(Received 28 May 1974)
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1 J. Phy.iol. (1975), 245, pp With 6 text-figurem Printed in Great Britain RECEPTIVE FIELDS IN CAT SUPERIOR COLLICULUS AFTER VISUAL CORTEX LESIONS BY NANCY BERMAN AND MAX CYNADER From the Department of Anatomy, School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A. and the Department of Psychology, Dalhousie University, Halifax, Nova Scotia, Canada (Received 28 May 1974) SUMMARY 1. The superior colliculus has been studied in intact cats and in cats with visual cortex lesions by recording the responses of single tectal units to visual stimuli. 2. Three classes of units have been identified in the superficial layers of the colliculus in these visually decorticate cats. 3. One class, comprising 5 % of the units studied, has receptive fields organized concentrically in a manner similar to retinal ganglion cells. 4. The second class, comprising 12 % of the units studied, responds to stimulus velocities over 300/sec, responds well to both small and large stimuli, and can be driven by strobe flashes at frequencies up to 35-40/sec. These units are termed 'flicker' cells. 5. The third class comprising 83 % of the units studied, responds best to stimuli which are not larger than the activating region of the receptive field, moving at relatively low velocities. These units show strong suppressive surrounds which are sensitive to higher velocities of stimulus movement than the central activating region. Responses from the activating region in these units are dramatically inhibited by flickering changes in the level of background illumination. 6. In intact cats few units are found which are strongly inhibited by background flicker. 7. It is suggested that a high-velocity sensitive element such as the 'flicker' cell or phasic retinal ganglion cell is responsible for the flickerinduced inhibition of collicular units in the visually decorticate cat.
2 262 NANCY BERMAN AND MAX CYNADER INTRODUCTION In recent years increasing attention has been focused on the role of midbrain structures, particularly the superior colliculus, in visual information processing. Cats with bilateral lesions of area 17 are able to perform surprisingly well on a wide variety of behavioural tasks including pattern discrimination (Doty, 1971). The spared visual capacities may be mediated through the superior colliculus and its efferent pathways to the posterior thalamus which projects in turn to the visual association areas (Graybiel, 1972). We and others have therefore been interested in studying how the superior colliculus processes the retinal input in the absence ofthe visual cortex. In studies of anaesthetized cats (Wickelgren & Sterling, 1969; Rosenquist & Palmer, 1971; Berman & Cynader, 1972) it has been found that visual cortex lesions alter two properties of collicular units: ocular dominance and direction selectivity. In the intact cat about two-thirds of the collicular units are direction selective, but after visual cortex lesions this feature is seldom found. Most units in the superior colliculus of the intact cat can be driven well by either eye, but after a visual cortex lesion the ipsilateral eye becomes much less effective than the contralateral eye. The work reported here was directed toward a closer study of the receptive field properties of collicular cells in the superficial layers after ablation of visual cortex. In so doing, we investigated the responses of these neurones to broad-field background strobe flashes and to stimuli of varied velocity moving through the receptive field. We compared the responses of collicular units to these stimuli in intact and visually decorticate cats, and we have distinguished three types of units in the decorticate colliculus. METHODS Visual cortex, including areas 17, 18 and 19, but sparing the Clare-Bishop area was unilaterally removed in nine cats days before the recording session. To do this, animals were first anaesthetized with i.v. sodium pentobarbitone (Neinbutal, Abbott) and then, after i.v. injection of 4 g mannitol (Osmitrol, Travenol Laboratories) in 20 ml. water, the visual cortex of one hemisphere was removed by subpial suction. Sterile conditions were maintained throughout. The procedures for preparing the animals, visual stimulation, recording, and reconstructing the lesion have been previously described (Cynader & Be; man, 1972; Berman & Cynader, 1972). Anaesthesia was initiated with i.v. sodium thiopentone (Pentothal, Abbott), and the cats were maintained on a mixture of nitrous oxide and oxygen during recording. We recorded extracellularly from single units in the superior colliculus using glass-coated platinum-iridium micro-electrodes. Paralysis was maintained by continuous infusion of a mixture of tubocurarine chloride (1-5 mg/hr), gallamine triethiodide (14 mg/hr), and 5% lactated dextrose in Ringer (Hartmann's solution) (3-4 ml/hr). Background illumination was 5-0 cd/m2 and stimuli were 1-2 log units above background. A Grass photostimulator produced 750,000 candlepower strobe flashes with 10 microsec durations. 226 units were studied in nine cats following visual cortex lesions. Sixty-two units were studied in three intact cats.
