A parametric study of movement detection properties of neurons in the cat's superior colliculus

BRAINRESEARCH

437

A PARAMETRIC STUDY OF MOVEMENT DETECTION PROPERTIES OF NEURONS IN THE CAT'S SUPERIOR COLLICULUS

BARRY E. STEIN AND MAKANJUOLA O. ARIGBEDE Department of Anatomy, University of California at Los Angeles, Los Angeles, Calif. 90024 (U.S.A.)

(Accepted April 27th, 1972)

INTRODUCTION The optic tectum is the primary central visual structure in sub-mammalian vertebrates, and thus the fundamental analyzer of retinal information. In phyletic development the neocortex becomes progressively elaborated and the visual cortex plays an increasingly important role in the analysis of visual information. In mammals the investigation of central nervous system transformations of visual information has been primarily directed toward the geniculostriate system, and its involvement in such complex visuo-behavioral functions as pattern discrimination has often been stressed13,16,23. Until very recently the participation of the superior colliculus (the homologue of the optic tectum) in mammalian visual function has received comparatively little emphasis. However, the findings that visual cortex resection does not eliminate orientation and following responses to visual stimuli, while severe deficits in these functions result from collicular lesions 3,23,25,27, have given impetus to electrophysiological and anatomical analysis of this structure. These data, in association with those indicating that orienting, or eye movement responses, can be elicited by stimulation of the superior colliculus and that eye movement associated responses can be recorded from single cells of this structurO2,34, 35, have suggested a functional division between the mesencephalic and geniculostriate systems. Anatomical investigations have revealed that the superior colliculus is a complex, laminated structure receiving topographic projections from retina and visual cortex as well as ascending and descending somatic and acoustic inputs1,~,7,21,24. Electrophysiological studies have established the organization of these projections and have shown that neurons in the upper laminae are primarily responsive to visual input, while neurons responsive to more than one modality of stimulation have been found in the deeper layersS,28,34,37,3s. Furthermore, these investigations have revealed that the nature of information transformation in the superior colliculus is different from that found in the retina and lateral geniculate body (LGB). Neurons of the superior colliculus lack the concentric receptive field organization typical of retinal and LGB neurons, show attenuated responsiveness following repeated stimulus Brain Research, 45 (1972)437--454

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B. E. STEIN A N D M. O. A R I G B E D E

presentations, are influenced by visual cortex and are most sensitive to moving visual stimuli17,19,26,29,31,z4,36,~9. However, the precise characterizations of the relevant stimulus parameters for superior collicular neurons have not been satisfactorily specified. The present experiments were undertaken in an effort to quantitatively determine (a) the relative effectiveness of moving as opposed to stationary stimuli for neurons in the superior colliculus, (b) sensitivity to movement in different directions, (c) the effect of altering stimulus velocity upon response properties, and (d) responsiveness to repeated stimulus presentations in different directions and at various stimulus velocities. METHODS Experiments were performed on 40 adult cats (2.6-3.5 kg). Initially intraperitoneal sodium pentobarbital was employed as the anesthetic agent, but difficulties encountered in locating and studying superior collicular neurons necessitated the use of nonbarbiturized preparations. Animals were, therefore, prepared under deep ether anesthesia. A craniectomy was performed, the dura was incised and reflected and cerebrospinal fluid was drained through the cisterna magna to reduce pulsations of the brain. Following surgery all wounds and pressure points were carefully infiltrated with liberal doses of Zyljectin (a long-acting local anesthetic) to insure adequate analgesia. Subsequent immobilization was provided by intravenous administration of a mixture of gallamine triethiodide and o-tubocurarine e2 and the animals were artificially respirated. Temperature was monitored continuously and maintained at 36-38 °C with a heating pad. The animal was placed in a stereotaxic head holder, the pupils were dilated with 1% atropine and the location of the optic discs (within 2 °C) was projected onto a plastic hemisphere positioned in front of the animal and used to map the receptive fields. Appropriate contact lenses were applied to prevent corneal drying and to correct for retinoscopically determined refractive errors. Extracellular records were obtained with platinum or steel microelectrodes with tips electrolytically etched to 2-5 #m in diameter. The electrodes were lowered through the overlying cerebral hemisphere and entrance of the electrode into the superior colliculus was signalled by a population response to changes in ambient illumination. Records were obtained from the right superior collicutus and, with the exception of tests for binocular driving, all data were obtained by stimulation of the contralateral eye and stored on magnetic tape for later analysis. It is most probable that these records were not obtained from retinal axons due to the dissimilarity of receptive field properties to those of retinal neurons and the high incidence of binocular driving; nor does it seem likely that the records were from fibers of cortical origin due to differences in directional selectivity. Visual stimuli consisted of light and dark rectangular bars, and pulsed electroluminescent lamps with which size, shape and intensity of light could be manipulated 15. Moving stimuli, consisting of bars and spots, were presented in all directions, manually or by means of an hydraulic mechanism, which provided precise, independent control Brain Research, 45 (1972) 437-454

