Camp. Biochem. Physiol. Vol. lOlA, No. 2, pp. 249-251, 1992
0300-9629/92 %5.00+ 0.00 0 1992 PergamonPressplc
Printedin Great Britain
THE RESPONSE OF STATOCYST RECEPTORS OF THE LOBSTER, HOMARUS AMERICANUS, TO MOVEMENTS OF STATOLITH HAIRS MARION L. PATTON*
ROBERT F. GROVE?
and
‘Department
of Biology, Occidental College, Eagle Rock, CA 90041, U.S.A. and ERCE, 5510 Morehouse Dr., San Diego, CA 92121, U.S.A.; tSouthem California Edison Co., Rosemead, CA 91770, U.S.A. (Received 31 May 1991)
Ah&act-l. While recording from the statocyst nerve of Homarus americanus, we deflected the statolith hairs from the “rest” position they assumed after the lith was removed. 2. Each of the smaller statocyst hairs apparently drove three sensory receptors; all receptors were sensitive to hair position, hair movement velocity, and hair movement direction. 3. Two of the receptors, types A and C, only responded when the hair was lifted up and away from rest; the third, type B, only responded vigorously when a hair was moved back toward rest from such a deflexion. 4. Type A and B receptors were phasic-tonic; type C receptors were phasic.
INTRODUCTION The inner walls of crustacean statocysts bear sensory hairs with sand grains fastened to their tips. These
sand grains tend to sink to the bottom of the statocyst; they therefore move, bend the hairs, and stimulate the sensory receptors when the animal changes its orientation relative to gravity (Stein, 1975; Patton and Grove, 1992). The sand grains are easily removed and the sensory hairs are large and tough enough to be manipulated experimentally. The classical experiments of Cohen (1955, 1960) take advantage of these properties. In Cohen’s first experiments, he rotated the intact cyst while recording from the statocyst nerve. He found four receptor classes: type I, type II, acceleration and vibration. The discharge of type I and II receptors is related to maintained tilt. The discharge of the type I receptor changes gradually with tilt; its discharge frequency reflects absolute position. The discharge of the type II receptor is also related to maintained tilt. The initial discharge of this receptor, however, is also related to the position from which this tilt had been approached. If the animal is rotated toward the position where the receptor responds maximally, the receptor response is transiently elevated. If the animal is rotated away from the position of maximum response, the receptor response is transiently depressed and adapts “upward” to a nonadapting discharge characteristic of the animal’s new position. The response curve of the maintained discharge of both receptors is bell-shaped, i.e. as the animal is rotated, the discharge rises to a peak and, with further rotation, declines again. The acceleration and vibration receptors respond only during acceleration and vibration, respectively, and are unaffected by maintained tilt. In his later experiments (1960), Cohen recorded from the nerve while moving the statocyst hairs with a micro-needle; he located hairs driving acceleration
receptors and showed that the largest statolith hairs drive a receptor with a bell-shaped curve. As the hair is deflected up and away from the center of the cyst, this receptor’s discharge rises to a peak and then declines. Cohen’s results were largely based on deflexions of the largest hairs (personal communication) and suggested that each statocyst hair drives a single neuron (Cohen, 1960). Anatomical studies of the crayfish, however, showed that these statocyst hairs were innervated by three neurons (Schone and Steinbrecht, 1968). We repeated Cohen’s experiments on both the largest and the smaller statocyst hairs. in Cohen’s laboratory, Our results, obtained confirmed his results for the receptors of the larger hairs, but also showed that the smaller hairs drive three receptors which were both distinct from each other and from the receptor Cohen described (1960). This communication describes these three receptors.
MATERIAIS AND METHODS Mature male and female lobsters (Homnrus americanus) were shipped by air from Maine and kept in aerated sea water at 10°C until use. The animals were first bled by opening the ventral abdominal sinus to prevent blood coagulation around the statocyst nerve. The cephalothorax anterior to the mouth was removed and mounted in Cole’s solution (Cole, 1941) buffered with TES (pH 7.5 f 0.05). The saline was maintained at 9.0 f 0.5”C with an ice bath. The statocyst nerve runs on the dorsolateral side of the antennular nerve and was exposed from the dorsal aspect by removing the rostrum and eyecups and chipping away the exoskeleton over the anterior surface of the brain. The brain and both statocysts were removed, and the nerve was split into small bundles with insect pins. The cut ends were sucked into glass electrodes that had funnel shaped tips. The hairs were exposed by removing the soft top of the cyst and washing the lith out with a stream of water. In order to isolate a few units from the large number of axons in the statocyst nerve, it was necessary to silence most receptors by 249
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removing all but one row of statocyst hairs before recording commenced. Receptor activity was displayed and photographed by conventional methods. The measurement of the change in hair angle during deflexion was calculated from the excursion of the micromanipulator used, in conjunction with a tungsten microfork, to move the hairs. After each experiment, the micromanip ulator excursion necessary to move the hair from “rest” to the vertical position was measured. “Rest” was the position the hairs assumed after the lith was removed. After all experiments were completed, the statocyst was cut in cross section and the angle of the hair at rest was measured directly so that the change in hair angle could be calculated.
RFSJL'IS Gross anatomy
Gross statocyst anatomy is described in the classical work of Cohen (1954, 1955, 1960) (Fig. 1). The thread (acceleration) hairs are attached to the anteromedia1 side of the cyst. The 400 statolith hairs are attached to the cyst floor and arranged in a rough crescent (Cohen, 1960). The lith is flexibly attached to the cyst floor by a secretion from the tegmental glands (Lang and Yonge, 1935). For the purposes of description, the hairs can be divided into two groups: the “row” hairs that are arranged in a hook around the posterior and lateral sides of the lith, and the very small “matt” hairs that lie under the lith near its anterior end (Patton and Grove, 1992). There are four complete rows of row hairs and one partial row. Starting from the outside, the rows will herein be referred to as rows 1, 2, 3-A (the partial row), 3 and
4 (Fig. 1). Cohen (personal communication) worked mostly with the row 2 hairs; we worked mostly with the row 3-A, 3 and 4 hairs. Since we were largely interested in the hairs mediating the roll response, we concentrated on hairs lying on the lateral side of the lith (Patton and Grove, 1992). Sensory physiology
After the lith was washed out, the smaller row hairs assumed a “rest” angle of 50” with the cyst floor; the hairs were inclined toward the center of the cyst. To simplify discussion, deflexions which increased this angle, lifting the hair up and away from the center of the cyst, will be called “lateral deflexions”; deflexions which pushed the hair tip down, tip towards the center of the cyst will be called “medial deflexions”. Receptors were classed as types A, B and C. It was often possible to stimulate two or three kinds of receptors with movements of the same hair (Fig. 2). To ensure that these results were not due to the accidental stimulation of more than one hair, all hairs neighboring the experimental hair were removed. Two receptors of the same type were never stimulated with movements of the same hair. The responses of the receptors of rows 3-A, 3 and 4 were similar. The type A receptors did not respond when the hair was at rest, when it was medial to rest, or during the return to rest from a medial deflexion. They responded to lateral deflexions with a phasic-tonic non-rhythmic discharge that was dependent on hair position, was sensitive to the direction from which this position was approached, and initially, was
Fig. 1. Dorsal view of the lobster statocyst with the lith removed. Anterior side is on the left. Hairs appear foreshortened in this dorsal view. The ntmrbered “row” hairs surround the lith and project into it from the side while the “matt” hairs lie beneath the lith. (Reproduced from Patton and Grove, in press.)
