Movement sensitivity of retinal ganglion cells in monkey

Vision Rrwarch Vol. ?I, pp. 181 to 190 Pergamon Press Ltd 1981. Printed in Great Br~lain

MOVEMENT

SENSITIVITY OF RETINAL CELLS IN MONKEY

GANGLION

ROBERT P. SCOBEY*

Department of Neurology, University of California at Davis, Davis, CA 95616. U.S.A. (Received 11 April 1980) Abstract-The

responses of on-center monkey retinal ganglion cells to small displacements of a spot light within the receptive field center were studied as a function of spot luminance. One group of cells reached peak rates of firing near 1000 spikes per set with small displacements of spots with moderate and high contrast. These units had non-opponent color characteristics, relatively large receptive fields and phasic responses to a stationary flashing light. Easily distinguished from these cells were a group which had a maximum firing rate to displacement at moderate contrast. Above and below this optimum luminance, the firing rate decreased to zero. These cells had lower peak firing rates (lW200 spikes per set), opponent color characteristics, tonic responses to stationary flashing light and relatively small receptive fields. All retinal ganglion cells isolated were potential candidates for detecting and transmitting movement information. For any individual units, histograms of responses to small displacements were very similar to histograms of responses to the stationary flashing spot. An ensemble code (crossfiber analysis) is proposed to account for transmission of visual form and motion information to the central nervous system via tonic (x-type) and phasic (y-type) units.

INTRODUmON

The visual system is exquisitely sensitive to small image movements. Humans can detect the direction of image displacements which are less than 15 set of arc (Stratton, 1902; Westheimer, 1979). In comparison, acuity for form vision is usually reported to be between 30 and 60sec of arc. This movement sensitivity has been extensively studied but has not yet been satisfactorily explained. Receptive fields of all visual neurons in all animals are larger than the displacement threshold. Nevertheless, neurons must somehow transmit information from small image movement on the retina to the central nervous system. If we consider the size of receptive fields in analogy to the size of the grain on photographic film, then it appears paradoxical that movements are seen which are smaller than the size or the spacing of the smallest grains. The first recording of activity from the optic nerve (Adrian and Matthews, 1928) and recording of single units (Hartline, 1940) revealed that retinal ganglion cells respond to small movements contained within their receptive fields. Subsequent studies on cat (Rodieck and Stone, 1965; Scobey and Horowitz, 1972), demonstrated that displacement sensitivity was greatest in the border zone between the geometric center and the antagonistic surround. Thus it is not a requirement that the receptive fields be smaller than the smallest detectable movements. Relatively little is known about the response of primate retinal ganglion cells to small movements. * Send all correspondence to: Robert P. &obey, Section of Neuroscience, School of Medicine, University of California, Davis, CA 95616, U.S.A.

Most studies have used a stimulus paradigm in which the stimulus is swept back and forth between widely separated sites, while luminance (e.g. Hamasaki et al., 1973) or velocity (e.g. Lee and Willshaw, 1978) is varied as a stimulus parameter. The present experiments on monkey were designed to determine the response properties of primate retinal ganglion cell receptive fields to small movements of a luminous spot. The Rhesus monkey was chosen because their vision resembles that of man (DeValois, 1965). There are a variety of retinal ganglion cells in monkey (DeMonasterio, 1978a, b, c) and it is unknown if all types of units have similar responses to small movements, or whether some types are more suited to the detection of movements than others. Such differentiation is crucial to psychophysical theory regarding form and movement channels at the level of man’s retina. Since different percentages of cell types are present in central and peripheral visual fields (Gouras, 1968; DeMonasterio, 1979a), determining the response characteristics of different types of cells might provide a neurophysiological correlation to the reports that the mechanisms for movement sensitivity are different in the central and peripheral visual fields of man (Tyler and Torres, 1972; Johnson and Scobey, 1980).