MOVEMENT DETECTION IN SUPERIOR COLLICULUS

439

over orientation and velocity (constant) of movement over a large traverse, and with which stimulus parameters could be accurately repeated on successive stimulus presentations. Acceleration was sufficiently rapid so that constant velocity was attained prior to the entry of the stimulus into the receptive field z0. The mechanism was positioned at approximately 45 cm from the eye and had a background illumination of 2600 Lux. The location of recorded units in the superior colliculus was determined by making small electrolytic lesions at the end of each successful penetration. Upon termination of each experiment, the animal was anesthetized with intravenous sodium pentobarbital and perfused through the heart with saline followed by 1 0 ~ formalin. The brain was embedded in paraffin, sectioned at 15/~m and then stained for cells and fibers with the Kl/iver-Barrera method for subsequent reconstruction of electrode tracks. Shrinkage of the brain and the size of marking lesions may have introduced some error in the exact laminar location of each neuron. RESULTS

A total of 201 single neurons were recorded throughout the superior colliculus and found to be excited by either moving rectangular bars or pulsed stationary light. In addition to these visually responsive cells, neurons responsive solely to somatic or acoustic stimuli, or responsive to more than one stimulus modality (e.g., cells responsive to visual, somatic and acoustic stimuli) were located within or below the stratum griseum intermediale 2s. When a single unit was clearly isolated, the borders of its receptive field were mapped on the transparent hemisphere with the edge of a hand-held rectangular bar. The bar was moved from the periphery (in all directions) inward until responses were repeatedly obtained at points in all areas and a closed area was delimited.

Receptive field properties There appeared to be no preponderance of receptive fields of a given size, but rather a continuous range o f sizes varying from fields as small as 1° × 1° to fields encompassing much of the contralateral visual field but whose boundaries were difficult to determine. These latter fields were difficult to delimit because responses could not always be obtained with repeated stimulus presentations at a given point despite long interstimulus intervals. Regardless of size, receptive fields usually had a long axis and were most closely approximated by a rectangle or an ellipse, although examples of squares and circles were sometimes seen. Receptive fields were always located in the temporal visual field, but occasionally fields were found in which the medial border overlapped the vertical meridian. These fields have also been noted by others 6,31 and are probably due to the crossed projection from the temporal retina3L The receptive field's areal extent and its depth in the superior colliculus were related, and a trend toward increasing field size with increasing depth was apparent. No attempts were made to relate medial-lateral or anterior-posterior position in

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TABLE I VISUAL PROPERTIES OF SUPERIOR COLLICULAR UNITS

Stationary light only

Moving Both stimulus only

Binocular

5 (3.5%) No. tested

53 (36.5%)

70 28 (71.4%) (28.6%) 98

87 (60.0%) 145

Monocular

Ocular dominance Contra

lpsi

21 (95.5%)