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Fig. 2. Responses of the type A, B and C receptors to a 70” “ lateral” deflexion. “Lateral” deflexions carry the hair up and away from the center of the floor of the statocyst. “Rest” is the position the hairs naturally assume after the lith is washed out of the statocyst. A,: Deflexion from rest. A,,: Return to rest. (0) Type. A receptor. (0) Type B receptor. (m) Type C receptor. (A) Start and end of movement. dependent on deflexion velocity. The early phasic velocity-sensitive discharge adapted to a tonic and apparently non-adapting tonic discharge in about
15 set (Figs 3 and 4). The phasic discharge was faster than the tonic discharge if the direction of hair movement was away from rest. If the direction of movement was back toward rest, the phasic discharge was slower than the tonic discharge. The response curves of the tonic discharge of the type A receptors were obtained by deflecting the receptor hairs laterally to different angles. Deflection duration was 20 set and mean discharge during the last 5 set was plotted against hair angle (Fig. 5). Deflexions were presented in random order and the hairs were returned to rest for 60 set between deflexions. Under these conditions, the discharge rate was roughly proportional to hair angle between threshold (about 10’) and 50” of deflexion. Receptor discharge was constant at the maximum for all deflexions larger than 60”, including those deflexions which pushed the
Fig. 3. Graph of the responses of typical type A, B and C receptors to a stepwise lateral deflexion from rest to 80” and back. The top three lines are receptor responses, each designated by the appropriate letter. The bottom line (D) represents hair position. The first two points after the stimulus represent discharge frequency averaged over 0.5 sec. intervals. Other points represent frequency averaged over 1 sec. intervals.
hair laterally to the cyst floor. The row 4 hairs could be moved through an arc of 140” to 150”. Throughout most of this arc, the receptors were either silent or discharging maximally. Extreme medial deflexions lasting 60 set did not detectably change subsequent responses to lateral deflexion. The type A receptors showed little between-receptor variation in their response curves (Fig. 5) and their tonic responses did not change with repeated hair deflexion. Directional sensitivity of the tonic discharge was examined by comparing the above mean response curve with the mean discharge of the same receptors during a stepwise return to rest from a 90” lateral deflexion. The hairs were held at 90” until the phasic adaptation was complete and then returned to rest in a series of 20 set steps. The mean discharge during the last 5 set was plotted against hair angle (Fig. 5). The difference between the two curves increased with each returning step, was maximal at 40”, and disappeared at 10”. The difference between the curves peaked at 40” because, during the return of the hair to rest, the
Fig. 4. Record of type A receptor response during lateral hair deflexions. (A) Rest to 30”. (B) Rest to 50”. (C) Rest to 80”. (D) 90”-80”. (E) W-50”. The upward movement of the lower trace indicates a lateral movement of the hair tip; downward movement of the lower trace indicates a movement of the hair back toward rest.
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Fig. 5. Response curves of type A receptors. (a) Mean response curve, adapted discharge elicited by separate lateral deflexions, &SE, N = 12 preparations. (A, A) Response curves of the two most dissimilar receptors, adapted discharge elicited by separate lateral deflexions. (0) Mean response curve, phasic discharge elicited by separate lateral deflexions, N = 8. (m) Mean response curve elicited by a stepwise return to rest from a lateral deflexion, N = 12.
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discharge of some of the receptors became silent at 40” and could decrease no further. Adaptation was measured with maintained lateral deflexions of 60”. Adaptation was rapid for the first
l-2 set and much slower after 2 sec. Little adaptation was observed after 15 set (Fig. 6). We found little difference in adaptation rates between receptors. The response curve of the phasic discharge elicited by lateral deflexions from rest was measured with deflexions of various amplitudes. The phasic discharge was operationally defined as the discharge during the first 0.5 set of the response. Deffexions had velocities of lSO”/sec and were presented in random order, 60 set apart. The response curve of the phasic discharge resembled the response curve of the tonic discharge, but was slightly steeper (Fig. 5). The relationship between the phasic discharge and deflexion velocity was measured by deflecting the hairs to 70” at various velocities and measuring the discharge while the hair was moving between 35” and 70”. DefIections were spaced and presented as before. The phasic discharge was almost directly proportional to deflexion velocity, though there was a hint of saturation at higher velocities (Fig. 7). The type A receptors, like the type B and type C receptors, responded to vibrations generated by tapping the apparatus, to jets of water directed into statocyst, and to distortions of the statocyst wall near the base of the hair. The type B receptor resembled the type A receptor in that its reponse was phasic-tonic, but differed from the type A receptor in its directional sensitivity and response curve. The “vector” of the directional sensitivity of the type B receptors was reversed from that of the type A receptors, and all type B receptors were more sensitive to the direction of hair movement than type A receptors. The discharges of all type B receptors were silenced by a lateral deflexion of more than 10” and would usually remain silent until the hair was subjected to a movement back toward rest within
Fig. 6. Adaptation of type A, B and C receptors following a maximally effective stimulus. (*) Mean adaptation rate of type A receptors, &SE, N = 10. (0) Adaptation rates of the two most dissimilar type A receptors. (--- 0 -- -) “Upward” adaptation of a type A receptor following a movement, from 60”~50”, back toward rest. (A) Mean adaptation rate of type B receptors, &SE, N = 8. (A) Adaptation rates of the two most dissimilar type B receptors. Inset: (m) mean adaptation rate of type C receptors, &SE, N = 8. (0) Adapta~on rate of typical A receptor. (A) Adaptation rate of typical type B receptor.
the receptor’s response range (Figs 3 and 8). The discharge of a few type B receptors, however, would adapt “upward” to a slow tonic discharge following lateral deflexions of less than 20”. The adaptation of the
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Fig. 7. Effect of deflexion velocity on phasic discharge of typical A, B and C receptors. (0) Type A receptor. (A) Type B receptor. (m) Type C receptor. See text.
