Exp Brain Res (1992) 90:40-46

9 Springer-Verlag 1992

Spatiotemporal characteristics of direction-selective neurons in the middle temporal visual area of the macaque monkeys Akichika Mikami Department of Neurophysiology, Primate Research Institute, Kyoto University, Inuyama 484, Japan Received July 29, 1991 / Accepted December 31, 1991

Summary. In an attempt to elucidate the mechanisms of directional selectivity in the neurons of the middle temporal visual area (MT) of macaque monkeys, we presented small numbers of sequentially flashed stimuli with various temporal and spatial intervals within the receptive field (RF) of direction-selective MT neurons. Experiments were performed using awake macaque monkeys trained to fixate on a set of short stationary lines. Stimuli were presented on a CRT screen under computer control. In two-flash experiments, responses to a test flash presented in the center of the RF were examined following a conditioning flash presented in various locations within the RF. Inhibition in the null direction was observed in about 78% of MT neurons, while facilitation was relatively weak in this group of neurons. In most of these neurons, the ranges of temporal and spatial intervals that produced directional selectivity in two-flash experiments were within half the values and double the values, respectively of those in multi-flash experiments. In the remaining 22% of direction-selective M T neurons, several flashed stimuli were necessary to produce directional selectivity. Most of these neurons showed facilitation in the preferred direction. It appears that the inhibitory mechanisms in the null direction are sufficiently strong to be induced by a single conditioning flash whereas the facilitatory mechanisms are weaker and several stimuli are required for production of the direction-selective response. Key words: Area M T - Visual motion - Spatial and temporal interaction - Single neuron activities - Rhesus monkey

visual motion (Newsome et al. 1985; Newsome et al. 1986; Newsome and Pare 1988). Most of the neurons whose activity has been recorded in the M T of macaque monkeys show direction-selective or directionally-biased responses (Dubner and Zeki 1971; Maunsell and Van Essen 1983; Mikami et al. 1986a; Saito et al. 1989). That is, a neuron has a preferred direction to which it responds best, and a null direction to which it responds least. Direction-selective M T neurons of macaque monkeys have an inhibitory mechanism that operates in the null direction and/or a facilitatory mechanism that operates in the preferred direction. Both mechanisms have been studied with sequentially presented, stationary stimuli (Mikami et al. 1986a, b). In a previous study, it was proposed that these mechanisms are the basic mechanisms that produce direction-selective and speed-selective responses of MT neurons. In previous experiments, many stimuli were presented sequentially within the receptive fields of M T neurons. Such multi-flash stimuli, when presented with proper spatial and temporal interflash intervals, produced strong direction-selective responses which were similar to those produced by smoothly moving stimuli. However, the previous multi-flash experiments did not permit us to analyze the way .in which summation effects might influence the spatio-temporal properties of direction-selective mechanisms in MT neurons. This issue is important because psychophysical experiments have shown that summation across sequentially presented stimuli improves motion perception (McKee and Welch 1985). In the present experiments, an examination was made of the effects of summation at the single-neuron level by comparing the responses of MT neurons to two-flash and multi-flash stimuli. A preliminary version of this study has appeared elsewhere (Mikami 1986).

Introduction

Methods

The middle temporal area (MT) is an extrastriate visual area that is selectively involved in the cortical analysis of

Behavioral trainin9 and electrophysiological recordin9

Correspondence to: A. Mikami

Experiments were performed in three awake macaque monkeys (Maeaca mulatta). In the case of the first monkey, experiments were