METHODS

The methods have been previously reported in detail (Scobey and Horowitz, 1976). Surgery was performed with the animal respired with 2% halothane. 68% nitrous oxide and 30% oxygen. Halothane concentration was 0.5% during recording. 181

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Action potentials from single units were isolated in the retina with micropippettes. The receptive field of units were characterized on a tangent screen (background 6 cd/m’) by the response to small and large spots of red, green, blue and white light. The location of the receptive field was recorded and the tangent screen was then replaced with a CRT stimulator to accurately control luminance, position and movement of a white circular target (34min arc). A sensitivity profile was obtained by adjusting the luminance of the stationary flashing spot at a series of points through the diameter of the receptive field until an auditory threshold was reached. Then, two sites were selected for a displacement study. The stimulus paradigm was composed of two sequential trials with the spot at the same luminance. In the first recording period, the spot was presented to site A, remained stationary for 0.5 set, and was then moved quickly (2 msec) to site B where it remained stationary for another 0.5 sec. After a 2 set delay, the second recording period commenced; the spot was presented to site B alone. The intervals between successive action potentials were recorded on digital magnetic tape with a minicomputer (Spear Microlinc). Up to 16 luminance values at the same sites were repeated in random order until 8 iterations of each luminance were completed. Upon completion of these data sets, the computer display presented the number of action potentials as a function of luminance. Additional luminances might be chosen and the procedure was repeated until a continuous relationship between response to a constant displacement and luminance was found. Peristimulus impulse histograms or frequency histograms of the 8 similar trails were made. A frequency

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Fig. 1. Experimental paradigm. Two sites called A and B were chosen in the receptive field. At a specified luminance, the spot stimulus flashed on at site A and evoked a burst of action potentials illustrated in the histogram (Fig. IA). The response to the onset of the flash was measured as the maximum change in firing rate and is denoted R(A). Fig. IB illustrates the time of flash onset at site A and the time the spot was moved to site B to evoke a displacement response R(D). In the next collection period (Fig. lC), the spot flashed on at site B and evoked the response R(B). Calibration is 100 spikes/set. Data is from a type I cell.

SCOBEY

histogram is the average of the instantaneous frequencies of the individual spike trains. Every bin of a frequency histogram between the occurrence of two action potentials has the same value. Frequency histograms are more regular in appearance than impulse density histograms when a small number of action potentials are evoked. The difference between the ongoing activity and the maximum rate of evoked action potentials was measured from frequency histograms (Fig. 1). The peak response R(A) to a stationary flash at site A was obtained from the first histogram of the set. The peak response R(B) was obtained from the second histogram. The peak response to displacement R(D) was measured from the first histogram after displacement of the spot to site B. In order to prevent selection of spuriously high values, the measure for peak response was an average frequency for a 28 msec period. These peak reesponse were plotted as a function of luminance (Fig. 2). To emphasize displacement responses, the general characteristics of the population of units isolated are described next in this method section. Receptive field characteristics to stationary Jiashing light Quantitative data for this report were based upon 21 on-center retinal ganglion cells from 10 Rhesus Macaque monkeys. All units were recorded for sufcient time (30min minimum) to briefly examine the color properties, obtain a sensitivity profile to a spot of white light along the diameter of the receptive field and collect data for histograms like those in Fig. 1. Qualitative data from the more numerous but briefly recorded units are not considered. The retinal ganglion cells were classified as type I through VI based upon the scheme and larger sample described by Demonasterio (1978). Eight color-opponent units were obvious in this sample (type I and IV). Sensitivity to blue light was found in only one of the color-opponent cells and 2 of the nonopponent units. Thirteen cells lacked obvious color opponent-color responses. On the basis of the “on-dip” in histograms (Demonsterio, 1978), 2 type IV units were identified in the 13 which lacked obvious color-opponent responses. Eleven were probably type III units. The receptive fields were between 5 and 20deg arc from the fovea. Nine hundred eighty pairs of histograms (like Fig. 1) were examined. Histograms were not obtained for units with on-off responses (N = 1) and type VI units were either not recognized or not found. RESULTS

Response to image displacements: general characteristics A displacement of the spot of “white” light from outside the center of the receptive field to within the centre of the receptive field evoked a response that