Lobster statocyst receptors
A
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Fig. 8. Response of typical type B receptor to a stepwise return to rest from a lateral deflexion. (A) 60”-50”. (B) 50”40”. (C) 40”-30”. (D) 2OO-W. (H) Type B receptor. (0) Type A receptor. (0) Type C receptor. (A) Represents the start and end of hair movements. Time calibration 1 sec.
response of the type B receptor was rapid in the first 2 set and almost complete in 6-7 set (Figs 6 and 8). During lateral deflexions, response curves of the tonic discharge of the type B receptors peaked at or near rest (Figs 8 and 9). The response curves were measured by deflecting the hairs 90” laterally from rest, returning them to rest in a series of 7 set steps, and plotting the mean discharge during the last 2 set of each deflexion against hair angle. Mean discharge was zero for lateral deflexions of more than 50”, but was almost directly proportional to hair angle between 40” and rest. Response curves of different type B receptors were similar, but exhibited more variation between receptors than did type A receptors. The mean tonic discharge following a return to rest in a single step was not significantly different (P > 0.50, t-test) from the mean tonic discharge following a return to rest in 7-8 steps, i.e. there was no long-term adaptation in the tonic discharge during the stepwise return to rest. The mean tonic discharge of the type B receptor following a return to rest was independent of the duration and size of the lateral, silencing deflexion. The mean tonic discharge at rest following such a deflexion with a duration of 1 set was not significantly different from that following a deflexion with a duration of 60 set (P > 0.50, t-test). The mean tonic discharge following a return to rest from a lateral deflexion of 10-20” was not significantly different (P > 0.60, t-test) from that following a return to rest from a deflexion of 50-70”. Response curves of the phasic discharge of the type B receptors were obtained by returning the hair to rest in a series of 7 set steps made at a deflexion velocity of lSO”/sec. Receptor discharges during the first 0.5 set were corrected individually for adaptation, and then averaged and plotted (Fig. 9). A
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correction for adaptation was necessary because the phasic discharge at rest was significantly greater (P = 0.05, t-test) if the hair were returned to rest in a single step than if it were returned to rest in 6-7 steps. The phasic response curve was slightly steeper than the tonic response curve. The effect of deflexion velocity on the phasic discharge of type B receptors was measured as the hair moved at different velocities between receptor threshold and rest. Velocities were presented in random order and were spaced 60 set apart. The initial deflexion was 70”. The velocity response of the type B receptor resembled that of the type A receptor (Fig. 7). Type B receptors responded to medial deflexions from rest, though such responses were usually weaker and varied more between receptors than the response to lateral deflexions. Some receptors were temporarily silenced by medial deflexions and responded to a return to rest with a phasic-tonic discharge. The phasic discharge was higher than the tonic discharge when the hair was returning to rest and lower when it was moving away (Figs 10 and 11). Other receptors responded to a medial deflexion with a burst of impulses and to a return to rest with a transient depression in frequency. The discharge of some type B receptors rose to a second peak when the hair was pushed medially to the cyst floor. Type C receptors were phasic receptors that responded to a lateral deflexion from rest with 2-10 impulses and to a return to rest from such a deflexion with fewer impulses at lower frequency (Figs 3 and 12). They responded neither to medial hair deflexion nor to the return to rest from a medial deflexion. Some type C receptors had a very slow tonic discharge that was not sensitive to hair position. The response range of the typical type C receptor was fairly broad (Fig. 12) and the threshold deflexion
b HAIR ANGLE t-3
Fig. 9. Response curves of type B receptors. (0) Mean response curve, adapted discharge elicited by stepwise return to rest from a later deflexion, *SE, N = 10 preparations. (A, A) Response curves of the two most dissimilar receptors, adapted discharge. (0) Mean response curve, phasic discharge elicited by stepwise return to rest from lateral deflexions, N = 10 preparations.
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Fig. 10. Graph of response of two type B receptors to medial and lateral deflexions from rest. Medial de8exion pushes the hair down and in toward the center of the statocyst. Top two lines represent receptor responses, bottom line represents hair movements.
Fig. 11. Records illustrating responses of two type B receptors to medial and lateral detlexions. (A,) First receptor, 50” medial deflexion. (Au) First receptor, return to rest from a 50” lateral detlexion; top trace is receptor discharge, bottom trace is hair position. (Bt) Sscond receptor, 50” medial defiexion. (Bu) Second receptor, return to rest from a 50” medial deflexion. (B,,,) Second receptor, return to rest from a 80” lateral deflexion; top trace is receptor discharge, bottom trace is hair position. Arrow: receptor spike. (A) Medial deflexion. (V) Return to rest from medial defiexion. 254
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Fig. 12. Response of type C receptor to 70” lateral deflexion at varying velocities. (I) 44”/sec.(II) 85”/sec. (III) 35o”/sec. (IV) 58o”/sec. Upper trace, receptor activity; lower trace, hair position. Arrow: receptor spike. Time calibration, 0.5 sec.
appears to become smaller with increasing velocity. The mean adaptation rate, measured with deflexions of 15O”/sec to the middle of the response range, was much faster than that of the type A and type B receptors (Fig. 6). The response during the return to rest from lateral deflexions (Figs 3 and 12) indicates that the lack of receptor response during large lateral deflexions was not due to adaptation but to the “bell” shape of its response curve. The velocity response was measured with deflexions that moved the hair laterally at different velocities to 70”. Deflexions were presented in random order and spaced 60 set apart. The velocity response resembled that of the type A receptor (Fig. 7). We also discovered a statocyst distortion receptor that responded to distortion anywhere in the cyst and to the bending of a narrow tongue cut from the top of the cyst. Many hair receptors responded to gross distortions of the statocyst wall near their sensory hairs, but none responded to the above stimuli and none were as sensitive to distortion as the statocyst distortion receptor. Unlike hair receptors, statocyst distortion receptors did not respond to the bending of any hair nor to jets of water directed into the statocyst. DISCUSSION
The responses of the type II receptor (Cohen, 1955) resemble those of type A receptors. Side-down rotation produces lateral movements of the lith hairs (Patton and Grove, 1992), and type II receptors respond to a side-down rotation in the same way as type A receptors responded to lateral hair movements: with a phasic discharge that adapts to a non-adapting tonic discharge. Phasic discharges of both type II and type A receptors had the same kind of directional sensitivity. The phasic discharge following a preparation rotation that would move the hair laterally was faster than the phasic discharge following rotation that would move hair back toward