3 DECORTICATE CAT SUPERIOR COLLICULUS 263 RESULTS A. Concentric receptive fields The first group of cells, which comprised about 5 % of the units found in the superficial colliculus of cats with visual cortex lesions, has receptive fields which are organized similarly to those of retinal ganglion and lateral A B C Flicker Concentric 10 Suppressive su rrou nd 30L oh 1 ~ ~~~~~s lo& a_, 11 1i1_1 Annulus S 180 ~~~~~~On On Off I. 1 sec On Off Fig. 1 A. Post-stimulus time histograms illustrating the sum of 40 responses of a unit with a concentrically organized receptive field to spots of various sizes and annuli projected on to its receptive field. The responses to the 10 and 30 spots are to stimulus onset, with the responses to the 30 spot clearly more vigorous. The response to the 8 spot is much weaker and when an annulus with an inner diameter of 3. 5 is used, pure 'off' responses are obtained. Stimulus cycle: 2 sec, activating region size: 3. B, histograms illustrating the sum of forty responses of a 'Flicker' cell in the superior colliculus to spots of various sizes. 'On' and 'off' responses are obtained with stimuli of all sizes and even stimuli much larger in size than the activating region produce good responses. Stimulus cycle: 2 see; activating region size: 6. C, histograms illustrating the sum of forty responses of a unit in the colliculus to spots of various sizes. 'On' and 'off' responses are obtained with stimuli smaller than the size of the activating region, but the larger stimulus evokes much weaker responses. Stimulus cycle: 2 see; activating region size: 30. Off
4 264 NANCY BERMAN AND MAX CYNADER geniculate cells. Their receptive fields consisted of 'on' and 'off' regions arranged concentrically. Some of the units of this group may have been retinal afferent fibres, but others were certainly cells for they could be activated by stimulating either eye, although the contralateral eye was usually more effective. Both 'on' and 'off' centred units giving either tonic and phasic responses (Hoffmann, 1972; Cleland et al. 1971; Fukada & Saito, 1971) could be identified, although phasic responses to flashed stimuli were predominant. Fig. IA illustrates the response of a phasic on-centre unit to spots of various sizes flashed in the receptive field. The unit gives vigorous 'on' responses to the 10 and 30 spots while the response to the 80 spot is much weaker. An annulus with an inner radius of 3.50 evokes 'off' responses exclusively. The latency for this unit was 40 msec which is typical (30-50 msec) for units of this type. These units will often respond to onset or offset of diffuse illumination and also to strobe flashes. Response to strobe 10 spikes k. Aiz_ t 30 msec l -i Fig. 2. A post-stimulus time histogram illustrating the sum of 16 responses of a 'flicker' cell to diffuse strobe flashes, stimulus cycle: 256 msec; 2 msec/bin, 128 bins. Arrow indicates time of strobe flash. B. 'Flicker' cell A second group of cells was termed 'flicker' cells because they responded to and followed high frequency flicker in the level of background illumination. These units comprised 12 % of the cells encountered in the superior colliculus following visual cortex lesions. They are distinguished from other tectal units by the following properties: (1) short latency of response to flashed visual stimuli (28-40 msec); (2) extremely broad velocity tuning; (3) ability to follow stimuli presented at high frequencies and (4) extremely weak surrounds. These cells were not direction selective and they responded at stimulus velocities beyond 300'/sec. Crisp 'on' and 'off' responses to both small and large stimuli were obtained when the stimuli were flashed anywhere within the receptive field. Fig. lb illustrates the response of one unit of this type to flashing spots of various sizes. Stimuli much larger than the receptive field evoked vigorous responses. The flicker cells were responsive to transient changes in diffuse illumination