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All cells tested manifested this behavior, whether or not the stationary flash evoked an offset response at the initial site (Kuffler, 1952) or no offset response (i.e. a silent surround). All cells responded to small displacements of a spot in the receptive field center (definition: intra-receptive field movement). The response to a displacement of a spot from an initial site within the center zone was different than described above and had the following properties. The peak firing rate might, or might no;, be smaller than the firing rate to a stationary flash at the final site. That is, the initial site never had a facilitation on the response evoked by displacement to the final site. Displacement of the spot to a site of lower sensitivity would decrease activity. In some instances, the ongoing activity would be silenced briefly. Displacement of the spot between nearby sites of equal sensitivity was as poor stimulus in monkey as in cat (Rodieck and Stone, 1965). For closely spaced sites, there was no change in the maintained response; for more distant sites, a brief pause was noted in the averaged responses. The response and sensitivity to displacement was primarily determined by the sensitivity difference between the initial site and test site (Scobey and Horowitz, 1972: 1976). Although all of the on-center units of monkey were sensitive to small movements, distinct quantitative differences between units were noted.

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Fig 2. Displacement response as a function of luminance: a phasic unit. The responses at site A and B to the stationary flash are overplotted in 2A. The responses at site A, R(A), are the filled squares and heavy line, and are to the right of R(B), the crosses and light line. The responses reach very high rates with small changes in luminance. The responses to image displacement, R(D), are in 2B, increase with luminance of the spot and saturate at very high rates. The distance from site A to site B was 17min. of arc and the diameter of the field was 63’ of arc. The short duration response can be seen in the histogram (duration 0.5 sec.) which was placed near the corresponding data point in 2A.

was independent of the direction of movement. Such large movements will be referred to as inter-receptive field movement. If the initial site of the spot was near the center region, presumably in the antagonistic surround, the response to displacement to the final site was less than if the spot were flashed at the final site.

Some cells were capable of discharging at very high rates of 1000 action potentials per second. Five units (24%) manifested this behavior, others were limited to a few hundred action potentials/set as maximum rates. This first group of units was distinguished on the basis of displacement response. They responded with only a brief burst of action potentials to displacement of images and to stationary flashing spots of any color. There were no color-opponent cells in this group. The receptive fields were usually medium to large for the sample of cells isolated. These cells appeared to be the same as the phasic cell described by Gouras (1968) and others (Scobey and Horowitz, 1976). A similar class of off-center units were isolated in this study (Hammon and Scobey, unpublished observations). The peak response of a phasic unit (63 min arc receptive field center) to a constant displacement is plotted as a function of stimulus luminance in Fig. 2 for a 2 min arc stimulus. In Fig. 2A. the response to a stationary flash at site A and site B is overplotted. Data for site A are to the right of data for site B by about l/3 log unit, illustrating that site A is less sensitive than site B. Despite the small size of the stimulus relative to the receptive field size, luminance change of only a few tenths of a log unit over threshold was needed to reach 100 spikes per set; a log unit change elicited a response of 1000 spikes/set. The displacement of the luminous spot from site A to site B

ROBERT P. SCOBEY

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evoked a response similar to the stationary flash. The magnitude reached saturation quickly and required only a tenth of log unit more light than a stationary flash at site B alone. Therefore, after a luminous spot was stationary in the field of a phasic unit for a few hundred msec, there was not a major adaptive influence of initial site A on final site B. This permits small movements to evoke a response from a low level of maintained activity, even when the stimulus contrast was high. A 1000

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In 2 instances, the displacement response of phasic units saturated at lower peak frequencies when the displacement was a small fraction of the receptive field diameter. Apparently, small regions of the receptive field had substantial interactions. Perhaps these regions correspond to the subzones described in cat by Hochstein and Shapley (1976). Units

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On the basis of response to movement, a second and third group of cells were evident. Both groups had small to medium size fields and the antagonistic surround was more easily demonstrated. The second group of units were the most common (52%). They were distinguished from the phasic units by a lower maximum response to image displacements and a more slowly adapting response to stationary flashing light at some luminance or wavelength. There were both type III and IV cells. The response to both stationary flashing spots and displacement as a function of luminance was similar to that of Fig. 2, but lower in amplitude. The peak response at response saturation was 200-300 spikes per sec. The response to displacement was similar and determined by the same parameters as the phasic units, i.e. distance moved from the initial site, sensitivity gradient of the receptive field and the spot luminance. A third group of cells also had a tonic discharge to stationary contrast and were distinguished on the basis of a small response to image displacements of both dim and bright targets. The firing rate to a constant displacement initially increased with luminance. but above an optimum luminance, the response to displacement decreased (Fig. 3). The decrease in rate from 200 action potentials per set at the optimum luminance to 10 per set at the highest luminance tested was striking. These cells have small receptive fields and were color-opponent (Type I). All type 1