rest from lateral deflexion. The type A receptor differed from the type I receptor (Cohen, 1955) but resembled the row 2 receptor (Cohen, 1960) in that its adapted discharge was sensitive to the direction from which a position was approached as well as the position itself. Apparently, the hairs driving type I receptors have not yet been identified. Cohen’s (1955) vibration receptor resembles our type. C receptor in that both exhibit a slow spontaneous discharge that is not affected by maintained position and both respond to vibration and have relatively large pulses. Cohen did not report a rotation-produced response in the vibration receptor. This is not surprising because hair movements produced by the rotation rates Cohen used would be slow, about 12”/sec, and the few spikes elicited from the type C receptor at such rates would be widely separated and difficult to detect. It is difficult to explain why Cohen (1955) did not observe a type B receptor in his study of the responses of the intact statocyst. Possibly his study was based largely on the responses of the row 2 receptors. The type A, B and C receptors differ from each other and from the receptors of the row 2 hairs (Cohen, 1960). The discharges of the A, B and C receptors show much more initial rapid adaptation than the row 2 receptors; in this they resemble the receptors of the thread hairs which are acceleration receptors that are not attached to the statolith (Cohen, 1960). The response of the row 2, type B, type C, and possibly the thread hairs are bell-shaped functions of hair angle, but response of the type A receptor is a saturating linear function of hair angle. The directional sensitivity of type B receptors is much greater than that of the other four. Only type C receptors gave a phasic response to hair deflexion. The fine structure of the crayfish statocyst receptors resembles that of the chordotonal organs of the crustacean limb (Schiine and Steinbrecht, 1968). The responses of some chordotonal organ receptors resemble the responses of the type A, type B or type
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C receptors (Wiersma and Boettiger, 1959; Wiersma, 1959; Hartman and Boettiger, 1967; Mill and Lowe, 1972). Responses of the statolith receptors of the crab and the crayfish resemble those of the lobster. Responses resembling those of the type A receptor have been reported in Scylla (Sandernan and Okajima, 1972) and in Procambarus (Ozeki et al., 1978; Takahata and Hisada, 1979; Takahata, 1981). Responses resembling type C receptor responses have been recorded in Procambarus (Ozeki et al., 1978; Takahata and Hisada, 1979; Takahata, 1981), and a crayfish statocyst receptor with “tonic inhibition with off excitation” could be a type B receptor (Ozeki et al., 1978). The type B receptors are evidently not used to measure maintained body tilt (Patton and Grove, 1992), but type B receptors could be used to resolve two ambiguities in the input from the receptors that evidently are used to measure body tilt, i.e. type A receptors (Patton and Grove, 1992). First, type A receptors can produce the same discharge frequency at two different hair angles if these angles are approached from different directions. Second, lith excursion, and therefore the response of type A receptors, is maximal at 90” of body tilt and decreases when the lobster is rotated either way (Cohen, 1955; Patton and Grove, 1992) and the lobster must be able to distinguish a rotation that turns it on its back from one which turns it toward its normal orientation. Type B receptors could resolve both ambiguities because they only respond vigorously after a movement of the hair back toward rest from a lateral deflexion, i.e. after a movement that only occurs when the animal is rotating toward its normal orientation. The responses of the type B receptors to medial deflexion were erratic and weak; this suggests that they may not be functionally important. The vigorous response of a few type B receptors to a deflexion which pushed the hair medially to the cyst floor is also probably unimportant because such deflexions are not produced by normal statolith movements (Patton and Grove, 1992). Resolution of such ambiguities would be important because a lobster will almost always respond vigorously when turned on its back (personal observation). The tail flip, pleopod movements, uropod movements and torsion of the abdomen (Davis, 1968) create a powerful righting torque that would seem to require an efficient “braking” system to prevent the organism from overshooting its desired orientation. Type B receptors are not used to measure body tilt (Patton and Grove, 1992) and the responses of these receptors peak when the hair is approaching rest. It is possible to speculate that type B receptors could mediate a braking reflex. The input from the type A receptor is also ambiguous in that the phasic discharge frequency produced by a small, fast deflexion could be the same as the tonic discharge frequency produced by a larger, slower deflexion. The type C receptor, which was essentially a velocity receptor, could resolve this ambiguity because it only responds phasically. Another ambiguity, that due to the response of the hair receptors to statocyst distortion, could be resolved by the statocyst distortion receptor.
In both lobster righting reflexes and the automatic control systems designed to maintain an object in a designated orientation, a property of the object, such as tilt, is measured and the measurement used to bring the object back to the designated orientation. Both reflexes and control systems must deal with the problem of inertia; inertia tends to carry the object past the desired orientation and thereby produces oscillation. In automatic control systems, this problem is solved by making the returning force proportional to the sum of the deviation of the object from the designated orientation and the first derivative of this deviation (Murphy, 1957). It is therefore interesting that statocyst receptors were sensitive to the first derivative of hair deflexion as well as the deflexion itself.
Acknowledgements-This
work was submitted in partial satisfaction of the requirements for the degree of PhD in Comparative Physiology, University of Oregon at Eugene, 1972. We are grateful to Dr M. J. Cohen, Dr S. B. Kater, Dr H. B. Hartman and Dr M. Burrows for advice and support and to Mr L. Vernon for technical assistance. Supported USPHS grant ROl NBO 1624 to M. J. Cohen, NIH training grant 671 2Tl GM336, and NIH grant 1 F02 NS47, 792-01 to M. L. P.
REFERENCES
Cohen M. J. (1955) The function of receptors in the statocyst of lobster, Homarus americanus. J. Physiol. 130, 9-34. Cohen M. J. (1960) The response patterns of single receptors in the crustacean statocyst. Proc. R. Sot. E. 152, 3&49. Cole W. H. (1941) A perfusing solution for the lobster (Homarus) heart and the effects of its constituent ions on the heart. J. gen. Physiol. 25, 16. Davis W. J. (1968) Lobster righting responses and their neural control. Proc. R. Sot. B. 70, 435456. Hartman H. B. and Boettiger E. G. (1967) Functional organization of the propus-dactylus organ in Cancer irroratus, Say. Comp. Biochem. Physiol. 22, 651-663. Lang D. and Yonge C. M. (1935) The function of the tegmental glands in the statocyst of Homarus americanus. J. mar. biol. Ass. U.K. 20, 333-339.
Mill P. J. and Lowe D. A. (1972) An analysis of the types of sensory units present in the PD proprioceptor of decapod crustaceans. J. exp. Biol. 56, 509-525. Murphy G. J. (1957) Basic Automatic Control Theory. pp. 527. D. Van Nostrand, Princeton, N.J. Ozeki M.. Takahata M. and Hisada M. (1978) Afferent response patterns of the crayfish statocyst with ferrite grain statolith to magnetic field stimulation. J. camp. Physiol. 123, l-10. Patton M. P. and Grove R. F. (1992) Statolith hair movements and the regulation of gravity reflexes in the lobster, Homarus americanus. Comp. Biochem. Physiol. IOIA, 259-268.
Sandeman D. C. and Okajima A. (1972) Statocystinduced eye movements in the crab, Scyl/a serrata. I. The sensory input from the statocyst. J. exp. Biol. Sr, 187-204. Schdne H. and Steinbrecht R. A. (1968) Fine structure of statocyst receptors of Astacus fidviatilis. Nature, Lond. 220, 184-186. Stein A. (1975) Attainment of positional information in the crayfish statocyst. Porrschr. Zool. 23, 109-119.
Lobster statocyst receptors Takahata M. (1981) Functional differentation of crayfish statocyst receptors in sensory adaptation. Comp. Biochem. Physiol. @A,
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Takahata M. and Hisada M. (1979) Functional polarization of statocyst receptors in the crayfish Procambarus clarkii, Girard. J. camp. Physiol. 130, 201-207.
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Wiersma C. A. G. (1959) Movement receptors in decapod Crustacea. J. Mar. Biol. Ass. U.K. 38, 143-152. Wiersma C. A. G and Boettiger E. G. (1959) Unidirectional movement receptors from a proprioceptive organ of the crab, Carcinus maenas. J. exp. Biol. 36, 102-I 12.
