Saccade correlated potentials in optic tectum and cerebellum of Carassius auratus

~RAIN RESEARCH

293

SACCADE C O R R E L A T E D POTENTIALS IN OPTIC T E C T U M AND C E R E B E L L U M OF C A R A S S I U S A U R A T U S HOWARD T. HERMANN Neurophysiology Laboratory, McLean Hospital, Belmont, Mass. 02178 and Department of Psychiatry, Harvard Medical School, Boston, Mass. (U.S.A.) (Accepted September 1st, 1970)

INTRODUCTION

The turning movements of teleost fish include highly regularized eye movements. Typically (in alert undisturbed fish), a conjugate horizontal eye saccade in the direction of the turn initiates the coordinated motor pattern of the turn. The eye movements consist of sharp saccades in the direction of turning, with a slow counter motion following each saccade that probably reduces or prevents slip of retinal image12, 21. Immobilized, spinal cord transected goldfish, maintained in total visual darkness, exhibit eye movements resembling those of the free swimming fish. These consist of conjugate saccadic shifts sweeping from side to side, each sweep composed of several saccadic steps 12. The present paper describes slow potentials that are correlated with saccadic eye movements recorded in the optic tectum and cerebellum of Carassius auratus. METHOD For surgical anesthesia, I immersed the fish (5-7 in. size) in a tap water solution of methane tricaine sulfonate (approximately 0.5 g/l) until the fish was unresponsive (usually within 5 rain). I then transferred it to a dechlorinated aerated tap water circulator of 15 1 capacity which, via oral intubation, pumped a continuous flow of water over the gills. Anesthesia lasted about 15-20 min, sufficient to (a) cut a dorsal window into the skull (avoiding the vestibules); (b) aspirate the fatty mucoid gel overlying the brain; and (c) transect the spinal cord at C1. The skull was drilled to accept several 0.5 in. No. 1 wood screws and the head was immobilized by cementing together the skull, inserting screws and applying a rigid headholder with dental acrylic 12. Within 0.5 h, the return of brisk eye movements signaled recovery from anesthetic and surgery*. Recording electrodes were glass-coated, electro-sharpened, tungsten needles, thinned over the last 3 mm to --~40-50 # m diameter shaft and insulated terminally with epoxylite to ~ 40/zm from the tip**. These were cemented into stainless steel tubes, * Adaptation of enc6phale isol6 preparation of fish developed by Dr. David Ingle. ** Adaptation of microelectrode developed by Professor D. H. Hubel (Sc&nce, 125 (1957) 549-550), Brain Research, 26 (1971) 293-304

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singly or as depth-staggered pairs (one needle set 250/tm deeper than the other with a lateral separation of ~ 250 #m). Grass P-14 preamplifiers with one-half power points set at 0.1 c/sec and 1 kc/sec amplified the brain signals. Connections were such that a positive signal into the upper (or equivalently, monopolar) electrode produced a positive output. Unless otherwise indicated the reference electrode was placed in the midline on the exposed muscles over the C2/C3 region. A multi-channel F M / A M tape recorder (P1 6108) running at 3.75 in./sec stored (1) the raw nerve pulse data, (2) synchronizing signals, and (3) analog output of the eye position detectors. A multitrace cathode ray oscilloscope and/or an optical oscillograph (Honeywell 'visicorder') provided continuous monitoring of all data. For signal averaging, I used a FabriTek 1062 preprogrammed digital computer. The synchronizing pulse was generated by a unidirectional rate sensitive electronic circuit that emitted a pulse whenever its threshold was exceeded (saccade detector). Eye position signals were always normalized to a zk 2 V maximum amplitude range so that the essential variables were the slope and direction of the eye position signal, together with the relative saccade amplitude*. Typically, the circuit emitted a signal 5-10 msec after the onset of the high velocity phase of the saccade. The characteristic phase relation of the synch pulse to the saccade may be seen in Figs. lb and 5. I wished to examine the averaged record before the saccade, as well as during and after. The precise transit delay from record head to readout head (1.4 sec) enabled me to pass data from the readout head to the computer at a point on the tape preceding the saccade**. The sequence was as follows: (1) the synchronizing pulse from the saccade detector signaled the onset of a saccade and started an external adjustable fixed delay circuit of a duration less than record/readout transit time. At that same instant, the synchronizing pulse, eye monitor signal and raw nerve signals were being recorded on tape at the record head site ('zero time site'); (2) at the end of the external delay interval, the delay circuit emitted an enabling pulse that started the computer. At this moment in time, the zero time site on the tape had not yet reached the readout head. Since the computer received its data from the tape readout head, the data accepted, beginning at the instant of the enabling pulse, lay on the portion of tape that preceded the zero time site of the eye saccade event. The computer then continued through the portion of the tape containing the saccade and into its aftermath. Eye movement sensors consisted of a pair of infrared sensitive photodiodes (G. E. L 14B) connected in a bridge circuit and centered on each eye3,12. These responded to the infrared (IR) energy reflected from a ~ 4 mm × 4 mm square patch of aluminum foil cemented to an opaque corneal lenscap. The IR source was a subminiature tungsten lamp run at 0.5 nominal voltage, placed in a blackened tube between the photodiodes, the port filtered by an Eastman Wratten filter (87a). The inequalities in reflected IR generated an analog current flow ( = voltage change) in the bridge circuit,