1 (4.5 ~o) 22

Pref. small edge

53 (74.6%) 71

the colliculus to field size due to insufficient sampling. However, our findings were consistent with topographical maps of the superior colliculus~, a4. In 75~o of the units tested the movement of an elongated rectangular bar, chosen especially so it would extend beyond the lateral boundaries of the receptive field, evoked markedly fewer discharges than that of a smaller bar confined within the lateral borders of the field. An antagonistic zone adjacent to the 'receptive field' may have provided response inhibitionlT, 31. Repeated stimulation of this antagonistic area alone, however, was never observed to evoke unit responses, and its inhibitory influence was never sufficient to completely suppress unit responsiveness when both the 'receptive field' and the adjacent inhibitory zone were simultaneously stimulated. These zones have been found bordering the long and/or the short axes of the receptive field. A moving stimulus was usually more effective than a stationary stimulus with regard to the number of impulses elicited. However, 63.5 % of the units tested were responsive to a stationary stimulus and 3.5 % could be activated by this stimulus only. In almost all binocularly driven units tested, stimulation of the contralateral eye was more effective than stimulation of the ipsilateral eye (see Table I). Flashing spots, bars and squares of various sizes were employed in testing the properties of units responsive to stationary stimuli. Not all portions of the receptive field were equally sensitive to these stimuli, but no center-surround organization like that present in retina and LGB could be delimited. Most of these units could clearly be classified on the basis of their response to diffuse stationary light as 'on' (5 %), 'off' (32 %), or 'on-off' (63 %), and no relationship between field type and field size, or unit location within the superior colliculus was observed. Directional selectivity

After mapping the receptive field boundaries of a movement-sensitive cell, the effects of movement in different directions were determined by manually moving rectangular bars (which were always smaller than the receptive field diameter) across the field in different directions and at various velocities. Variability in the number of discharges evoked by stimuli moving in the same directions and at approximately Brain Research, 45 (1972) 437-454

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MOVEMENT DETECTION IN SUPERIOR COLLICULUS

the same velocity was often noted, however, and was attributed to the inability to duplicate exactly the successive stimuli presented. Therefore, rectangular bars were mounted on the hydraulic device described under Methods and moved across the receptive fields in symmetrical movements in each of 4 axes (8 directions) separated by 45 °, and at velocities of 1.5°/sec-100°/sec. Thus, stimuli could be precisely controlled and duplicated on successive tests. However, variability in the number of spikes evoked even by identical stimuli was found to be a common property of superior colliculus neurons and will be dealt with in greater detail below. Since any evaluation of the possible effects of movement in different directions necessitated overcoming errors of evaluation due to response variability, 5 identical stimuli were repeated for every direction and velocity of movement tested. After this was accomplished, and when possible, the same unit was tested for responsiveness for up to 50 identical stimulus presentations in a number of different directions of movement in order to further examine response variability and to measure the time course of response attenuation, if present. Thus, the choice of 5 stimulus repetitions represents a compromise between the security of a given set of observations and the number of different observations available. A total of 37 well-isolated units, stimulated with rectangular bars mounted on the hydraulic device, was maintained for the extensive period of time required to quantitatively evaluate the effects of repeated movement in different directions and at various velocities. This sample included a variety of receptive field sizes, shapes and locations within the superior colliculus. In the majority of units studied, movement in aU directions was capable of evoking unit discharges, although with differing degrees of effectiveness. Quantitative analysis revealed that the direction of movement

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Fig. 1. Type II neuron located in stratum griseum intermediale (SGI) of the superior colliculus (SC) and having an elongated receptive field (7° × 12°). A rectangular stimulus was employed in this and subsequent figures and moved at 100°/sec in 4 axes (8 directions) as illustrated by the arrows. Oscillographic tracings show that movement was most effective in two directions with opposing mgvements (180° disparity) being totally ineffective. Records were obtained from stimulation of the contralateral eye in all figures. Brain Research, 45 (1972) 437-454

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B.E. STEIN AND M. O. ARIGBEDE