41

performed by a previously described method (Mikami et al. 1986a). The monkey was trained to fixate on a small spot of light and the monkey's eye position was monitored by a magnetic search coil system. Surgical procedures and visual flash presentation were as described in the above-mentioned report. In the case of the other two monkeys, a modified visual-fixation task was used. Figure 1A shows schematically the sequence of a trial of the visual fixation task. When the monkey pressed a lever, a pair of short vertical, parallel lines (0.225 deg in length, 0.075 deg separation) appeared on the screen. After a variable period of time (0.5-4 s), the orientation of the pair of lines changed to horizontal. The monkey was rewarded when he released the lever within 0.5 s of the change in orientation. Behavioral control, presentation of stimuli and collection of data were controlled by a personal computer (PC-9801F; NEC). The monkey's weight was checked weekly, and supplemental water was given as needed to maintain the animal's health. Each monkey was returned to its home cage after the day's training or experimental session. After the initial period of training, surgery was performed under pentobarbital anesthesia. A metal cylinder (inner diameter, 19 mm) and a head holder were implanted over a cranial aperture made in the skull. Ag-AgC1 electrodes for electro-oculogram (EOG) recording were also implanted (Bond and Ho 1970). During the recording sessions, the monkey's head was secured to the chair frame. A hydraulic microdrive (MO-9; Narishige) was mounted on the recording cylinder, and glass-coated Elgiloy microelectrodes were used for recording of the neuronal activities. The electrode was connected to a preamplifier with FET inputs. The output was led to a DC amplifier (5A15N; TEKTRONIX) and converted into pulses using a window discriminator (4115/40; ANALOG DEVICE). The timing of the occurrence of each converted pulse and the timing of each task event were stored on a floppy disk for later analysis. Converted pulses were also fed to another personal computer (PC-9801F; NEC) for on-line data analysis which displayed the responses to 32 different stimulus conditions. Off-line analyses, such as peri-stimulus-time histograms, raster displays and calculation of average discharge rates during each task period, were performed using data stored on the floppy disks.

Presentation of stimuli In the case of the first monkey, visual stimuli (0.3 x 3.0 deg slit, brightness, 1.5 cd/m a) were projected from an optic bench onto a tangent screen (90 d e g x 6 0 deg). In the case of the other two monkeys, stimuli (0.3 x 2.4 deg slit, brightness, 3.2 cd/m 2) were displayed on a CRT screen (PC-KD551; NEC) under computer control. Stimuli were presented 2 s after the appearance of the fixation pattern. In about 10% of trials, the fixation pattern changed its orientation before the presentation of stimuli, and the trial was terminated without stimuli. Receptive field (RF) boundaries were plotted, and approximate tunings for both direction and speed was determined using moving slits controlled by a joy stick connected to an AD convertor board (DA12-4(98); CONTEC) of the personal computer. With the monkey sitting 28.5 cm from the CRT screen, the screen covered 48 degrees horizontally and 30 degrees vertically. During recording sessions, the fixation pattern was displaced from the center of the screen so that the center of the screen matched the center of the RF of the recorded neuron. When the center of the RF was far from the center of gaze, the stimulus patterns were moved from the center of the screen to a more peripheral location so that stimuli fell within the RF. Then, direction tuning was measured by presentation of a moving slit oriented perpendicular to the direction of movement in 8 different directions in pseudo-random order. Speed tuning was also determined by presentation of 8 different speeds in both the preferred and null directions. Two-flash experiments were conducted next, as illustrated in the schematic diagram in Fig. 1B. A test stimulus was presented in the center of the RF, after presentation of a conditioning stimulus at

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Fig. 1A-C. Schematic representation of the stimulus presentation conditions. A Time course of the visual fixation task. FP: fixation point; Stim: timing of presentation of the stimulus; Lever: timing of pressing of the lever; dx: spatial interval between stimuli; dt: temporal interval between stimuli. Two short parallel lines above the FP trace indicate fixation patterns. B Two-flash paradigm: a single conditioning stimulus (C) prior to a single test stimulus (T). T was presented in the center of the receptive field (RF). C Multi-flash paradigm: more than two-flashes were presented sequentially

various locations on axis of preferred and null direction in the RF. With this stimulus schedule, the temporal interval between stimuli (dt) was kept constant, and the spatial separation between stimuli (dx) was changed from trial to trial. Eight different values of dx were presented in a session in pseudorandom order. In the multi-flash stimulus schedule (Fig. 1C), three or more stimuli were presented sequentially. DC potentials recorded from the Ag-AgC1 electrodes were fed to a DC amplifier. The output of the amplifier was connected to an AD convertor board in the second personal computer. Eye position was monitored on the CRT screen of the PC. The second PC connected with the first PC through an RS-232C interface, also received data on neuronal activity from the first PC which controlled the monkey's behavior. This second PC calculated peri-stimulus-time histograms. Thus, the preferred direction and the preferred speed were determined from on-line histograms. The online histograms helped to select the parameters to test in the next experiment during the recording session.