* Mr. R. E. Olsen designed the eye monitor and saccade detector. The saccade detector showed a triangular bandpass, with 6 dB rising and falling slopes and a peak at 30 c/sec. ** Mr. David Butz suggested the use of tape transport delay for pre-saccadic averaging.

Brain Research, 26 (1971) 293-304

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~J Fig. i. a, Simultaneous bilateral eye monitor and bilateral tectal records during saccadic movements of the eye. N and T refer to direction (nasal, temporal) of gaze shift in each eye. LEM, REM refer to left and right eye monitor output. Tect. refers to optic tectum. Vertical broken line is placed for grid alignment, b, Averaged bilateral TSEP and bilateral eye monitor output from the same preparation synchronized by REM and LEM respectively. Vertical dashed lines represent instant of synchronization referred to each eye monitor. Eye monitor output: 16 averaged traces; TSEP: 32 averaged traces. Eye monitor averages taken from same portion of record as TSEP. Electrode depth 125/~m. Inset diagram refers to electrode positions; © (circle) = reference; × = probe; Cb = cerebellum; OT = optic tectum.

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sensed by the subsequent logic circuits and displayed on the CRO. The gain and zero balance of each eye monitor was set to record a shift of 4 V ( ± 2 V) correspondent to the full excursion of eye movement (extreme nasal to extreme temporal). When necessary during an experiment the system was adjusted to maintain the ± 2 V deflection. The eye monitors registered voltage values proportional to and monotonic with saccade excursion over the entire range. Typical total eye excursions ranged from 12 to 32 ° (by direct visual measurement) and the eye monitor system proved to be linear for eye movements encountered in all but 2 of the over 40 experiments performed for this research 12. The LI4B diodes had a delay of 60 /zsec and rise time of 250 #sec, well above the highest saccade velocities encountered (rise time of 20-100 msec). For all mechanical stimulation experiments the extraocular muscles were dissected free from their insertions (except for retractor bulbi). A 15 cm length of 20gauge hypodermic needle tubing was fastened to the voice coil of a high compliance speaker. The blunted end of the tubing poked the eye directly. A step change of current drove the voice coil (and therefore the tubing) through a displacement variable from 0 to 4- 2 ram, with a rise time of 20 msec at full displacement. Eye muscles were stretched by linking them to the tubing with 6/0 thread. RESULTS

Surface recordings In dark adapted preparations, following the onset of each conjugate saccade, with latencies varying from 50 to 200 msec, one can detect in the CRO traces from the dorsal surface of both optic tecta a negative going slow wave, typically ,-~ 150-200 msec in duration and ,- 100-400/zV. Even when not directly visible, averaged response computation always reveals its presence. A saccadic evoked potential (SEP) appears also in the superficial folia of the cerebellum (especially v a l v u l a ) b u t not on forebrain, diencephalon or rhombencephalon. Fig. la shows a typical recording of tectal SEP (TSEP) together with the simultaneous eye monitor recordings. The eye monitor traces in Fig. la show a terminal sharp 'overshoot' in the leftward conjugate gaze saccade of each eye, in contrast to the smoothly damped termination of the rightward gaze saccade 12. About 200 msec after each saccade onset, one can detect negative going slow waves in the tectal traces. Despite the differences in direction, waveform and amplitude of the two conjugate saccades, the TSEP waveforms appear to be grossly similar. In this recording the saccadic movement clearly stopped before the onset of the TSEP. This is not always so; at times the TSEP begins during the terminal phase of the saccade. But always, the TSEP onset lags that of the saccade. Fig. lb shows the averaged records of 16 saccades (5 ° or greater in amplitude), all of which were in the same direction, recorded in total visual darkness. The TSEP duration was ~220 msec, starting ~ 180 msec after the saccade onset, ,-~ 130 msec after the termination of the saccade. The time measurements are approximate owing to the residual baseline fluctuation and arbitrary criterion of waveform onset. In some