was a significant factor in determining unit responsiveness in 58 ~ o f the neurons studied (2-way analysis o f variance, P < 0.05). Directional selectivity has been attributed to the asymmetrical distribution o f ' o n ' and 'off' areas o f the receptive field in visual cortexL N o such clear asymmetrical organization was noted in collicular receptive fields when flashing spots o f light were utilized. Reversing the stimulus contrast from a black bar on a white background to a white bar on a black background was also never seen to reverse the directional selectivity observed. Furthermore, directionally selective neurons were located with or without adjacent antagonistic zones. These observations are in agreement with previous reports 17,31 and indicate that directional effects are not necessarily due to these factors. Since most receptive fields were elongated, it might be expected that directional selectivity could be directly related to the longest axis o f the field. However, in the majority o f units studied the most effective direction o f m o v e m e n t was not t h r o u g h the longest axis o f the receptive field. Fig. 1 illustrates the properties o f a directionally selective neuron with an elongated receptive field. In this example, m o v e m e n t across the field was totally ineffective in both directions o f one diagonal axis and quite effective in only one direction o f the other diagonal axis. M o v e m e n t along the vertical axis was ineffective in one direction and only moderately effective in the other while m o v e m e n t across the short axis (horizontal) was very effective from the center to the periphery o f gaze (nasal to temporal). A n u m b e r o f different types o f movement-sensitive neurons in the superior colliculus were noted. Type I. M o v e m e n t in a horizontal axis, away from the center o f gaze, was the one direction of m o v e m e n t most often (40 ~ o f the directionally selective units) found to evoke the greatest n u m b e r o f discharges, while m o v e m e n t in the horizontal axis,

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MOVEMENT DETECTION IN SUPERIOR COLLICULUS

from the periphery to the center of gaze, was the one direction of movement most often (46 % of these units) found to elicit the fewest number of discharges. These were sometimes found to be, respectively, the 'preferred' and 'null' directions of movement 4 in the same unit. Fig. 2 illustrates this effect. Movement along the horizontal axis of this unit's receptive field from center to periphery evoked a vigorous discharge, whereas opposing movements were totally ineffective. These were, respectively, the preferred and null directions of movement. All other directions were found to evoke an intermediate number of impulses. The presence of a preferred and a null direction as opposing movements in the horizontal axis has been reported as typical by other investigators 31. This organization was only observed in 28 % of the neurons tested in the present study. In some cases a single preferred or null direction of.movement was difficult to determine. In 15 units, however, a preferred-null direction relationship could clearly be observed and was most frequently two directions separated by 180° (6 units). Preferred and null directions were also encountered with disparity of 135° (4 units), 90° (3 units) and 45 ° (2 units). Unfortunately, the small number of units in each category renders hazardous any estimate of the relative frequency of these relationships in the superior colliculus. In the majority of these units studied, one direction of movement was often most effective and opposing movements (180° or 135° from it)

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Fig. 3. Type IlI neuron located in stratum griseum profundum (SGP) of SC. The receptive field was extremely large (33 ° x 13 °) and the long axis was vertically oriented. The key in the upper right corner illustrates the directions of stimulus movement. Each point represents the mean number of spikes for 5 stimulus repetitions and the vertical lines at each point represent one standard deviation above and below the mean in this and subsequent figures. This neuron showed axis selectivity without regard to the absolute direction of movemeht within a given axis.

Brain Research, 45 (1972) 437--454

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B . E . STEIN A N D M. O. A R I G B E D E

least effective. Those neurons which had a preferred and a null direction of movement were designated type I. Type II. In some instances it was observed that movement in either of two directions was clearly more effective than any other direction, and movement 180 ° from either of these two directions evoked the fewest number of spikes. These neurons were designated type II. Four such neurons were studied and in all cases the most (and least) effective directions of movement were spatially contiguous. Thus, in type II neurons there was a relatively broad area in which movements in a given direction were either optimal or null. In the unit illustrated in Fig. l movements from the right to the left of the field (within a 90 ° angle) were effective while opposing movements were totally ineffective. In this neuron 3 other directions of movement were also ineffective in evoking discharges. Type IlL Movement-sensitive units were also encountered in which the response properties to moving stimuli differed radically from those of type I and type II cells. These neurons showed preference to movement in a given axis without regard to the absolute direction of movement. Thus, if movement in a vertical axis from top to bottom was ineffective, while movement in a horizontal direction from right to left was optimal, movement in opposing directions (180 ° disparity) would be respectively ineffective and optimal. These relationships were sometimes obscured at velocities evoking minimal numbers of discharges. Fig. 3 illustrates such a unit. At a velocity of 10°/sec, movements in the 3 axes studied were clearly differentiated, while movements in opposing directions of the same axis had almost identical effects. This relationship became progressively less obvious with increasing velocities until it was almost totally obscured at 80°/sec. For these neurons it is more appropriate to speak of orientation or axis preference rather than directional preference. Type III cells were encountered infrequently. Type IV. Movement in different directions was not always observed to have a profound effect upon neuronal responsiveness, despite the fact that movement was clearly a more effective stimulus than a stationary pulsed light. Within the limitations of the directions studied and the method of analysis employed, 4 2 ~ of the neurons studied were not significantly altered in their discharge properties by varying the directions of movement, and these neurons were designated type IV. Any classification scheme is inherently arbitrary and criteria other than those employed here (the direction and/or velocity evoking the greatest number of spikes) might also be valuable in differentiating neurons. For example, there were substantial differences among neurons in the number of spikes evoked in response to the presentation of an optimal stimulus. Superior collicular neurons might, therefore, be classified on this basis as low (see Figs. 1, 2 and 4) or high (see Figs. 3, 6 and 7) frequency responding neurons.