Analysis of data Data were quantitatively analyzed using off-line computer programs. Peri-stimulus-time histograms were created for each stimulus condition, and the histograms were smoothed by calculation of a weighted average of the spikes in neighboring bins. For the ith bin, the weighted average was obtained using the following formula: s(i) = 0.25 x h ( i - 1) + 0.5 x h(i) + 0.25 x h(i + 1), where h(i) is the number of spikes in the ith bin and s(i) is the weighted average after smoothing. The duration of time bin was varied from 2 to 20 ms as a function of the time interval of each stimulus condition, so that a

42 smaller time bin was used for shorter time intervals and a larger time bin was used for larger time intervals. In the two-flash experiment, for each histogram obtained from a single type of stimulus presentation, the average discharge rate was calculated within a response window that approximated the duration of the response. The computer program first smoothed the histogram using the weighted average described above. The beginning of the response window was set at the point at which the response first exceeded a value equal to (rate[spont] + 2 x sd[spont]; where rate[spont] is the spontaneous discharge rate and sd[spont] is the standard deviation of the spontaneous discharge rate), or at a point 40 ms after onset of the stimulus onset (to allow for the response latency), whichever came later. The end of the window was set at the time at which the response rate, after the maximal response, fell to within two standard deviations of the rate[spont], or 200 ms after the offset of the stimulus, whichever came first. The spontaneous discharge rate was measured for 560 ms prior to presentation of the stimulus. When the maximum neuronal response failed to exceed a value equal to rate[spont]+2x sd[spont], the response of the neuron to a single stimulus was regarded as a negligible response. Under the multi-flash conditions, the response window was calculated in the same way as described above for the two-flash experiment. A response window was established within a range that began 40 ms after stimulus onset and continued up to 200 ms after termination of stimuli to include the entire response.

An anodal current (5 10 #A, 20-40 s) was passed through the recording electrode at the end of selected recording tracks. After the experimental sessions, animals were perfused under deep anesthesia, and locations of recording sites were determined histologically.

Histology

In 59 neurons, the discharge rate in response to a single stimulus flash exceeded r a t e [ s p o n t ] + 2 x sd[spont]. I n these neurons, we tested the i n h i b i t o r y effect of a prior c o n d i t i o n i n g flash on the response to a test flash presented in the center of the RF. I n 46 neurons, the response to the test flash in this experiment was less t h a n 20% of the response to a single test flash alone. A n example is shown in Fig. 2. In A, a c o n d i t i o n i n g flash was presented 36 ms

The procedure to determine the location of MT during the recording sessions were described in detail in the previous report (Mikami et al. 1986a). MT was identified on the posterior bank of the superior temporal sulcus by the characteristic direction selectivity of its neurons, by its receptive-field sizes, which were in the similar range of our previous report. Eccentricities of the center of the receptive field in each neuron were ranged from 3 deg to 26 deg.

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Results Recordings were made from 70 direction-selective n e u r o n s in 5 hemispheres of 3 monkeys. We calculated a n index of directionality (DI) for each n e u r o n according to the c o m m o n l y used formula D I = 1 - ( r e s p o n s e in the null direction/responses in the preferred direction). The value of this index ranged from zero for n e u r o n s with no directionality, t h r o u g h unity for n e u r o n s with strong directionality, to values greater t h a n unity for n e u r o n s that were inhibited in the null direction. We classified M T n e u r o n s as direction-selective when the D I exceeded 0.8, which was indicative of a preferred-to-null response ratio of 5:1.