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Fig. 3. Displacement response as a function of luminance: opponent-color (tonic) unit. The responses to a stationary spot of light flashed at site A and site B are overplotted in 3A. The responses increase with luminance and saturate. The responses to displacement of the image from site A to site B were different than Fig. 2. At higher luminances the displacement responses decrease from a peak of 200 to 10 spikes/set, a value near the maintained activity to background alone. The distance from site A to site B was 19 min arc and the diameter of the receptive field was 40 min arc.

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Fig. 4. Comparison of displacement and flash response. The heavy trace is the response to the spot flashed on at site A, evoking a transient peak and then a tonic response before it is displaced to site B. The peak displacement response is similar in magnitude to the response evoked by the flash of the spot at site B (light trace).

Displacement

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color-opponent cells were rather insensitive to image displacement of a bright spot in the center region of the receptive field. However, the units responded with maximum discharge rates of a few hundred action potentials to a bright stationary flash of light (Fig. 3A) indicating that a displacement of a bright image from outside the center of the receptive field to inside the receptive field would be an effective stimulus (i.e. inter-receptive field movement). The histogram in Fig. 4 illustrates two characteristics of tonic units which are not optimal for detection of small movements. First, as previously mentioned, the peak firing rates were significantly lower in the tonic units than in phasic units. Secondly, the displacement response of tonic units had to be distinguished from an irregularly maintained activity evoked by the spot of light at the initial spot in the receptive field. Thus the displacement response was limited by a ceiling effect caused by a low maximum rate of firing and a floor effect caused by a high variable maintained activity. These response limitations can be seen in Fig. 4 where the displacement of the spot (heavy trace) can be compared to the response at site B alone (over plotted light trace). The peak re-

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sponse of the displacement was equal to the response to a flash at site B alone, as might be expected from a linear system (i.e. for X-type cells, Enroth-Cugell and Robson, 1966). The response to displacement in type 1 cells can be accounted for by the response to stationary flashing light. Consider motion from site A to site B in the receptive field as the spot increases in luminance. As the luminance increases above the threshold for site B (the most sensitive site), the displacement threshold is reached and then the response increases with increase in luminance until the luminance reaches the threshold of site A. With further increase in luminance, the maintained response from the initial site increases (floor effect). After the response at site B saturates (ceiling effect), the displacement response will decrease toward zero (difference between ceiling and floor). Other than these response limitations, the response to spot displacement by opponent color and tonic units was basically similar to phasic units. In summary, the response and sensitivity to displacement was primarily determined by the sensitivity difference between the initial and test site. This determines the magnitude of the effective luminance

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as a function of distange. One half of the receptive field sensitivity profile is illustrated of light was positioned at the outer left hand edge and displaced to sites of higher response to 4 displacements (SB) is shown in the post-stimulus time histograms (5D-G). action potentials in the first 100 msec following the displacement is plotted as a function moved in 5C. An increase in response with an increase in movement is seen throughout of the receptive field. This was a non-opponent-color unit with a phasic response.

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ROBERT P. SCOBEY

change to the receptive field on displacement of a constant luminance spot. Secondary considerations were: (1) the maintained firing of the cell to the stationary spot at the initial site, (2) the maximum firing rate of the unit, and (3) the rate of increase of the response with luminance change. Most of these units were isolated in the parafoveal region, and the displacement response of these cells appear to be determined by the same receptive field parameters that accounted for the displacement sensitivity of more peripheral units (Scobey and Horowitz. 1976). Response as a function of distance The response of all monkey retinal ganglion cells increased with increased displacement if the stimulus was appropriately positioned in the border zone of the central region in the receptive field. An example is illustrated in Fig. 5. A spot of light was initially positioned at the site of least sensitivity in the receptive field. This was chosen to provide a large range for displacement to final sites of higher sensitivity. The luminance of the spot was 2 log units above minimum threshold for this unit and was equal to the threshold of the initial site. The spot was then displaced to more central sites in the receptive field and poststimulus histograms were collected for 16 trials at an iteration rate of 1 trial each 2 sec. The magnitude of displacement for each of the 4 histograms illustrated (Fig. 5DE) is indicated below the left hand section of the receptive field profile to aid comparison (Fig. 5B). The response increases with increasing displacements. The number of action potentials in the first 100 msec after the image displacement (shaded area of histograms) was plotted as a function of displacement in Fig. 5C. The response to displacement was not an increasing function beyond the geometric center. Thus, magnitude of motion is encoded as a change in the firing rate of the cells as well as a spatial shift in the neural activity between cells. Intra-receptive field movement was directionally sensitive. That is, only movement toward the receptive field center from the initial site evoked a discharge.