Velocity selectivity Attempts were made to test the effect of altering stimulus velocity upon unit responsiveness by presenting stimuli at the following velocities: 1.5, 2.5, 5, 10, 15,

Brain Research, 45 (1972) 437-454

MOVEMENT DETECTIONIN SUPERIOR COLLICULUS 2

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Fig. 4. Type II neuron located in SG1 of SC. Responsiveness was dependent upon the interaction of direction and velocity of stimulus movement. Increasing the stimulus velocity from 25°/sec to 100°/sec increased the effectivenessof movement in direction 2 and decreased the effectiveness of movement in direction 5. The interspike interval was also decreased when the velocity was increased. Typical oscillographic tracings for the two directions are presented above and a graphical representation is shown below. 25, 50, 80 and 100°/sec. Although all directions and all velocities could not be employed in the study of every unit, it was often possible to employ 5 or more of the velocities listed above in all 8 directions (5 replications of each stimulus presentation). Thirtytwo cells were maintained for a period of time sufficient for the above tests. In 59 % of these neurons a change in stimulus velocity significantly altered the number of impulses evoked (2-way analysis of variance, P < 0.05) and an optimal velocity could usually be determined within this range. On the basis of these parametric tests two velocities most often evoked the most vigorous discharges: 10°/sec and 50°/sec, and this is in agreement with the qualitative observations of others z7,86. With the exception of 1.5°/sec, each of the velocities listed above was optimal for at least one unit. In the neuron illustrated in Fig. 2, increasing the stimulus velocity from 25°/sec to 100°/see increased the effectiveness of movement in the horizontal direction and decreased the interspike interval (see also Fig. 4), but did not alter the preferred-null direction relationship. Fig. 4, however, illustrates the critical nature of varying velocity. At velocities of 10°/sec and 25°/sec, movement in the vertical direction from Brain Research, 45 (1972) 437-454

446

B . E . STEIN AND M. O. ARIGBEDE 25

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Fig. 5. Type I neuron located in SGI of SC. The preferred-null direction relationship was velocity dependent. All 8 directions were tested but only the effect of movement in two directions is reproduced here. When the target was moved at 40°/sec in direction 7 a significantly greater number of spikes (t = 5.57, df = 8, P < 0.001) was evoked than when it was moved in direction 4. These appeared to be, respectively, the preferred and null directions of movement at 40°/sec. At 80°/sec movement in the two directions was equally effective, while at 100°/sec direction 4 became significantly more effective than direction 7 (t = 2.96, df = 8, P < 0.02).

b o t t o m to top was completely ineffective, while m o v e m e n t in the horizontal direction at these same velocities evoked vigorous discharges. Increasing the stimulus velocity increased the effectiveness o f vertical movements while it decreased the effectiveness o f horizontal movements until these differential effects were minimized at 100°/sec.