Examination of inhibitory mechanisms in two-flash experiments

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Fig. 2A-C. Responses of a direction-selective MT neuron tested under two-flash conditions. In A, the temporal interval (dt) is fixed at 36 ms. The spatial intervals (dx) are different from top to bottom. In A-C, the left column illustrates responses when a conditioning flash

was presented in the preferred direction. The right columns show responses when a conditioning flash was presented in the null direction. In B, dt=89 ms. In C, dt=161 ms. See text for details

43 before presentation of a test flash. From top to bottom, the spatial distance between the conditioning and the test stimulus (dx) varies from 0 deg to 1.65 deg in visual angle. In the left column, the conditioning and test pair of flashes were presented in the preferred direction, and in the right column, conditioning and test pair of flashes was presented in the null direction. For sequences in the null direction, inhibition was observed after an initial excitatory response when the spatial interval (dx) was 0.375 or 0.75 deg. In B, the time interval between the two flashes (dt) was 89 ms. Here, two phasic peaks were observed when the stimulus sequence was presented in the preferred direction. The amplitude of the second phasic peak was reduced or the peak was eliminated when the stimulus sequence was presented in the null direction. When the spatial interval between the two flashes was 0.375 or 0.75 deg, the inhibition was sufficiently strong to suppress the spontaneous discharge rate. In C, the time interval was 161 ms, and suppression of the second peak (the response to the test flash) was observed only when the spatial interval was 0.375 deg. Thus, an inhibitory mechanism, operative in the null direction, was revealed for this neuron when the temporal interval and the spatial interval between the two flashes were within the optimal range. When the time interval between the conditioning flash and the test flash is smaller than the decay time of the response to a single flash, the responses to the two flashes overlap one another and it becomes difficult to isolate the response to the test flash. In order to solve this problem and to quantify the effect of the conditioning flash, a response histogram for the conditioning flash presented alone was subtracted from the histogram of the two stimuli presented together. Figure 3 illustrates this procedure. In the first step (Fig. 3A), the response histogram to a single test flash was smoothed and the beginning and end of the response window were established as described in Methods. In Fig. 3A, the left histogram is the original histogram for a single test flash, and the right one is the smoothed histogram obtained from the left one. The start point is 80 ms and the end point is 200 ms after the onset of a flash. In the second step (Fig. 3B), the response to a test flash, after a conditioning flash had been presented in the preferred direction, was calculated. This was done by subtracting the response histogram to a single conditioning flash from the response histogram for the paired conditioning and test stimuli. The response window established in the first step of the process was applied to the resultant histogram, and the discharge rate within the response window was calculated. This discharge rate corresponds to the response of the cell to the test flash when such a flash is paired with a conditioning flash in the preferred direction. In the third step (Fig. 3C), the response to a test flash, when a conditioning flash was presented in the null direction, was calculated by subtracting the histogram of responses to a single conditioning flash from the response histogram for the paired stimuli. Using the same procedure as in the second step, the average discharge rate in response to the test flash, presented after a conditioning flash in the null direction, was calculated.

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Fig. 3A-C. An example of the procedure used to calculate discharge rates in the preferred direction and in the null direction, and the directional index (DI) under two-flash conditions. In A, an averaged peri-stimulus-time histogram of the response to a single test stimulus was smoothed using the weighted filter described in the Methods section. The short vertical line mark under each histogram indicates the onset of the stimulus. The small arrows indicate the onset and the offset of the response, or the onset and the offset of the response window. In B, the histogram of the response to a single conditioning stimulus is subtracted from the histogram of the response under the two-flash conditions for the preferred direction. In C, the response to a single conditioning stimulus is subtracted from the response under the two-flash conditions for the null direction. The well-known formula for calculation of the directional index (DI) is shown at the bottom. C and T are defined in the legend in Fig. 1