DISCUSSION

Displacement response The receptive field of retinal ganglion cells in monkey have been studied with stationary flashing light and gratings to determine their spectral characteristics and organization (e.g. Gouras, 1968; Demonasterio, 1978a, b, c). Nevertheless, there is little known about the response of primate retinal ganglion cells to movement of images. Scobey and Horowitz (1976) described the displacement threshold of phasic retinal ganglion cells and found the motion characteristics to be similar to retinal ganglion cells in cat. That study was limited in the types of cells isolated because the tungsten microelectrodes and their position on the

retina provided a recording bias towards larger retinal ganglion cells. In this study micropippettes were used to isolate a greater variety of retinal ganglion cells in the parafoveal region. Other technical improvements provided longer recording period from smaller cells. The responses of retinal ganglion cells to small movements of a spot “white” light were found to be a function of receptive field parameters and stimulus luminance. There were no cells which responded exceptionally well to stationary flashing light and not to motion, or vice versa. Similar peak rates of firing were found with both flashing spots and displacement. Phasic units responded with exceptionally high frequencies of action potentials to both stationary flashes of light and to small displacements. Other units also responded to both stimuli but their peak rates of firing were lower. The displacement response was also limited by the maintained activity evoked by a stationary spot in their receptive field. These quantitative differences between cells are noteworthy, but are not emphasized here. Rather, the similarity of response of all cells when compared to the sensitivity profile of the receptive field is considered more important because it suggests a common mechanism for the detection of motion. All on-type retinal ganglion cells of monkey were sensitive to large movements which take the constant luminance spot from well outside the receptive field to within the receptive field. In addition. all cells responded to image movements which were less than l/l0 of the diameter of their receptive fields. For oncenter cells, movement of a luminous spot from a site of low to a site of higher sensitivity excited the unit. Motion between sites of equal sensitivity, such as in the geometric center was not an effective stimulus (Rodieck and Stone, 1965; Scobey and Horowitz, 1972: 1976). Cells with small receptive fields responded to smaller movements than cells of the same type with larger receptive fields. This may be explained by the higher spatial gradient of sensitivity in small receptive fields. A constant luminance target would have to move less in a small receptive field to produce the same change in effective luminance response. The present findings and previous studies in monkey peripheral retina (Scobey and Horowitz, 1966). indicate that the sensitivity gradient is the primary parameter for determining the response to small displacements for all cells. Secondary parameters are the peak firing rate, the presence of maintained activity, and the rate of change of response with luminance. The response of a retinal ganglion cell to small motion in its receptive field is expected to be related to the spatial summation characteristics of the receptive field. Rodieck (1965) assumed in his model for detection of motion that a linear sum of elementary responses from all parts of the cat receptive field would describe motion. While this may be an approximation for brisk units (Lee and Wilshaw, 1978),