Interaction between velocity and direction of movement In the majority o f movement-sensitive units tested, the difference between the effectiveness o f different directions o f m o v e m e n t was altered by varying stimulus velocity. Similarly, the differential effects o f various velocities were altered by varying the direction o f movement. In several units the preferred direction (direction X, for example) was significantly m o r e effective than one or m o r e o f the other 7 directions o f m o v e m e n t (for example, direction Y) at a given stimulus velocity (e.g., 25°/sec). Altering stimulus velocity (e.g., increasing to 50°/sec) reversed the differential effectiveness o f these directions o f movement, so that m o v e m e n t in direction Y now elicited significantly more impulses than m o v e m e n t in direction X. Altering stimulus velocity in the unit illustrated in Fig. 5 reversed the preferred-null direction relationship. Direction 7 was clearly m o r e effective than direction 4 at 40°/sec (t -- 5.57, df =~ 8, P < 0.001), and o f the 8 directions tested at this velocity these two appeared to be respectively the preferred and null directions o f movement. W h e n stimulus velocity was increased to 80°/sec the differential effectiveness o f these directions o f m o v e m e n t

Brain Research, 45 (1972) 437-454

MOVEMENT DETECTION IN SUPERIOR COLLICULUS

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STIMULUS PRESENTATION Fig. 6. Type IV neuron located in stratum griseum superficiale (SGS) of SC and stimulated by a target moved in the horizontal axis at 3 stimulus velocities. Each point represents the number of spikes evoked by a single stimulus presentation. N o consistent response trends were noted with repeated stimulus presentations. Interstimulus intervals are from top to bottom: 2 sec, 3 sec, and 4.5 sec.

Brain Research, 45 (1972) 437--454

448

B. E. STEIN A N D M. O. ARIGBEDE

was minimized, and a further velocity increment to 100°/sec reversed the relationship between directions so that direction 4 became significantly more effective than direction 7 (t = 2.96, d f = 8, P < 0.02). While a reversal of the most and least effective directions of movement at any two velocities was uncommon, an interaction between velocity and direction of movement was present in 59 ~o of the units tested.

Response variability In an attempt to evaluate the effectiveness of different directions and velocities of movement in the absence of significant errors due to response variability, 5 replications of each stimulus were usually employed. Since it has been observed that response attenuation with repeated stimulus presentations is a property of superior collicular neurons17,2~,31, 34, we questioned whether the response variability we encountered was due to a specific trend of response attenuation. I f so, perhaps response or earliest responses would have been more appropriate choices in evaluating the effectiveness of different stimuli. The possibility that moving as opposed to stationary stimuli, or that direction and velocity of moving stimuli (critical variables in determining unit responsiveness) might be factors in determining the ease with which response attenuation might be effected, led us to examine this phenomenon quantitatively. Stationary or moving stimuli were presented for up to 50 identical stimulus presentations in 37 units. It was usually not possible to vary systematically all stimulus parameters in a given unit. However, among the cells tested, the interstimulus interval was varied between ! and 4.8 sec, the velocity was varied between 15°/sec and 80°/sec and the direction of movement was varied among the directions described earlier. In some units responses varied about a given range with no obvious trend (see Fig. 6). In the majority of units studied, however, response trends were obvious and were sometimes incremental and sometimes decremental. Fig. 7 illustrates a single unit, tested in all 8 directions of movement, which showed the predominant response trends observed in all units studied. Typical are the decremental trends observed in response to movement in directions 4, 5, 6 and 7, but such decremental trends were often followed by incremental trends (Fig. 7). The response trend effected by movements in directions 2 and 8, which consisted of an initial decrement followed by variable responses at somewhat lower levels, was also observed in some units. Movement in direction 1 effected the greatest response decrement and, despite variability, there appeared to be a consistent response decrement. This suggests that direction of movement may be related to the ease with which response attenuation may be effected. Only 14~o of the neurons studied showed a consistent response decrement like that caused by movements in direction 1. More typical were the response trends observed in the other 7 directions of movement. This proportion of neurons showing consistent response attenuation may be a low estimate, however, as those neurons which were extremely difficult to activate or whose receptive field boundaries were difficult to delimit were excluded from these tests. From these findings it became apparent that the choice of only the first response to define the effectiveness of different stimuli was, in many cases, inappropriate. The choice of 5 stimulus repetitions was a minimal compromise between