In the last step, a direction selectivity index (DI) was calculated from the rates of response to the test flash when it was paired with a preferred- or null-direction conditioning stimuli. The formula is shown in the figure, where rate[null] is the discharge rate when the conditioning flash was presented in the null direction, rate[pref] is the discharge rate when the conditioning flash was presented in the preferred direction, and rate[spont] is the discharge rate prior the stimulus presentation. The maximum spatial separation (dmax) for directional selectivity was the largest value of dx for which the criterion of directional interaction (DI_>0.8) was met. Similarly, the maximum temporal interval (tmax) for directional selectivity was the largest value of dt for which the criterion of directional interaction was met. The minimum spatial separation (dmin) and the minimum temporal interval (tmin) for directional selectivity were determined in an ar/alogous fashion. The values of dmax and tmax for directional selectivity were also determined in the multiple-flash experiment by the procedure described in a previous paper (Mikami et al.

44 1986a). The values of dmin and tmin for direction, selectivity could not be determined in the multiple-flash experiment since the effects of several prior stimuli always influenced the effect of the stimulus presented at the smallest values of dx and/or dt values. For most cells, the values of dmax and tmax were not very different in the two-flash and multiple-flash experiments. An example is shown in Fig. 4. In this case, the neuron responded optimally to a range of low speeds for smoothly moving stimuli (2-32 deg/s; eccentricity, i.e., distance from the center of gaze to the center of the receptive field, 23.1 deg). The maximum spatial separation (dmax) for directional selectivity was 1.65 deg under the two-flash conditions (Fig. 4A). The maximum temporal interval (tmax) for directional selectivity was 161 ms under the two-flash condition. Spatiotemporal characteristics measured under multi-flash conditions are shown in Fig. 4B. The maximum spatial separation was 1.2 deg and the maximum temporal interval was 161 ms under multiflash conditions. The ~alues of dmin and tmin determined during the two-flash experiments were the smallest values tested in this neuron. In 39 neurons, the value of dmax determined under the two-flash was between half the value and double the value of dmax obtained under multi-flash conditions. The results are shown in Fig. 5. In one neuron, the value of dmax under the two-flash conditions was larger than double the dmax value in the multi-flash condition. In three neurons, dmax values under the two-flash conditions were less than half the value under the multi-flash conditions. In two neurons, the value of dmax could not be determined because of unstable responses. In all neurons tested, the value of tmax determined under two-flash conditions was between half the value and double the value of tmax measured under the multi-flash conditions. The value of drain corresponded to the smallest value tested (0.375 deg) in 44 neurons. In two neurons, the value of dmin was larger than the smallest value tested. The value of tmin was the smallest value tested (17.9 ms) in 43 neurons. In three neurons, the value of tmin

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was greater than the smallest value tested. Such an exception is shown in Fig. 6. In this neuron, tmin under the two-flash conditions was larger than the smallest value of dt tested. In Fig. 6A, the DI was smaller than 0.8 when dt equaled 20 ms and 40 ms. Under the multi-flash conditions in Fig. 6B, the responses were direction-selective down to the smallest value of dt tested. In 13 neurons, there was a clear response to the test flash, but a single conditioning flash in the null direction did not produce the criterion level of inhibition. In these neurons, weak inhibition was observed over a certain range of value ofdx and dt, but the D I was less than 0.8. DI reached the criterion level in these neurons when 3-5 flashes were presented in the null direction.