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Displacement response of ganglion cells non linear summation has been found in all types of cat retinal ganglion cells (Shapley and Victor, 1979). The reason for an obvious non linear summation in the center region of some receptive fields called y-type (Enroth-Cugell and Robson. 1966) is still unknown. A most marked departure from linear summation was first described by Kuffler (1952) and is relevant to the displacement response. A spot of light in the antagonistic surround will evoke an offset response if it is extinguished and an onset response if it is flashed in the center region. However, these two responses from different sites in the receptive field never summate. In this study, a displacement from a site in the antagonistic surround to a more central site was never greater than the response to a flash at the central site alone. The displacement response was always less. Thus it is quite clear that models of neural function do not yet quantitatively account for all of the responses evoked by motion. Although quantitative descriptions of neural data are still incomplete one can ask if sufficient neural data is available to qualitatively compare to human psychophysical data. The displacement threshold of retinal ganglion cells in peripheral retina of monkey is similar to the psychophysical data from humans (Scobey and Horowitz, 1976; Johnson and &obey, 1980). The known increase in human displacement threshold with eccentricity is similar to the increase in receptive field size of visual neurons with increasing visual field eccentricity. The smallest receptive fields of retinal ganglion cells in the fovea could be limited by diffraction of light if the center of the receptive field was dominated by the size of a single cone (Polyak, 1941). Suppose that a fovea1 unit would respond if the light flux to the receptive field would change a tenth of a log unit and the sensitivity gradient of the receptive field is a log unit change in a few minutes of arc. Then, a displacement threshold of one quarter of a minute of arc or less seems likely for a single fovea1 retinal ganglion cell. This prediction is in agreement with the movement sensitivity of fovea1 vision in man. Values between 10 set arc and 40 set arc have been reported (Stratton, 1922; Westheimer, 1979; Johnson and Scobey, 1980). This agreement between prediction and measurement is interesting. but not totally convincing. The opponent color (x-type) units are found in greatest percentage near the fovea of monkey, and presumably in the fovea of man. These units were found in this study to decrease their firing rate towards zero with displacements of bright targets. No psychophysical correlates of these data are known. Furthermore, the displacement threshold in fovea1 vision of man is relatively insensitive to changes in line length and luminance. This is not true in peripheral vision (Johnson and Scobey, 1980). These observations indicate that neural and psychophysical data are in weak agreement although a convincing neural explanation for psychophysical data is not yet available.

Channels for form and motion at the primate

retina

The most conspicuous feature of the response following an image displacement was a brief burst of action potentials which may or may not be followed by a maintained increase in discharge rate. The response to displacement, as is illustrated by histograms, could not be distinguished by inspection from the response evoked by a change in luminance of a stationary spot in the same receptive field. Therefore, it seems unlikely that some pattern of action potentials from a single unit distinguishes a response to movement from a response to a stationary flash of light. The human fovea is the most sensitive retinal site for the detection of motion. Suppose that y-type ganglion cells are only channels for motion detection and x-type cells are only channels for form vision. This would require that there be a dense packing of y-type units for fovea1 vision because fovea1 vision is the most sensitive site for motion detection. This has not been found for any animal. It would be an unsatisfactory scheme because both x- and y-type retinal ganglion cells would be required to explain fovea1 vision; this requires more cells than a scheme that permitted x-type units to transmit both form and motion information. Furthermore, this retinal channel hypothesis infers that afferent information regarding vision of motion in x-type units, and information about vision of form in y-type afferents, be discarded at cortical levels. Therefore, it is parsimonious if discrete channels for form and motion did not occur at the retina and information about both form and motion were transmitted by every cell. If this were true, the problem would be to determine how the simultaneous firing of a group of cells permitted the cortex to distinguish stationary and moving targets. Ensemble coding: a hypothesis

Perception of either an increment or decrement of light is seldom confused with motion. A powerful and exact code for these common stimulus variables (form and motion) must be available at the retinal level. The possibilities that distinct channels for form and motion exist at the level of the optic nerve has been rejected for several aforementioned reasons. The search for neural codes should not omit the possibility of “ensemble coding” (McIllwain, 1976), also 1974), known as “cross fiber analysis” (Erickson, because each point of visual space excites a multiple of retinal ganglion cells. With an increment of a spot of light, on-type neurons increase their rate of firing, while off-type units decrease their rate of firing. In a complementary fashion, a decrement of a spot of light evokes an increase in the firing of off-type units, while on-type. units decrease their rate of firing. Obviously, this ensemble code has more contrast information encoded as the difference between the firing rates of on- and off-type afferents than in one cell type alone (Scobey et a/.,

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encoded by the difference in firing rates and the resolution of the eye is accounted for by the size and overlap of receptive fields. The displacement threshold might be accounted for by the notion that cells respond to intrareceptive field motion as previously discussed. However. it is difficult

P. SCOBEY

for directional sensitivity on the basis of a single cell. In the ensemble code, any displacement of a spot will simultaneously excite overlapping on- and off-type units. Retinal receptive fields overlap considerably (Fischer, 1973). A luminous spot which moves into on-type receptive fields will likely also simultaneously move out of off-type receptive fields.