5 DECORTICATE CAT SUPERIOR COLLICULUS 265 (usually to both on and off) and also to strobe flashes. They could be driven at very high rates by diffuse strobed light and in some cases would follow each presentation of the strobe at frequencies of up to flashes/sec. In a few cases, we noted that the pattern of responsivity to the flickering environment changed from a phase-locked relationship to one in which the unit exhibited a high-frequency firing rate which was no longer synchronized with the photostimulator. This is similar to the phenomenon of photically-induced activity described by Saito & Fukada (1973). The most characteristic response for this type of neurone, however, was a burst of several spikes after each strobe flash with a second weaker burst sometimes appearing later. The response of a typical unit to strobe flashes is shown in Fig. 2. Surround inhibition 20 =, msec Fig. 3. A histogram representing the unit's response to a 150 x j' line moved back and forth across the receptive field. A I' spot was moved constantly within the activating region of the receptive field to increase the unit's firing rate. Stimulus cycle: 1 sec, stimulus excursion: 160 in each direction, stimulus velocity: 320/sec, 128 bins. C. Units inhibited by background flicker The third type of tectal unit is characterized by a somewhat longer latency ( msec as a group), a tighter velocity tuning, and a suppressive surround. These units comprised 83 per cent of the cells encountered in the superior colliculus after visual cortex lesions. They were not direction selective and responded to onset and/or offset of stimuli presented anywhere within the activating region. Stimuli extending outside the activating region evoked weaker responses presumably because of encroachment on to the suppressive surround. The optimum stimulus was often smaller than the size of the activating region. Fig. 1C illustrates the response of a unit of this type to a stimuli of various sizes. Most of these units responded
6 266266NANCY BERMAN AND MAX CYNADER optimally to stimuli moving at velocities between 1 and 30'/sec. The responses of units in this third group were more erratic than those of the first two and the responsivity to the visual stimulus tended to wax and wane unpredictably. This last class of collicular units usually exhibited clear suppressive surrounds, and we attempted to examine some response charactertistics, of these suppressive receptive fields. We raised the unit firing level with an effective stimulus, such as a small moving spot, while simultaneously moving a long slit back and forth across the receptive field. The inhibitory effect of the slit was then revealed as a lowering of the base line of the post-stimulus histogram. A similar procedure has been employed by Bishop, Coombs & Henry (1973) to assess inhibition in the striate cortex. The results of a typical analysis of this type are shown in Fig. 3. The inhibitory receptive field of this unit exhibited neither orientation nor direction selectivity, but did exhibit a much broader velocity tuning than the excitatory responses in the same unit. A slit moved across the receptive field at 320/sec produced clear inhibition whereas excitatory responses with small spots were not obtainable from this unit at stimulus velocities above 50/sec. In studying the influence of diffuse strobe flashes on this class of collicular units, we noted that a striking and powerful inhibitory effect could be obtained by flickering changes in the level of background illumination. Fig. 4A shows a histogram illustrating the response of a typical unit to a small moving spot in the steady-state condition. The peaks show that the unit fires vigorously in both directions as the spot traverses the receptive field. The inhibitory effect of diffuse strobe flashes at 20 Hz is illustrated in Fig. 4 B which shows that there is virtually no response at all to the previously effective stimulus in the presence of the background flicker. It seemed possible that the inhibitory effect of the background flicker was due simply to a lessening of the contrast of the visual stimulus. This possibility was examined by varying the frequency of the background flicker. Fig. 5 is a graph of the number of spikes/minute in the response of a representative neurone to a continuously moving spot as a function of the frequency of the background flicker. Were the inhibitory effect merely a consequence of decreased stimulus contrast, one would expect that the curve in Fig. 5 would be a monotonic function of frequency. However, this is not the case. The inhibitory effect does increase up to 37 flashes/ second but, quite suddenly, the effect disappears at about 40 Hz and the unit again responds vigorously to the moving visual stimulus. These data show that the decreased contrast of the stimulus is not a major factor in the lessened responsivity of the unit. The latency and duration of the inhibition produced by each flash