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Fig. 4A, B. Spatiotemporal characteristics of a direction-selective MT neuron under two-flash conditions (A) and multi-flash conditions (B). Asterisks (*) represents values of dx and dt when the direction index (DI) is greater than 0.8. Dashes ( 3 represents values of dx and dt when the DI is smaller than 0.8

Examination of the facilitatory mechanism With eleven of the neurons in our sample, we did not observe a significant response to a single flash. Two neurons in this group showed a significant response after a

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single pair of conditioning and test flashes in the preferred direction. In these neurons, the spatial and temporal characteristics were within half the values and double the values of spatial and temporal intervals determined under the multi-flash conditions. In the other nine neurons, three to eleven sequential conditioning flashes in the preferred direction were necessary to produce sufficient facilitation for the neuron to achieve the criterion level of directional selectivity (DI > 0.8). An example is shown in Fig. 7. In this neuron, clear facilitation was not observed in the two-flash experiment (corresponds to upper histograms in Fig. 7). Facilitation in the preferred direction was observed only when five to seven flashes were presented sequentially. In

Neuronal mechanisms of directional selectivity were first studied in the rabbit retina by Barlow and Levick (1965). They analyzed the effects of a conditioning flash stimulus on a neuron's response to a reference flash stimulus. As a result of systematically varying the location of the conditioning flash within the receptive field, they proposed that the mechanism of directional selectivity in the rabbit retina involves a potent inhibition that operates in the null direction. In our previous reports (Mikami et al. 1986a, 1986b), we presented the first analysis of directional selectivity in the monkey's visual cortex. We found that both inhibitory and facilitatory mechanisms contribute to the directional selectivity of M T neurons under sequentially presented multi-flash conditions. In the present experiments, the inhibitory mechanism operating in the null direction was found to be strong. In 78% of neurons, a single conditioning flash presented in the null direction produced a strong inhibitory effect on the response to the test flash. By contrast, the facilitatory mechanism that operates in the preferred direction is not as strong as the inhibitory mechanism. In most cells, a single conditioning flash presented in the preferred direction did not produce any detectable facilitation of the response to the test flash. Barlow and Levick (1965; in the rabbit retina) and Granz and Felder (1984; in the cat visual cortex) concluded that facilitation was of minor importance, as compared to inhibition. The present results obtained in the visual area M T of the macaque, also suggest that inhibition is stronger and more important than facilitation. Values of dmax and tmax measured under two-flash conditions were somewhat different from the values measured under multi-flash conditions. This difference was probably due to the differences in methods used to calculate the direction indices. In most cases, the values of dmax and tmax under the two-flash conditions were between half the value and double the value, respectively, of the dmax and tmax under the multi-flash conditions. It seems, thus, that the values of dmax and tmax values do not differ very much between multi-flash and two-flash conditions. In other words, the inhibitory effect in the null direction is strong enough that a single conditioning flash suppresses the response to the test flash. In a small number of neurons, dmin and tmin were not the smallest values tested. In these cases, there may exist a delay mechanism that is operative only within a particular spatial or temporal range. Since the number of neurons of this type was small, further experiments are necessary before the results can be taken as conclusive. Under the multi-flash conditions, dmin and tmin were not possible to define, since, under these conditions, the effects of two or

46 three prior flashes could mask the smallest effective spatial or temporal interval. I n a b o u t 16% of neurons, n o response to a single flash was detectable. The m a i n m e c h a n i s m for a directional response in these n e u r o n s was a facititatory effect that operated in the preferred direction. I n most of these neurons, three or more stimuli were necessary to produce a detectable directional response. The n u m b e r of stimuli necessary to produce directional responses differed from n e u r o n to neuron. In the multi-flash condition, when the first stimulus was presented within the excitatory receptive field, the first flash produced the excitatory response in both the preferred a n d the null direction. A n i n h i b i t o r y m e c h a n i s m operating in the null direction became evident as a reduced response to the second or third flash in the sequence. However, when the first flash was presented outside the excitatory receptive field, a response to a null-direction sequence was never observed. This result indicates that there is a strong i n h i b i t o r y zone outside the excitatory receptive fields of individual M T neurons. N a k a y a m a a n d Silverman (1984) reported that three flashes are not sufficient to achieve the m a x i m u m ability to detect coherent motion. M c K e e a n d Welch (1985) reported that a sequence of seven to eight lines is necessary for optimal performance in tests of the perceptual discrimi n a t i o n of speeds. I n the present experiments, seven to eleven sequential stimuli were sufficient to produce optimal encoding of directional m o t i o n via a direction-selective response in the case of almost all n e u r o n s within area MT. Since most direction-selective M T n e u r o n s are also speed-selective, seven to eleven stimuli might be sufficient to elicit optimal encoding of speed in area MT.