to account

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Fig. 6. Cross-fiber analysis: A simplified conceptual example. (A) Two sites called A and B are shown within the intersection of two receptive field locations (I and II). B. Schematic representation of two sensitivity profiles for on- and off-center receptive fields at both I and II. A movement from site A to site B causes a luminous spot to move to a site of lower sensitivity for fields at I and a site of higher sensitivity for fields at II. C. The predicted response of on- and off-center ceils with receptive fields at I and II when a spot is moved from site A to site B. D. The predicted responses to an increment of a stationarv spot of light. E. A cross fiber analysis scheme to decode increments, decrements and direction of small displacements. Excitatory and inhibitory postsynaptic summation is one of the possibilities to decode this population response.

Displacement

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The simultaneous firing of on- and off-type units with partially shifted receptive fields is suggested here as an ensemble code for movement. How could relatively stereotyped retinal ganglion cells provide information on form and motion without requiring labeled lines from retina? An ensemble code (cross fiber analysis) is illustrated in Fig. 6. Only 2 overlapping receptive field locations are shown (I and II) for a simplified conceptual model. The sensitivity profile of the center regions are shown in 6B. At these 2 receptive field locations there are both on-center and off-center ganglion cells. When a luminous spot is displaced from site A to site B, an on cell with receptive field at location II will fire together with an off cell with a receptive field location at I; the other cells are silent (6C). For an increment of the spot at either site A or B, both overlapping on-center cells fire, but off-center cells are silent (6D). On- and off-type cells at receptive field locations I and II are represented as parallel axons in 6E. Suppose there were excitatory and inhibitory effects on four cortical neurons as shown. Four events, an increment, a decrement, an intrareceptive field displacement to the right, and a displacement to the left, can be resolved independently by simple post synaptic summation. These 4 different stimuli are recognized in the ensemble code even though the responses on individual axons do not define motion and luminance change. This over simplified example cannot account for all physiological data or psychophysical events. For example, another type of decode is necessary to account for cortical cells with directional response to light and dark spots. This example is to emphasize ensemble coding as a possible mechanism to transmit information from primate retina to cortex. If the scheme is correct, it does not argue against presence of detectors for form and motion, nor against the notion that x-and y-type retinal neurons may be more suited for forms and motion data respectively. This will be discussed further below. The ensemble code hypothesis states that the neural message need not be segregated into different axons for transmission of data. The functional properties of linear x-type units were shown to impose restrictions on the response to image movements (Fig. 4). That is, the maintained response to standing contrast in the receptive field and low peak firing rate limits the response range of the unit. The Froperties of the phasic unit (y-type) is expected to have superior response characteristics because: (1) the rapid adaption would lower the maintained response, (2) phasic units have both a higher peak frequency of firing and (3) show greater change in response per luminance change (Fig. 2; Hammon and Scobey, unpublished observations on off-type cells). Perhaps the functional role of the y system is to expand the operational range of response and increase the response to a given effective luminance change to the receptive field. Combining the notion that displacement response

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is generated by an effective luminance change to the receptive field and the notion that the response for a luminance change is greater in y-type units, an idea for the organization of receptive fields on the retina is reached. Consider the possibility that fixed displacement could evoke the same response in either a x- or y-type unit. The y-type unit could have a much larger receptive field (i.e. a lower sensitivity gradient) than an x-type unit. Both x and y cells may have receptive fields at the same point in the primate visual field (Gouras, 1968). At other sites in the visual field the proportion of x- and y-type units might vary. A shift from equal distribution of x- and y-type toward x-type would require more units for detection of motion, but would permit better resolution of stationary contrast (cf. the human fovea). A shift of the population of x and y units toward y-type units permits fewer neurons to provide the same sensitivity to small movements and luminance change, but at the expense of stationary contrast information (cf. the human peripheral visual fields). Acknowledgements-I would like to thank Robert W. Hammon for assistance in obtaining this data, Dwight Howard for the electronics, Janice M. Scobey for computer programs and Chris A. Johnson for many helpful comments on the manuscript. This work was supported by National Eye Institute Research Grant EY-01495. REFERENCES

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