Brain Research, 45 (1972) 437-454

449

MOVEMENT DETECTION IN SUPERIOR COLLICULUS

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Fig. 7. Type II neuron located in stratum opticum (SO) of SC and activated by stimulus movement in all 8 directions (as illustrated by the circular key) at 50°/sec. Each point represents the number of spikes evoked by a single stimulus presentation. Decremental response trends followed by incremental response trends can be observed in response to movements in direction 3, 4, 5, 6 and 7. Decremental trends followed by variable responding at somewhat lower levels can be observed in response to movements in directions 2 and 8, and consistent response attenuation followed repeated stimulus presentation in direction 1.

the effects of variability and those of incremental or decremental response trends. The possibility that all neurons might show response attenuation to repeated stimulation if velocity, direction and number of presentations were correctly chosen for a given unit prompted us to look closely at the 5 neurons that did show such a phenomenon. There was no apparent commonality of receptive field size, initial effectiveness of the direction or velocity of movement employed for each neuron, interstimulus interval, or unit location in the superior colliculus that might distinguish these 5 neurons. However, since direction of movement may have been a determining factor (as exemplified by Fig. 7), and since the critical direction might differ among neurons, a larger proportion of neurons showing consistent response attenuation might have been obtained if all 8 directions o f movement were tested in each neuron studied. Brain Research, 45 (1972)437-454

450

B. E. STEIN A N D M. O. ARIGBEDE

DISCUSSION

The present experiments indicate that both direction and velocity of movement are critical variables in determining the responsiveness of superior collicular neurons and that these variables may be interdependent. Therefore, any analysis of the response properties of neurons in the superior colliculus of the cat is complicated by the necessity for manipulation of both variables independently. In the experiments reported here, several movement-sensitive neuronal types were designated and included: type I, neurons with clearly defined preferred and null directions of movement; type II, neurons in which two spatially contiguous, highly effective directions of movement were opposed (180 ° disparity) by two poorly effective directions of movement; type III, neurons showing axis selectivity; and type IV, neurons with no apparent selectivity with regard to direction of movement. In addition, movement-insensitive neurons activated by diffuse light only were observed. The mechanism underlying directional selectivity in the cat superior colliculus has been considered similar to that hypothesized for the rabbit retina 4, and includes unidirectional inhibitory and facilitatory mechanisms 17,31,36. The magnitude of inhibition in the null, and/or facilitation in the preferred direction, would be expected to depend upon the interaction of the rise and decay time of the inhibition (or facilitation) produced by stimulation of successive receptive field positions, and the velocity of movement across the field. This mechanism appears capable of explaining some of the effects of altering stimulus velocity upon directional selectivity that were observed here, but some difficulty is encountered in attempting to explain axis selectivity, or alteration of the preferred direction of movement at certain velocities by this same mechanism. These effects appear to require the action of bidirectional mechanisms. The cat is clearly capable of tracking objects moving in any direction within a wide range of velocities and of making rapid adjustments coincident with alterations in object movement. The selective sensitivity of superior collicular neurons to direction and velocity of movement suggests that this structure may be related to these behavioral functions. This is supported by the paucity of directionally selective neurons in the retina and LGB of the cat 14,33 and the presence of directional selectivity in superior collicular neurons following ablation of visual cortex 8A8. In addition, the effects of collicutar destruction are consistent with the view that the superior colliculus is involved in orienting and following responses 3,23. Within this context we may speculate upon the roles of these various types and it seems probable that they serve separate, yet complementary roles. Type IV neurons appear to signal only the presence of a moving target. Since all 4 movement-sensitive types would also signal such information, type IV neurons might serve only to enhance sensitivity to movement. Type II neurons appear to signal additional information regarding the general direction of movement, while type III neurons might be of greatest importance with regard to oscillating targets within a given axis. Type I neurons would add very specific information regarding the absolute direction of target movement. Thus, the detection of moving stimuli appears to be of prime Brain Research, 45 (1972) 437-454