Acknowledgements. The initial part of these experiments has been done at the Laboratory of Sensorimotor Research at the National Eye Institute of U.S.A. I am grateful to Dr. R.H. Wurtz and Dr. K. Kubota for their support during the course of these experiments, and to Dr. W.T. Newsome for reading the manuscript and making critical comments. I also thank Mr. A. Hays and Mr. J. Show for assistance in the design of computer programs, Mr. A. Ziminsky for construction of instruments, Ms. G. Snodgrass for training as well as Ms. T. Miwa, Mr. G. Creswell and Ms. L. Cooper for performing the histology, and Ms. J. Steinberg for typing. This work was supported by grants-in-aid from the Ministry of Education, Science and Culture, Japan (no 61134030, 1986; no 62124033, 1987; no 63115017, 1988).

References Barlow HB, Levick WR (1965) The mechanism of directionally selective units in rabbit's retina. J Physiol 178:477 504

Bond HW, Ho P (1970) Solid miniature silve~silver chloride electrodes for chronic implantation. Electroenceph Clin Neurophysiol 28:206-208 Dubner R, Zeki SM (1971) Response properties and receptive fields of ceils in an anatomically defined region of the superior temporal sulcus. Brain Res 35:528-532 Ganz L, Felder R (1984) Mechanism of directional selectivity in simple neurons of the cat's visual cortex analyzed with stationary flash sequences. J Neurophysiol 51:294-324 Komatsu H, Wurtz RH (1989) Modulation of pursuit eye movements by stimulation of cortical areas MT and M ST. J Neurophysio162: 31 47 Komatsu H, Wurtz RH (1988a) Relation of cortical area MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. J Neurophysiol 60:580 603 Komatsu H, Wurtz RH (1988b) Relation of cortical area MT and MST to pursuit eye movements. III. Interaction with full field visual stimulation. J Neurophysiol 60:621 644 Maunsell JHR, Van Essen DC (1983) Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction speed and orientation. J Neurophysiol 49:1127-1147 McKee SP, Welch L (1985) Sequential recruitment in the discrimination of velocity. J Opt Soc Am 2:243 251 Mikami A, Newsome WT, Wurtz RH (1986a) Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT. J Neurophysio155:1308 1327 Mikami A, Newsome WT, Wurtz RH (1986b) Motion selectivity in macaque visual cortex. II. Spatiotemporal range of directional interactions in MT and V1. J Neurophysiol 55:1328-1339 Mikami A (1986) Inhibition and facilitation of the direction selective MT neurons of the macaque monkeys tested by a small number of stimuli. Neurosci Res Suppl 3:186 Nakayama K, Silverman GH (1984) Temporal and spatial characteristics of the upper displacement limit for motion in random dots. Vision Res 24:293-299 Newsome WT, Pare EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201-2211 Newsome WT, Britten KH, Movshon JA (1989) Neuronal correlates of a perceptual decision. Nature 341:52 54 Newsome WT, Mikami A, Wurtz RH (1986) Motion selectivity in macaque visual cortex. III. Psychophysics and physiology of apparent motion. J Neurophysiol 55:1340-1351 Newsome WT, Wurtz RH, Dursteler MR, Mikami A (1985) Deficits in visual motion processing following ibotenic acid lesions of extrastriate area MT of the macaque monkey. J Neurosci 5: 825-840 Saito HK, Tanaka K, Isono H, Yasuda M, Mikami A (1989) Direction selective response of cells in the middle temporal area (MT) of the macaque monkey to the movement of equiluminous opponent color stimuli. Exp Brain Res 75:1-14 Wurtz RH (1969) Response of striate cortex neurons to stimuli during rapid eye movements in the monkey. J Neurophysiol 32: 975 986