Brain Research, 26 (1971) 293-304

SACCADECORRELATEDPOTENTIALSIN OPTIC TECTUM

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Fig. 2. a, First (left) column: samples of TSEP depth study in dark adapted goldfish. TSEP averaged over 32 events using right eye nasal saccadesto generate the synchronizingpulse (vertical dashed line). Inset diagram refers to electrode positions, b, Second and third columns: Different preparation, same format and parameters; simultaneous recordings at different sites, but identical depths (375 Fm; 750/~m; 1500/~m). preparations, a positive going wave continues the upsweep of the negative wave, producing a biphasic waveform. When present, the positive after potential is broader, with durations in the order of 150-200 msec.

Depth studies Scotopic: Averaged TSEP at successive depths (usually 62 • 5 # m steps) reveal a successive graduation of polarity changes, with the loss of negative wave occurring around the 500-750 #m depths and the appearance at deeper levels of a positive wave of the same latency. The changes occur similarly wherever one probes in such a radial path, anteriorly or posteriorly, in one tectum or the other. Fig. 2a shows representative traces of a series of averaged records from left tectum, taken via a monopolar electrode just medial to the intersection of the horizontal and vertical projection meridians 16. Fig. 2b (from another preparation) shows the same surface negative/null/deep positive sequence, as recorded simultaneously at two different points on the rectum. Brain Research, 26 (1971) 293-304

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H . T . HERMANN

NASAL SACCADE ELECTRODE RENETRATION DEPTH (H')

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Fig. 3. Depth study of tectal photic evoked potentials (TPEP) each averaged over 16 events using temporal saccades of left eye for synchronization (vertical dashed line). Inset diagram refers to electrode position.

TSEP at locations more medial and rostral show varying degrees of positivity in the TSEP, giving a more biphasic appearance. In the most medial extent the TSEP shows largely positive going potentials, but similar in latency to the more lateral negative waves. Photopic: TSEP differ in waveform and latency from photic, movement evoked potentials (TPEP). To distinguish TSEP from the tectal photic evoked potential, I applied an opaque corneal patch over the pupil and illuminated the eye with enough photic energy ( > 650 nm) to produce a well-defined photic response without swamping the TSEP. Until the electrode tip reached 250 #m, the TPEP was not evident, the TSEP being the main detectable waveform at the superficial levels (Fig. 3). Beginning at a depth of 312 # m the TPEP emerged as a sharp, well-defined positive wave, growing in clarity and amplitude until it reached a maximum at ~ 562 #m. It showed a characteristic double peaked 'M' shape with little waveform variability. (The second hump appeared at deeper levels.) At ~ 562 #m the latency of the response decreased. Even at this relatively reduced level of photic stimulation, the TPEP dominated the records in the 500-800 #m levels. At the deepest levels (beyond 1000 #m) the waveforrn resembled the SEP of the dark adapted state. Brain Research, 26 (1971) 293-304

SACCADE CORRELATEDPOTENTIALSIN OPTIC TECTUM

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Fig. 4. Mechanical stretch of abducens muscle bundle in dark adapted state, a, Control, slack thread! b, Stretch. Averaged over 16 events. Vertical dashed line refers to onset of stretch.

Effects of mechanical deformation of globe and extraoeular eye muscle Poking the eye globe at the scleral rim through a step displacement of 2 mm failed to produce a detectable tectal wave when recording in total darkness. Sudden stretch of the eye muscles in the dark, through a 0.5 mm displacement (equivalent to a 500°/sec of eye rotation) produced an evident negative going wave with a late, positive, after potential in the tectum (Fig. 4). In this experiment I stretched the left abducens and recorded in the right tectum. The total latency was about 15 msec (including rise time of 10 msec).