7 DECORTICATE CAT SUPERIOR COLLICULUS 267 were studied by raising the firing rate of the unit with an effective stimulus and then using the flash from the photostimulator to trigger an averaging device. As in Fig. 3, the inhibitory effect of the stimulus is then visualized as a lowering of the baseline of the post-stimulus-time histogram. The histogram in Fig. 6 taken from a representative unit shows Moving spot 30 -A Moving spot background flicker 8 C._ 0 15._ UL Fig. 4A. A histogram representing the sum of 16 sweeps of a I' spot moving back and forth across the unit's receptive field. The arrows indicate the direction of stimulus movement. Stimulus cycle: 16 sec, stimulus excursion: 80 in each direction, stimulus velocity: 1V/sec, 128 bins. B, the response of this unit to the same stimulus in the presence of 20 Hz background flicker. The histogram represents the sum of 16 sweeps of a I' spot moving back and forth across the unit's receptive field. The arrows indicate the direction of stimulus movement. Stimulus cycle: 16 sec, stimulus excursion: 80 in each direction, stimulus velocity: 1V/sec, 128 bins. that inhibition of unit discharge could be observed 40 msec after the strobe flash and that this inhibition is quite long-lived with a clear suppression of the unit's responsivity still noted 200 msec after the background flash. In other units we noted inhibition for up to 400 msec after single strobe flashes. The latency of inhibition following the strobe flash was usually within the range of msec.
8 268 NANCY BERMAN AND MAX CYNADER These inhibitory effects were observed in nearly all units of this type tested in this way. Many units were completely unresponsive to normally adequate stimuli when the background level of illumination flickered \ 125 7S E , I Strobe frequency (Hz) Fig. 5. Responses of a unit inhibited by background strobe flashes as a function of strobe frequency. The ordinate represents the number of spikes obtained during 1 minute of response to a 1 spot moving continuously back and forth through the unit's receptive field at 50/sec. The abscissa represents the frequency of background strobe flashes. Inhibition by strobe 10 spikes WONLA06A.L.. a. A A a a.,& a &JL msec Fig. 6. A post-stimulus time histogram illustrating the inhibitory response to background flicker. The histogram represents the sum of the response to sixty-four presentations of the strobe flash. Stimulus cycle: 640 msec; 5 msec/bin, 128 bins.
9 DECORTICATE CAT SUPERIOR COLLICULUS 269 To determine whether this effect was confined to the decorticate colliculus, we studied the influence of background flicker on the response characteristics of 62 units in the colliculus of intact cats. In the intact cat colliculus units were only relatively weakly influenced by the flickering background. Fourteen units were excited or facilitated, fifteen were inhibited, seven were modulated by the background flicker (a combined effect of excitation and inhibition), and twenty-six were unaffected by the background flicker. DISCUSSION Three unit types have been found in the superficial layers of the decorticate colliculus. Two of the three unit types represent only a small percentage of the units encountered in the decorticate colliculus but are distinguished by their characteristic receptive-field properties. The first class of units resembles retinal ganglion cells in its receptive field properties. Wickelgren & Sterling (1969) also found an increase in the proportion of concentrically organized units in the cat colliculus after visual cortex lesions. The second class of units, or 'flicker' cells are in many ways similar to the phasic retinal ganglion cells described in the retina (Cleland et al. 1971, Fukada & Saito, 1971). Phasic retinal ganglion cells also respond to stimulus velocities beyond 300'/sec and are able to follow high frequency flicker. Both phasic retinal ganglion cells and 'flicker' cells occasionally exhibit the phenomenon of photically induced activity described by Saito & Fukada (1973); that is, at certain frequencies of strobe presentation they