969). Optokinetic eye movements in the rabbit: input-output relations. Vision Res. 9, 117-132. COLLEWIJN, H. (1970). The normal range of horizontal eye movements in the rabbit. Expl Neurol. 28, 132-143. DIcHGANs, J., Bizzi, E., MORASSO, P. & TAGLIASCO, V. (1973). Mechanisms underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys. Expl Brain Res. 18, 548-562. DIcOGA.S, J., SCHMIDT, C. L. & WIST, E. R. (1972). Frequency modulation of afferent and efferent unit activity in the vestibular nerve by oculomotor impulses. In Basic Aspects of Central Vestibular Mechanisms, vol. 37, ed. BRODAL, A. & POMPEIANO, 0. Progress in Brain Research, pp. 449-456. Amsterdam: Elsevier. DODGE, R. & CLINE, T. S. (1901). The angle velocity of eye movements. Psychol. Rev. 8, 145-157. DONAGHY, M. J. (1975). The role of vestibular feedback in the control of gaze changes accomplished by co-ordinated eye and head movements. Abstract First European Neurosciences Meeting, Munchen. Expl Brain Res. suppl. 23, 450. FUCHS, A. F. (1967). Saccadic and smooth pursuit eye movements in the monkey. J. Physiol. 191, 609-631. FUCHS, A. F. & ROBINSON, D. A. (1966). A method for measuring horizontal and vertical eye movements chronically in the monkey. J. apple. Physiol. 21, 1068-1070. GRESTY, M. A. (1974). Coordination of head and eye movements to fixate continuous and intermittent targets. Vision Res. 14. 395-403. GRESTY, M. A. (1975). Eye. head and body movements of the guinea pig in response to optokinetic stimulation and sinusoidal oscillation in yaw. Pfliugers Arch. ges. Physiol. 353, 201-214. GRESTY, M. A. (1976). A re-examination of 'neck reflex' eye movements in the rabbit. Acta oto-lar. 81, 386-394. 20-2

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Eye- and head movements in freely moving rabbits.

J. Phyaiol. (1977), 266, pp. 471-498 With 15 text-figure8 Printed in Great Britain 471 EYE- AND HEAD MOVEMENTS IN FREELY MOVING RABBITS BY H. COLLE...
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