Effect of removal of proprioceptor afferent feedback The tectal waves evoked by mechanical stretch of extraocular muscles speak strongly in favor of proprioceptor afferent contribution directly or indirectly to the TSEP. To explore this possibility further, I removed the proprioceptor feedback of one eye by dissecting off the eye muscles from the globe. .... Using the saccadic synchronization of the intact eye, I averaged TSEP from both tecta. Prior to dissection(Fig, lb) one sees typical TSEP bilaterally. The post-dissection, averaged records reveal the effectiveness of the dissection (Fig. 5). Although movement appears in the nasal LEM recording, it is extremely small. The gain of the left eye monitor had been increased by a factor of.approximately 100. Thus, the averaged LEM record of Fig. 5 represents an extremely small movement (during its nasal saccade). The temporal saccadic movement (left column) vanished. The averaged REM increased relative to pre-dissection amplitude,

Brain Research,26 (1971) 293,304

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Fig. 5. Post-dissection records of experimental removal of proprioceptive input. Right and left eye monitor output averaged simultaneously. Same preparation and format as in Fig. lb. See text for explanation. The unilateral near complete removal of proprioceptive afferents affected the ipsilateral (left) tectum more than the contralateral (right). The amplitude in the left rectum fell to one-fourth of the original value (75 % decrease) as opposed to a 30 % decrease in the contralateral tectum. The latencies did not appear significantly altered, nor did the duration of the negative wave. Immobilization of the left eye exaggerated the saccadic motion of the right eye. Despite the larger amplitude saccades, the contralateral TSEP are less than pre-dissection amplitudes. Saccadic evoked responses in the cerebellum Pilot studies had revealed slow waves and unit responses correlated with eye saccades in the caudal dorsal convexity of the cerebellum and the midline valvula. The cerebellar saccadic evoked potentials of the midline valvula (CSEP) differ from the TSEP in several aspects: (1) they start before the onset of the eye saccade; (2) a positive going, high amplitude slow wave begins the complex; and (3) the overall waveform of the CSEP is pronouncedly biphasic, the initial positive wave being followed by a deep negative wave and a final small late positive wave. Fig. 6a illustrates samples of a successive depth penetration in the midline of the valvula of the cerebellum (see inset diagram). The vertical dashed line represents the instant of saccade synchronization. These records were obtained by synchronization with left eye nasal saccades. The track of the electrode was in a parasagittal plane ~ 100 mm lateral to the midline, passing successively through tectal commissural fibers, valvula, ventricle and mesencephalic floor. The data show three distinct regions: (a) surface to 250/~m positive wave, (b) a post-saccadic potential inversion from 500 # m to 750/~m and (c) a Brain Research, 26 (1971) 293-304

SACCADE CORRELATED POTENTIALS IN OPTIC TECTUM

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200 msec Fig. 6. a, Samples of depth study of slow potentials correlated with saccadic eye movement in the valvula of cerebellum, averaged over 16 events. Staggered bipolar electrode. Reference electrode in muscle over dorsal cervical spine, b, Different preparation, same format and parameters, averaged at successive sites along a midsagittal path on surface of valvula cerebelli.

large positive potential around 1000 #m beginning before the saccade onset. This last was similar in waveform and timing to the valvula surface potentials. Fig. 6b, from a different preparation, shows typical variations in waveform encountered along a rostro-caudal midline path over the valvula surface.

Variations of SEP due to direction of conjugate saccadic gaze shift In every preparation, TSEP of a conjugate saccade in one direction differed at least slightly but highly consistently from TSEP due to opposite direction conjugate

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saccades. However, no consistent relationship could be found between saccade parameters or direction of conjugate saccade and the TSEP. DISCUSSION