0300-9629/92 %5.00+ 0.00 0 1992 PergamonPressplc
Printedin Great Britain
THE RESPONSE OF STATOCYST RECEPTORS OF THE LOBSTER, HOMARUS AMERICANUS, TO MOVEMENTS OF STATOLITH HAIRS MARION L. PATTON*
ROBERT F. GROVE?
and
‘Department
of Biology, Occidental College, Eagle Rock, CA 90041, U.S.A. and ERCE, 5510 Morehouse Dr., San Diego, CA 92121, U.S.A.; tSouthem California Edison Co., Rosemead, CA 91770, U.S.A. (Received 31 May 1991)
Ah&act-l. While recording from the statocyst nerve of Homarus americanus, we deflected the statolith hairs from the “rest” position they assumed after the lith was removed. 2. Each of the smaller statocyst hairs apparently drove three sensory receptors; all receptors were sensitive to hair position, hair movement velocity, and hair movement direction. 3. Two of the receptors, types A and C, only responded when the hair was lifted up and away from rest; the third, type B, only responded vigorously when a hair was moved back toward rest from such a deflexion. 4. Type A and B receptors were phasic-tonic; type C receptors were phasic.
INTRODUCTION The inner walls of crustacean statocysts bear sensory hairs with sand grains fastened to their tips. These
sand grains tend to sink to the bottom of the statocyst; they therefore move, bend the hairs, and stimulate the sensory receptors when the animal changes its orientation relative to gravity (Stein, 1975; Patton and Grove, 1992). The sand grains are easily removed and the sensory hairs are large and tough enough to be manipulated experimentally. The classical experiments of Cohen (1955, 1960) take advantage of these properties. In Cohen’s first experiments, he rotated the intact cyst while recording from the statocyst nerve. He found four receptor classes: type I, type II, acceleration and vibration. The discharge of type I and II receptors is related to maintained tilt. The discharge of the type I receptor changes gradually with tilt; its discharge frequency reflects absolute position. The discharge of the type II receptor is also related to maintained tilt. The initial discharge of this receptor, however, is also related to the position from which this tilt had been approached. If the animal is rotated toward the position where the receptor responds maximally, the receptor response is transiently elevated. If the animal is rotated away from the position of maximum response, the receptor response is transiently depressed and adapts “upward” to a nonadapting discharge characteristic of the animal’s new position. The response curve of the maintained discharge of both receptors is bell-shaped, i.e. as the animal is rotated, the discharge rises to a peak and, with further rotation, declines again. The acceleration and vibration receptors respond only during acceleration and vibration, respectively, and are unaffected by maintained tilt. In his later experiments (1960), Cohen recorded from the nerve while moving the statocyst hairs with a micro-needle; he located hairs driving acceleration
receptors and showed that the largest statolith hairs drive a receptor with a bell-shaped curve. As the hair is deflected up and away from the center of the cyst, this receptor’s discharge rises to a peak and then declines. Cohen’s results were largely based on deflexions of the largest hairs (personal communication) and suggested that each statocyst hair drives a single neuron (Cohen, 1960). Anatomical studies of the crayfish, however, showed that these statocyst hairs were innervated by three neurons (Schone and Steinbrecht, 1968). We repeated Cohen’s experiments on both the largest and the smaller statocyst hairs. in Cohen’s laboratory, Our results, obtained confirmed his results for the receptors of the larger hairs, but also showed that the smaller hairs drive three receptors which were both distinct from each other and from the receptor Cohen described (1960). This communication describes these three receptors.
MATERIAIS AND METHODS Mature male and female lobsters (Homnrus americanus) were shipped by air from Maine and kept in aerated sea water at 10°C until use. The animals were first bled by opening the ventral abdominal sinus to prevent blood coagulation around the statocyst nerve. The cephalothorax anterior to the mouth was removed and mounted in Cole’s solution (Cole, 1941) buffered with TES (pH 7.5 f 0.05). The saline was maintained at 9.0 f 0.5”C with an ice bath. The statocyst nerve runs on the dorsolateral side of the antennular nerve and was exposed from the dorsal aspect by removing the rostrum and eyecups and chipping away the exoskeleton over the anterior surface of the brain. The brain and both statocysts were removed, and the nerve was split into small bundles with insect pins. The cut ends were sucked into glass electrodes that had funnel shaped tips. The hairs were exposed by removing the soft top of the cyst and washing the lith out with a stream of water. In order to isolate a few units from the large number of axons in the statocyst nerve, it was necessary to silence most receptors by 249
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removing all but one row of statocyst hairs before recording commenced. Receptor activity was displayed and photographed by conventional methods. The measurement of the change in hair angle during deflexion was calculated from the excursion of the micromanipulator used, in conjunction with a tungsten microfork, to move the hairs. After each experiment, the micromanip ulator excursion necessary to move the hair from “rest” to the vertical position was measured. “Rest” was the position the hairs assumed after the lith was removed. After all experiments were completed, the statocyst was cut in cross section and the angle of the hair at rest was measured directly so that the change in hair angle could be calculated.
RFSJL'IS Gross anatomy
Gross statocyst anatomy is described in the classical work of Cohen (1954, 1955, 1960) (Fig. 1). The thread (acceleration) hairs are attached to the anteromedia1 side of the cyst. The 400 statolith hairs are attached to the cyst floor and arranged in a rough crescent (Cohen, 1960). The lith is flexibly attached to the cyst floor by a secretion from the tegmental glands (Lang and Yonge, 1935). For the purposes of description, the hairs can be divided into two groups: the “row” hairs that are arranged in a hook around the posterior and lateral sides of the lith, and the very small “matt” hairs that lie under the lith near its anterior end (Patton and Grove, 1992). There are four complete rows of row hairs and one partial row. Starting from the outside, the rows will herein be referred to as rows 1, 2, 3-A (the partial row), 3 and
4 (Fig. 1). Cohen (personal communication) worked mostly with the row 2 hairs; we worked mostly with the row 3-A, 3 and 4 hairs. Since we were largely interested in the hairs mediating the roll response, we concentrated on hairs lying on the lateral side of the lith (Patton and Grove, 1992). Sensory physiology
After the lith was washed out, the smaller row hairs assumed a “rest” angle of 50” with the cyst floor; the hairs were inclined toward the center of the cyst. To simplify discussion, deflexions which increased this angle, lifting the hair up and away from the center of the cyst, will be called “lateral deflexions”; deflexions which pushed the hair tip down, tip towards the center of the cyst will be called “medial deflexions”. Receptors were classed as types A, B and C. It was often possible to stimulate two or three kinds of receptors with movements of the same hair (Fig. 2). To ensure that these results were not due to the accidental stimulation of more than one hair, all hairs neighboring the experimental hair were removed. Two receptors of the same type were never stimulated with movements of the same hair. The responses of the receptors of rows 3-A, 3 and 4 were similar. The type A receptors did not respond when the hair was at rest, when it was medial to rest, or during the return to rest from a medial deflexion. They responded to lateral deflexions with a phasic-tonic non-rhythmic discharge that was dependent on hair position, was sensitive to the direction from which this position was approached, and initially, was
Fig. 1. Dorsal view of the lobster statocyst with the lith removed. Anterior side is on the left. Hairs appear foreshortened in this dorsal view. The ntmrbered “row” hairs surround the lith and project into it from the side while the “matt” hairs lie beneath the lith. (Reproduced from Patton and Grove, in press.)