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451

importance in the superior colliculus and there are neurons possessing the capacity for analysis of various parameters of movement. Velocity of movement is of critical importance in determining unit responsiveness, and all movement-sensitive neuronal types described above responded selectively to this stimulus parameter. Some neurons were most sensitive to high velocities and others to low velocities of movement. The interdependence of velocity and direction of movement was shown by a significant interaction between these variables in 59 % of the units studied. In many cases this interaction was directly related to reduced directional selectivity due to a loss of neuronal sensitivity at one or another of the velocity extremes. This need not create serious confusion with regard to these variables, due to the presence of other neurons, most selective with respect to direction at these velocities. In some instances, however, what appeared to be the most effective direction of movement at one velocity was less effective than some other direction of movement at another velocity. In one neuron a reversal of what appeared to be the preferred-null direction relationship at 40°/sec was observed at 100°/sec. The functional significance of such a reversal is obscure at present. In addition to testing the responsiveness of superior collicular neurons to movement in different directions and at various velocities, responsiveness to repeated identical stimulus presentations was investigated. In some of the neurons studied consistent response attenuation was observed with repeated stimulus presentations, as noted by otherslT,a6, 31,aa. Previous reports, however, have indicated that consistent response attenuation is a common property of superior collicular neurons, and such findings imply that this is the counterpart of the behavioral phenomenon of habituation. In the present experiments only 14 % of the neurons studied showed consistent response attenuation and a corresponding proportion of such neurons has recently been reported in the rabbit 20. More often than consistent attenuation, alternating decremental and incremental response trends were observed, and an analogous phenomenon of response instability has been noted in the rat 11. It is possible that the response trends described in the present study are related to 'arousal' or 'attentiveness' of the animal z6 and future studies should relate E E G states to these trends to see if such a relationship does, in fact, exist. However, these data suggest caution in interpreting attenuating response trends and in inferring underlying mechanisms and behavioral consequences. The present experiments are consistent with the conclusion that the response properties of neurons in the superior colliculus differ markedly from those of neurons in the geniculostriate system26, 31. The clearly defined 'on' and 'off' regions of receptive fields of neurons in retina, LGB and simple cortical cells, as well as their sensitivity to stationary light, distinguish them from most superior collicular neurons which are poorly responsive to stationary light and most sensitive to a moving visual stimulus. In addition, unlike LGB neurons, most superior collicular neurons are clearly responsive to stimulation of either eye. Superior collicular neurons are most similar to the complex and hypercomplex cortical cells, although the relationships between the most and least effective directions of movement present in cortical neuronsg, 10 differ from those found in neurons of the superior colliculus. Brain Research, 45 (1972) 437-454

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These experiments indicate the complexity of the stimulus parameters determining neuronal responsiveness in the superior colliculus. Responsiveness is determined by the interaction of at least two stimulus continua, velocity and direction, requiring the integration of groups of neurons for an accurate assessment of stimulus characteristics, and ultimately the appropriate behavioral response. SUMMARY

Neurons responding to moving and stationary visual stimuli were studied in the superior colliculus of the cat. The majority of neurons were most responsive to stimuli moved in particular directions. Four movement-sensitive neuronal types were characterized: type I, neurons with clearly defined preferred and null directions of movement; type II, neurons in which two spatially contiguous highly effective directions of movement were opposed (180° disparity) by two poorly effective directions of movement; type III, neurons showing axis selectivity; and type IV, neurons with no apparent directional selectivity. Movement-insensitive neurons activated by diffuse light only were also located. Velocity of movement was found to be a potent variable and velocities of 10°/sec and 50°/sec were most often found to be optimal. In some instances altering stimulus velocity changed the optimal direction of movement, and in the majority of neurons studied an interaction between stimulus direction and velocity was observed. Repeated identical stimulus presentations were sometimes observed to induce marked response attenuation. In many of the neurons studied, however, alternating decremental and incremental response trends were noted. ACKNOWLEDGEMENTS

We are indebted to Dr. L. Kruger for his advice, encouragement and helpful criticisms of this manuscript. We would also like to thank J. Achor, S. Sampogna and H. Homier for their technical assistance. Computing assistance was obtained from the Health Science Computing Facility, U.C.L.A., sponsored by N.I.H. Special Resources Grant RR-3. This research was supported by U.S. Public Health Service Grant EY-571, National Eye Institute.

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