Slow potentials precede, accompany and follow saccadic eye movements in the brain of the dark adapted enc6phale isol6 goldfish. The largest, most uniform, and earliest detected waves arise 1000.1200 #m beneath the midline surface of the valvula. At the same time, large surface waves erupt in the outer (0-250 #m) layers of the midline valvula, similar in form to the deep waves. Starting before the saccade onset, these waves peak during the high velocity phase of the saccade. Their timing corresponds grossly to pre-saccadic potentials found in pontine reticular formation of cat 5 and monkey6. During and after the saccade, slow waves occur in the outer layers of the dorsal cerebellar surface. Following the saccade (or during its terminal phase), in the region around the central retino-tectal projection, a monophasic surface negative wave appears in the outer layers of the tectum (0-400 #m) and a surface positive potential appears in the lateral valvula at a depth of ~ 1200 #m. Their timing corresponds grossly to the post-saccadic potentials seen in monkey9 and cat la. Depolarization of the radial dendritic trees rising from cells in the internal grey layer14 could generate the negative potential gradients seen in the tectum. The dendrites of these cells reach up to the afferent retinal plane. But they would not account for the deep positive wave, emerging well beneath the tectal layers (t200-1500 /zm), since no transitional potential inversion can be observed. (The 'null' region extends nearly 700/~m). At 1200-1500/~m beneath the tectal surface, the electrode tips are in the lateral valvula, a likely source of the deep positive potential. The reduction in amplitude of TSEP ipsilateral to the transection of extrinsic eye muscles, together with the sharp negative tectal wave produced by sudden eye muscle stretch, argue for a proprioceptor origin of TSEP. In the artiodactyl, Cooper et al. s demonstrated short latency, first order, stretch responses in single units of the mesencephalic root of the fifth cranial nerve. Fillenz1° confirmed this for the cat. In the fish (trout and bow fin19; goldfish14) the mesencephalic fifth root lies in the deepest nuclear layer of the rostro-medial aspect of the optic tectum. This does not match the observed distribution of TSEP. (The TSEP reaches a maximum in the lateral two-thirds of the tectum ~ 250 #m deep.) However, the ipsilateral projection of this root would be consistent with the predominantly ipsilateral effects of eye muscle removal. This hypothesis requires a short latency with respect to the saccade onset. But, TSEP lag the saccade by 50-200 msec, implying a polysynaptic pathway. TSEP could arise from proprioceptor excitation of other classes of cells. Cooper et al. s also noted long latency stretch responses of units in other midbrain sites (median longitudinal fasciculus and cerebellar pathways). 'Other multiunit responses were heard in the eye muscle nuclei themselves and in the deeper layers of the superior colliculus.' If teleost optic tectum and mammalian superior colliculus are homologous, TSEP might indicate similar activity/

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While the CSEP must register the saccade within eye-body postural coordinating systems of the cerebellum, the TSEP does not so easily suggest a function. Bizzi4, Michael and Stark 15, Gross et al. 11, Wurtz 20 and Collewijn 7 have all noted suppression of visual evoked responses during saccadic eye movement. None have noted suppression after the sacCade. If anything, then, TSEP must reflect a more complex sensory bias (for example, retinal image stabilization). The timing of the TSEP coincides with the onset of the slow pursuit phase in the free-swimming turn pattern of the teleostlL Thus, TSEP may signal onset of the 'visual grasp' operations of the tectum 1, shown also for the cat2,17,18; and artiodactyls. SUMMARY

(1) In the enc6phale isol6 goldfish, Carassius auratus, when recording in the dark adapted state, 50-200 msec after the onset of a conjugate eye saccade, a predominately negative potential, 150-200 msec in duration, with peak amplitudes ranging from 100 to 500 #V, appears over the lateral two-thirds of the optic rectum. (2) Recording at successive depths, the negative Wave decreases in amplitude, disappearing at a depth of ~ 500-750 /zm. A positive going potential emerges at depths of 1000-1250 #m, whose peak corresponds in time to the superficial negative wave peak; it originates in the valvula. (3) Potentials in the optic rectum evoked by saccadic eye movement in the light show shorter latency, more uniform, multiphasic waveform and absence of detectable potentials in the surface to ~ 300/zm levels of the tectal layers. (4) Stretch of the abducens eye muscle can produce a 5-10 msec latency, negative going wave in the contralateral tectum. Transection of all eye muscles of the globe reduces the amplitude of TSEP largely in the ipsilateral tectum, without change in waveform or timing. Also, saccadic movements of the opposite eye increase in amplitude. (5) The midline valvula of the cerebellum exhibits a pre-saccadic, positive going 200-600 #V slow wave. High amplitude slow potentials, starting before the saccade, occur 1200/zm beneath the valvula surface. (6) Mechanical distortion of the globe failed to produce any of these phenomena. ACKNOWLEDGEMENTS

This work was supported by Grants MH 2479 of the National Institute of Mental Health and General Research Support Grant FR 05484 of the National Institutes of Health. I am most grateful for the critical guidance of Professor J. Y. Lettvin in the early stages of this work. Miss Martha Constantine assisted in many of the experiments, and in the preparation of this paper, and collaborated in the exploration of the cerebellum potentials.