Lobster statocyst receptors
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I
Fig. 2. Responses of the type A, B and C receptors to a 70” “ lateral” deflexion. “Lateral” deflexions carry the hair up and away from the center of the floor of the statocyst. “Rest” is the position the hairs naturally assume after the lith is washed out of the statocyst. A,: Deflexion from rest. A,,: Return to rest. (0) Type. A receptor. (0) Type B receptor. (m) Type C receptor. (A) Start and end of movement. dependent on deflexion velocity. The early phasic velocity-sensitive discharge adapted to a tonic and apparently non-adapting tonic discharge in about
15 set (Figs 3 and 4). The phasic discharge was faster than the tonic discharge if the direction of hair movement was away from rest. If the direction of movement was back toward rest, the phasic discharge was slower than the tonic discharge. The response curves of the tonic discharge of the type A receptors were obtained by deflecting the receptor hairs laterally to different angles. Deflection duration was 20 set and mean discharge during the last 5 set was plotted against hair angle (Fig. 5). Deflexions were presented in random order and the hairs were returned to rest for 60 set between deflexions. Under these conditions, the discharge rate was roughly proportional to hair angle between threshold (about 10’) and 50” of deflexion. Receptor discharge was constant at the maximum for all deflexions larger than 60”, including those deflexions which pushed the
Fig. 3. Graph of the responses of typical type A, B and C receptors to a stepwise lateral deflexion from rest to 80” and back. The top three lines are receptor responses, each designated by the appropriate letter. The bottom line (D) represents hair position. The first two points after the stimulus represent discharge frequency averaged over 0.5 sec. intervals. Other points represent frequency averaged over 1 sec. intervals.
hair laterally to the cyst floor. The row 4 hairs could be moved through an arc of 140” to 150”. Throughout most of this arc, the receptors were either silent or discharging maximally. Extreme medial deflexions lasting 60 set did not detectably change subsequent responses to lateral deflexion. The type A receptors showed little between-receptor variation in their response curves (Fig. 5) and their tonic responses did not change with repeated hair deflexion. Directional sensitivity of the tonic discharge was examined by comparing the above mean response curve with the mean discharge of the same receptors during a stepwise return to rest from a 90” lateral deflexion. The hairs were held at 90” until the phasic adaptation was complete and then returned to rest in a series of 20 set steps. The mean discharge during the last 5 set was plotted against hair angle (Fig. 5). The difference between the two curves increased with each returning step, was maximal at 40”, and disappeared at 10”. The difference between the curves peaked at 40” because, during the return of the hair to rest, the
Fig. 4. Record of type A receptor response during lateral hair deflexions. (A) Rest to 30”. (B) Rest to 50”. (C) Rest to 80”. (D) 90”-80”. (E) W-50”. The upward movement of the lower trace indicates a lateral movement of the hair tip; downward movement of the lower trace indicates a movement of the hair back toward rest.
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Time
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Fig. 5. Response curves of type A receptors. (a) Mean response curve, adapted discharge elicited by separate lateral deflexions, &SE, N = 12 preparations. (A, A) Response curves of the two most dissimilar receptors, adapted discharge elicited by separate lateral deflexions. (0) Mean response curve, phasic discharge elicited by separate lateral deflexions, N = 8. (m) Mean response curve elicited by a stepwise return to rest from a lateral deflexion, N = 12.
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discharge of some of the receptors became silent at 40” and could decrease no further. Adaptation was measured with maintained lateral deflexions of 60”. Adaptation was rapid for the first
l-2 set and much slower after 2 sec. Little adaptation was observed after 15 set (Fig. 6). We found little difference in adaptation rates between receptors. The response curve of the phasic discharge elicited by lateral deflexions from rest was measured with deflexions of various amplitudes. The phasic discharge was operationally defined as the discharge during the first 0.5 set of the response. Deffexions had velocities of lSO”/sec and were presented in random order, 60 set apart. The response curve of the phasic discharge resembled the response curve of the tonic discharge, but was slightly steeper (Fig. 5). The relationship between the phasic discharge and deflexion velocity was measured by deflecting the hairs to 70” at various velocities and measuring the discharge while the hair was moving between 35” and 70”. DefIections were spaced and presented as before. The phasic discharge was almost directly proportional to deflexion velocity, though there was a hint of saturation at higher velocities (Fig. 7). The type A receptors, like the type B and type C receptors, responded to vibrations generated by tapping the apparatus, to jets of water directed into statocyst, and to distortions of the statocyst wall near the base of the hair. The type B receptor resembled the type A receptor in that its reponse was phasic-tonic, but differed from the type A receptor in its directional sensitivity and response curve. The “vector” of the directional sensitivity of the type B receptors was reversed from that of the type A receptors, and all type B receptors were more sensitive to the direction of hair movement than type A receptors. The discharges of all type B receptors were silenced by a lateral deflexion of more than 10” and would usually remain silent until the hair was subjected to a movement back toward rest within
Fig. 6. Adaptation of type A, B and C receptors following a maximally effective stimulus. (*) Mean adaptation rate of type A receptors, &SE, N = 10. (0) Adaptation rates of the two most dissimilar type A receptors. (--- 0 -- -) “Upward” adaptation of a type A receptor following a movement, from 60”~50”, back toward rest. (A) Mean adaptation rate of type B receptors, &SE, N = 8. (A) Adaptation rates of the two most dissimilar type B receptors. Inset: (m) mean adaptation rate of type C receptors, &SE, N = 8. (0) Adapta~on rate of typical A receptor. (A) Adaptation rate of typical type B receptor.
the receptor’s response range (Figs 3 and 8). The discharge of a few type B receptors, however, would adapt “upward” to a slow tonic discharge following lateral deflexions of less than 20”. The adaptation of the
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Fig. 7. Effect of deflexion velocity on phasic discharge of typical A, B and C receptors. (0) Type A receptor. (A) Type B receptor. (m) Type C receptor. See text.
Lobster statocyst receptors
A
AA.