stop responding to each flash but instead fire continuously at a rate much higher than their spontaneous rate. It seems likely from the receptive field properties and short-latency responses of the 'flicker' cells that they are directly influenced by phasic retinal ganglion cells. The 'flicker' cells, however, are clearly distinguishable from phasic retinal ganglion cells since the receptive fields of the 'flicker' cells are not divisible into discrete 'on' and 'off' areas while those of phasic retinal ganglion cells are concentrically organized. It has recently been found that a special class of retinal ganglion cells called W cells projects heavily on to the cat colliculus and may form the bulk of the retinocollicular projection (Hoffman, 1972). W cells in the retina are characterized by mixed 'on-off' receptive fields, relatively low velocity tuning and a slow conduction time to the colliculus. The receptive field properties of the third group of collicular units are similar to those of retinal W cells and we suggest that W cells may play a major role in determining the receptive-field characteristics of these neurones. To date there have been no investigations of suppressive surrounds in the W retinal ganglion cells and so it is not possible to compare directly the
10 270 NANCY BERMAN AND MAX CYNADER surround properties and inhibition by background flicker in the slow velocity collicular units with the surround properties of the W ganglion cells. The units in the decorticate colliculus which are inhibited by background flicker show different velocity tuning for the activating region and suppressive surround. While the units will generally respond more weakly to spots moving more rapidly than 30'/sec, the response can be suppressed by a stimulus in the surround moving as fast as 300'/sec. This suggests that the suppressive surround of these units is made up of a high velocitysensitive element. The most likely candidates for this function are the flicker cells in the colliculus or the phasic retinal ganglion cells. The surround influences are extremely powerful in the decorticate colliculus since over two-thirds of the units were strongly inhibited by high frequency flicker of the entire visual field. Under these circumstances the experimenter had no difficulty perceiving the now ineffective stimulus, and units in the colliculus of the intact cat are only relatively weakly influenced by this flickering environment. It seems likely that if the colliculus is important in the visual capacities remaining after cortical ablation, a pronounced decrement in these spared visual capacities would be found if the cats were tested in the presence of a high frequency background flicker. This research was supported by Grant Number MA-5201 from the Medical Research Council of Canada. REFERENCES BERMAN, N. & CYNADER, M. (1972). Comparison of receptive-field organization of the superior colliculus in Siamese and normal cats. J. Physiol. 224, BISHOP, P. O., COOMBS, J. S. & HENRY, G. H. (1973). Receptive fields of simple cells in the cat striate cortex. J. Physiol. 231, 3f-60. CLELAND, B. G., DUBIN, M. W. & LEVICK, W. R. (1971). Sustained and transient neurones in the cat retina and lateral geniculate nucleus. J. Physiol. 217, CYNADER, M. & BERMAN, N. (1972). Receptive-field organization of monkey superior colliculus. J. Neurophysiol. 35, DOTY, R. W. (1971). Survival of pattern vision after removal of striate cortex in the adult cat. J. comp. Neurol. 143, FUKADA, Y. & SAITO, H. (1971). The relationship between response characteristics to flicker stimulation and receptive-field organization in the cat's optic nerve fibers. Vision Res. 11, GRAYBIEL, A. M. (1972). Some fiber pathways related to the posterior thalamic region in the cat. Brain, Behav. & Evol. 6, HOFFMANN, K. P. (1972). The retinal input to the superior colliculus in the cat. Invest. Ophthal. 11, RoSENQUIST, A. C. & PALMER, L. (1971). Visual receptive field properties of cells in the superior colliculus after cortical lesions in the cat. Expl Neurol. 33, SATO, H. & FUKADA, Y. (1973). Repetitive firing of cat's retina] ganglion cell. Vision Res. 13, WICKELGREN, B. G. & STERLING, P. (1969). Influence of visual cortex on receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32,
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