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REFERENCES 1 AKERT, K., Der visuelle Greifreflex, Helv. physiol, pharmaeol. Acta, 7 (1949) 112-134. 2 APTER, J. T., Eye movements following the strychninization of the superior colliculus in cats, J. Neurophysiol., 9 (1946) 73-86. 3 BARMACK,N., Photoelectric measurement of horizontal eye movements in monkeys, Vision Res., 10 (1970) 439-443. 4 BrzzI, E., Changes in the orthodromic and antidromic response of optic tract during the eye movements of sleep, J. Neurophysiol., 29 (1966) 861-870. 5 BIzZI, E., AND BROOKS, D. C., Functional connections between pontine reticular formation and lateral geniculate nucleus during deep sleep, Arch. itaL Biol., 101 (1963) 666-680. 6 COHEN, B., AND FELDMAN, M., Relationship of electrical activity in pontine reticular formation and lateral geniculate body to rapid eye movements, J. Neurophysiol., 31 (1968) 806-817. 7 COLLEWIJN, H., Changes in visual-evoked responses during the fast phase of optokinetic nystagmus in the rabbit, Vision Res., 9 (1969) 803-814. 8 COOPER, S., DANIEL, P. M., AND WHITTERIDGE, D., Muscle spindles and other sensory endings in the extrinsic eye muscles; the physiology and anatomy of these receptors and of their connexions with the brain stem, Brain, 78 (1955) 564-583. 9 FELDMAN, M., AND COHEN, B., Electrical activity in the lateral geniculate body of the alert monkey associated with eye movements, J. Neurophysiol., 31 (1968) 455-466. 10 FIELENZ, M., Responses in the brain stem of the cat to stretch of extrinsic ocular muscles, J. Physiol. (Lond.), 128 (1955) 182-199. 11 GROSS, E. G., VAUGHAN, H. G., AND VALENSTEIN, E., Inhibition of visual-evoked responses to patterned stimuli during voluntary eye movements, Electroenceph. clin. NeurophysioL, 22 (1967) 204-209. 12 HERMANN, H. T., AND CONSTANTINE, M., Eye movements in the goldfish, Vision Res., (1970) in press. 13 JEANNEROD, M., AND SAKAI, K., Occipital geniculate potentials related to the eye movements of the unanesthetized cat, Brain Research, 19 0970) 361-377. 14 LEGmSSA, S., La struttura microscopica e la citoarchitetonica del tetto ottico del pesci teleostei, Z. Anat. Entwickl.-Gesch., 118 (1955) 427-463. 15 MICHAEL, J. A., AND STARK, L., Interactions between eye movements and the visually evoked response in the cat, Electroenceph. clin. NeurophysioL, 21 (1966) 478-488. 16 SCHWASSMAN, H. D., AND KRUGER, L., Organization of the visual projection upon the optic tectum of some fresh water fish, J. comp. NeuroL, 124 (1965) 113-126. 17 STERLING, P., AND WICKELGREN, B. G., Visual receptive fields in the superior colliculus of the cat, J. Neurophysiol., 32 (1969) 1-15. 18 STRASCHILL, M., AND HOFFMAN, K. P., Functional aspects of localization in the cat's tectum opticum, Brain Research, 13 (1969) 274-283. 19 WEINBERG, E., The mesencephalic root of the fifth nerve. A comparative anatomical study, J. comp. NeuroL, 46 (1928) 249-405. 20 WURTZ, R. H., Visual cortex neurons: Response to stimuli during rapid eye movements, Science, 162 (1968) 1148-1150. 21 YOUNG, L. R., Pursuit eye tracking movements, Proc. Symp. Control of Eye Movements, San Francisco, 1969,

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