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A
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Fig. 8. Response of typical type B receptor to a stepwise return to rest from a lateral deflexion. (A) 60”-50”. (B) 50”40”. (C) 40”-30”. (D) 2OO-W. (H) Type B receptor. (0) Type A receptor. (0) Type C receptor. (A) Represents the start and end of hair movements. Time calibration 1 sec.
response of the type B receptor was rapid in the first 2 set and almost complete in 6-7 set (Figs 6 and 8). During lateral deflexions, response curves of the tonic discharge of the type B receptors peaked at or near rest (Figs 8 and 9). The response curves were measured by deflecting the hairs 90” laterally from rest, returning them to rest in a series of 7 set steps, and plotting the mean discharge during the last 2 set of each deflexion against hair angle. Mean discharge was zero for lateral deflexions of more than 50”, but was almost directly proportional to hair angle between 40” and rest. Response curves of different type B receptors were similar, but exhibited more variation between receptors than did type A receptors. The mean tonic discharge following a return to rest in a single step was not significantly different (P > 0.50, t-test) from the mean tonic discharge following a return to rest in 7-8 steps, i.e. there was no long-term adaptation in the tonic discharge during the stepwise return to rest. The mean tonic discharge of the type B receptor following a return to rest was independent of the duration and size of the lateral, silencing deflexion. The mean tonic discharge at rest following such a deflexion with a duration of 1 set was not significantly different from that following a deflexion with a duration of 60 set (P > 0.50, t-test). The mean tonic discharge following a return to rest from a lateral deflexion of 10-20” was not significantly different (P > 0.60, t-test) from that following a return to rest from a deflexion of 50-70”. Response curves of the phasic discharge of the type B receptors were obtained by returning the hair to rest in a series of 7 set steps made at a deflexion velocity of lSO”/sec. Receptor discharges during the first 0.5 set were corrected individually for adaptation, and then averaged and plotted (Fig. 9). A
253
correction for adaptation was necessary because the phasic discharge at rest was significantly greater (P = 0.05, t-test) if the hair were returned to rest in a single step than if it were returned to rest in 6-7 steps. The phasic response curve was slightly steeper than the tonic response curve. The effect of deflexion velocity on the phasic discharge of type B receptors was measured as the hair moved at different velocities between receptor threshold and rest. Velocities were presented in random order and were spaced 60 set apart. The initial deflexion was 70”. The velocity response of the type B receptor resembled that of the type A receptor (Fig. 7). Type B receptors responded to medial deflexions from rest, though such responses were usually weaker and varied more between receptors than the response to lateral deflexions. Some receptors were temporarily silenced by medial deflexions and responded to a return to rest with a phasic-tonic discharge. The phasic discharge was higher than the tonic discharge when the hair was returning to rest and lower when it was moving away (Figs 10 and 11). Other receptors responded to a medial deflexion with a burst of impulses and to a return to rest with a transient depression in frequency. The discharge of some type B receptors rose to a second peak when the hair was pushed medially to the cyst floor. Type C receptors were phasic receptors that responded to a lateral deflexion from rest with 2-10 impulses and to a return to rest from such a deflexion with fewer impulses at lower frequency (Figs 3 and 12). They responded neither to medial hair deflexion nor to the return to rest from a medial deflexion. Some type C receptors had a very slow tonic discharge that was not sensitive to hair position. The response range of the typical type C receptor was fairly broad (Fig. 12) and the threshold deflexion
b HAIR ANGLE t-3
Fig. 9. Response curves of type B receptors. (0) Mean response curve, adapted discharge elicited by stepwise return to rest from a later deflexion, *SE, N = 10 preparations. (A, A) Response curves of the two most dissimilar receptors, adapted discharge. (0) Mean response curve, phasic discharge elicited by stepwise return to rest from lateral deflexions, N = 10 preparations.
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30
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Fig. 10. Graph of response of two type B receptors to medial and lateral deflexions from rest. Medial de8exion pushes the hair down and in toward the center of the statocyst. Top two lines represent receptor responses, bottom line represents hair movements.
Fig. 11. Records illustrating responses of two type B receptors to medial and lateral detlexions. (A,) First receptor, 50” medial deflexion. (Au) First receptor, return to rest from a 50” lateral detlexion; top trace is receptor discharge, bottom trace is hair position. (Bt) Sscond receptor, 50” medial defiexion. (Bu) Second receptor, return to rest from a 50” medial deflexion. (B,,,) Second receptor, return to rest from a 80” lateral deflexion; top trace is receptor discharge, bottom trace is hair position. Arrow: receptor spike. (A) Medial deflexion. (V) Return to rest from medial defiexion. 254
Lobster statocyst receptors
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Fig. 12. Response of type C receptor to 70” lateral deflexion at varying velocities. (I) 44”/sec.(II) 85”/sec. (III) 35o”/sec. (IV) 58o”/sec. Upper trace, receptor activity; lower trace, hair position. Arrow: receptor spike. Time calibration, 0.5 sec.
appears to become smaller with increasing velocity. The mean adaptation rate, measured with deflexions of 15O”/sec to the middle of the response range, was much faster than that of the type A and type B receptors (Fig. 6). The response during the return to rest from lateral deflexions (Figs 3 and 12) indicates that the lack of receptor response during large lateral deflexions was not due to adaptation but to the “bell” shape of its response curve. The velocity response was measured with deflexions that moved the hair laterally at different velocities to 70”. Deflexions were presented in random order and spaced 60 set apart. The velocity response resembled that of the type A receptor (Fig. 7). We also discovered a statocyst distortion receptor that responded to distortion anywhere in the cyst and to the bending of a narrow tongue cut from the top of the cyst. Many hair receptors responded to gross distortions of the statocyst wall near their sensory hairs, but none responded to the above stimuli and none were as sensitive to distortion as the statocyst distortion receptor. Unlike hair receptors, statocyst distortion receptors did not respond to the bending of any hair nor to jets of water directed into the statocyst. DISCUSSION
The responses of the type II receptor (Cohen, 1955) resemble those of type A receptors. Side-down rotation produces lateral movements of the lith hairs (Patton and Grove, 1992), and type II receptors respond to a side-down rotation in the same way as type A receptors responded to lateral hair movements: with a phasic discharge that adapts to a non-adapting tonic discharge. Phasic discharges of both type II and type A receptors had the same kind of directional sensitivity. The phasic discharge following a preparation rotation that would move the hair laterally was faster than the phasic discharge following rotation that would move hair back toward
rest from lateral deflexion. The type A receptor differed from the type I receptor (Cohen, 1955) but resembled the row 2 receptor (Cohen, 1960) in that its adapted discharge was sensitive to the direction from which a position was approached as well as the position itself. Apparently, the hairs driving type I receptors have not yet been identified. Cohen’s (1955) vibration receptor resembles our type. C receptor in that both exhibit a slow spontaneous discharge that is not affected by maintained position and both respond to vibration and have relatively large pulses. Cohen did not report a rotation-produced response in the vibration receptor. This is not surprising because hair movements produced by the rotation rates Cohen used would be slow, about 12”/sec, and the few spikes elicited from the type C receptor at such rates would be widely separated and difficult to detect. It is difficult to explain why Cohen (1955) did not observe a type B receptor in his study of the responses of the intact statocyst. Possibly his study was based largely on the responses of the row 2 receptors. The type A, B and C receptors differ from each other and from the receptors of the row 2 hairs (Cohen, 1960). The discharges of the A, B and C receptors show much more initial rapid adaptation than the row 2 receptors; in this they resemble the receptors of the thread hairs which are acceleration receptors that are not attached to the statolith (Cohen, 1960). The response of the row 2, type B, type C, and possibly the thread hairs are bell-shaped functions of hair angle, but response of the type A receptor is a saturating linear function of hair angle. The directional sensitivity of type B receptors is much greater than that of the other four. Only type C receptors gave a phasic response to hair deflexion. The fine structure of the crayfish statocyst receptors resembles that of the chordotonal organs of the crustacean limb (Schiine and Steinbrecht, 1968). The responses of some chordotonal organ receptors resemble the responses of the type A, type B or type
256
MARIONL. PATIY)Nand ROBERTF. GROVE
C receptors (Wiersma and Boettiger, 1959; Wiersma, 1959; Hartman and Boettiger, 1967; Mill and Lowe, 1972). Responses of the statolith receptors of the crab and the crayfish resemble those of the lobster. Responses resembling those of the type A receptor have been reported in Scylla (Sandernan and Okajima, 1972) and in Procambarus (Ozeki et al., 1978; Takahata and Hisada, 1979; Takahata, 1981). Responses resembling type C receptor responses have been recorded in Procambarus (Ozeki et al., 1978; Takahata and Hisada, 1979; Takahata, 1981), and a crayfish statocyst receptor with “tonic inhibition with off excitation” could be a type B receptor (Ozeki et al., 1978). The type B receptors are evidently not used to measure maintained body tilt (Patton and Grove, 1992), but type B receptors could be used to resolve two ambiguities in the input from the receptors that evidently are used to measure body tilt, i.e. type A receptors (Patton and Grove, 1992). First, type A receptors can produce the same discharge frequency at two different hair angles if these angles are approached from different directions. Second, lith excursion, and therefore the response of type A receptors, is maximal at 90” of body tilt and decreases when the lobster is rotated either way (Cohen, 1955; Patton and Grove, 1992) and the lobster must be able to distinguish a rotation that turns it on its back from one which turns it toward its normal orientation. Type B receptors could resolve both ambiguities because they only respond vigorously after a movement of the hair back toward rest from a lateral deflexion, i.e. after a movement that only occurs when the animal is rotating toward its normal orientation. The responses of the type B receptors to medial deflexion were erratic and weak; this suggests that they may not be functionally important. The vigorous response of a few type B receptors to a deflexion which pushed the hair medially to the cyst floor is also probably unimportant because such deflexions are not produced by normal statolith movements (Patton and Grove, 1992). Resolution of such ambiguities would be important because a lobster will almost always respond vigorously when turned on its back (personal observation). The tail flip, pleopod movements, uropod movements and torsion of the abdomen (Davis, 1968) create a powerful righting torque that would seem to require an efficient “braking” system to prevent the organism from overshooting its desired orientation. Type B receptors are not used to measure body tilt (Patton and Grove, 1992) and the responses of these receptors peak when the hair is approaching rest. It is possible to speculate that type B receptors could mediate a braking reflex. The input from the type A receptor is also ambiguous in that the phasic discharge frequency produced by a small, fast deflexion could be the same as the tonic discharge frequency produced by a larger, slower deflexion. The type C receptor, which was essentially a velocity receptor, could resolve this ambiguity because it only responds phasically. Another ambiguity, that due to the response of the hair receptors to statocyst distortion, could be resolved by the statocyst distortion receptor.
In both lobster righting reflexes and the automatic control systems designed to maintain an object in a designated orientation, a property of the object, such as tilt, is measured and the measurement used to bring the object back to the designated orientation. Both reflexes and control systems must deal with the problem of inertia; inertia tends to carry the object past the desired orientation and thereby produces oscillation. In automatic control systems, this problem is solved by making the returning force proportional to the sum of the deviation of the object from the designated orientation and the first derivative of this deviation (Murphy, 1957). It is therefore interesting that statocyst receptors were sensitive to the first derivative of hair deflexion as well as the deflexion itself.
Acknowledgements-This
work was submitted in partial satisfaction of the requirements for the degree of PhD in Comparative Physiology, University of Oregon at Eugene, 1972. We are grateful to Dr M. J. Cohen, Dr S. B. Kater, Dr H. B. Hartman and Dr M. Burrows for advice and support and to Mr L. Vernon for technical assistance. Supported USPHS grant ROl NBO 1624 to M. J. Cohen, NIH training grant 671 2Tl GM336, and NIH grant 1 F02 NS47, 792-01 to M. L. P.
REFERENCES
Cohen M. J. (1955) The function of receptors in the statocyst of lobster, Homarus americanus. J. Physiol. 130, 9-34. Cohen M. J. (1960) The response patterns of single receptors in the crustacean statocyst. Proc. R. Sot. E. 152, 3&49. Cole W. H. (1941) A perfusing solution for the lobster (Homarus) heart and the effects of its constituent ions on the heart. J. gen. Physiol. 25, 16. Davis W. J. (1968) Lobster righting responses and their neural control. Proc. R. Sot. B. 70, 435456. Hartman H. B. and Boettiger E. G. (1967) Functional organization of the propus-dactylus organ in Cancer irroratus, Say. Comp. Biochem. Physiol. 22, 651-663. Lang D. and Yonge C. M. (1935) The function of the tegmental glands in the statocyst of Homarus americanus. J. mar. biol. Ass. U.K. 20, 333-339.
Mill P. J. and Lowe D. A. (1972) An analysis of the types of sensory units present in the PD proprioceptor of decapod crustaceans. J. exp. Biol. 56, 509-525. Murphy G. J. (1957) Basic Automatic Control Theory. pp. 527. D. Van Nostrand, Princeton, N.J. Ozeki M.. Takahata M. and Hisada M. (1978) Afferent response patterns of the crayfish statocyst with ferrite grain statolith to magnetic field stimulation. J. camp. Physiol. 123, l-10. Patton M. P. and Grove R. F. (1992) Statolith hair movements and the regulation of gravity reflexes in the lobster, Homarus americanus. Comp. Biochem. Physiol. IOIA, 259-268.
Sandeman D. C. and Okajima A. (1972) Statocystinduced eye movements in the crab, Scyl/a serrata. I. The sensory input from the statocyst. J. exp. Biol. Sr, 187-204. Schdne H. and Steinbrecht R. A. (1968) Fine structure of statocyst receptors of Astacus fidviatilis. Nature, Lond. 220, 184-186. Stein A. (1975) Attainment of positional information in the crayfish statocyst. Porrschr. Zool. 23, 109-119.
Lobster statocyst receptors Takahata M. (1981) Functional differentation of crayfish statocyst receptors in sensory adaptation. Comp. Biochem. Physiol. @A,
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Takahata M. and Hisada M. (1979) Functional polarization of statocyst receptors in the crayfish Procambarus clarkii, Girard. J. camp. Physiol. 130, 201-207.
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Wiersma C. A. G. (1959) Movement receptors in decapod Crustacea. J. Mar. Biol. Ass. U.K. 38, 143-152. Wiersma C. A. G and Boettiger E. G. (1959) Unidirectional movement receptors from a proprioceptive organ of the crab, Carcinus maenas. J. exp. Biol. 36, 102-I 12.
