Constraints on the source of short-term motion adaptation in macaque area MT. II. tuning of neural circuit mechanisms

Neurons in area MT, a motion-sensitive area of extrastriate cortex, respond to a step of target velocity with a transient-sustained firing pattern. The transition from a high initial firing rate to a lower sustained rate occurs over a time course of 20-80 ms and is considered a form of short-term adaptation. In the present paper, we compared the tuning of the adaptation to the neuron's tuning to direction and speed. The tuning of adaptation was measured with a condition/test paradigm in which a testing motion of the preferred direction and speed of the neuron under study was preceded by a conditioning motion: the direction and speed of the conditioning motion were varied systematically. The response to the test motion depended strongly on the direction of the conditioning motion. It was suppressed in almost all neurons by conditioning motion in the same direction and could be either suppressed or enhanced by conditioning motion in the opposite direction. Even in neurons that showed suppression for target motion in the nonpreferred direction, the adaptation and response direction tuning were the same. The speed tuning of adaptation was linked much less tightly to the speed tuning of the response of the neuron under study. For just more than 50% of neurons, the preferred speed of adaptation was more than 1 log unit different from the preferred response speed. Many neurons responded best when slow motions were followed by faster motions (acceleration) or vice versa (deceleration), suggesting that MT neurons may encode information about the change of target velocity over time. Finally, adaptation by conditioning motions of different directions, but not different speeds, altered the latency of the response to the test motion. The adaptation of latency recovered with shorter intervals between the conditioning and test motions than did the adaptation of response size, suggesting that latency and amplitude adaptation are mediated by separate mechanisms. Taken together with the companion paper, our data suggest that short-term motion adaptation in MT is a consequence of the neural circuit in MT and is not mediated by either input-specific mechanisms or intrinsic mechanisms related to the spiking of individual neurons. The circuit responsible for adaptation is tuned for both speed and direction and has the same direction tuning as the circuit responsible for the initial response of MT neurons.     

Motion selectivity in macaque visual cortex. II. Spatiotemporal range of directional interactions in MT and V1

We measured the spatial and temporal limits of directional interactions for 105 directionally selective middle temporal (MT) neurons and 26 directionally selective striate (V1) neurons. Directional interactions were measured using sequentially flashed stimuli in which the spatial and temporal intervals between stimuli were systematically varied over a broad range. A direction index was employed to determine the strength of directional interactions for each combination of spatial and temporal intervals tested. The maximum spatial interval for which directional interactions occurred in a particular neuron was positively correlated with receptive-field size and with retinal eccentricity in both MT and V1. The maximum spatial interval was, on average, three times as large in MT as in V1. The maximum temporal interval for which we obtained directional interactions was similar in MT and V1 and did not vary with receptive-field size or eccentricity. The maximum spatial interval for directional interactions as measured with flashed stimuli was positively correlated with the maximum speed of smooth motion that yielded directional responses. MT neurons were directionally selective for higher speeds than were V1 neurons. These observations indicate that the large receptive fields found in MT permit directional interactions over longer distances than do the more limited receptive fields of V1 neurons. A functional advantage is thereby conferred on MT neurons because they detect directional differences for higher speeds than do V1 neurons. Recent psychophysical studies have measured the spatial and temporal limits for the perception of apparent motion in sequentially flashed visual displays. A comparison of the psychophysical results with our physiological data indicates that the spatiotemporal limits for perception are similar to the limits for direction selectivity in MT neurons but differ markedly from those for V1 neurons. These observations suggest a correspondence between neuronal responses in MT and the short-range process of apparent motion.     

Changes in firing pattern of lateral geniculate neurons caused by membrane potential dependent modulation of retinal input through NMDA receptors

An optimal visual stimulus flashed on the receptive field of a retinal ganglion cell typically evokes a strong transient response followed by weaker sustained firing. Thalamocortical (TC) neurons in the dorsal lateral geniculate nucleus, which receive their sensory input from retina, respond similarly except that the gain, in particular of the sustained component, changes with level of arousal. Several lines of evidence suggest that retinal input to TC neurons through NMDA receptors plays a key role in generation of the sustained response, but the mechanisms for the state-dependent variation in this component are unclear. We used a slice preparation to study responses of TC neurons evoked by trains of electrical pulses to the retinal afferents at frequencies in the range of visual responses in vivo . Despite synaptic depression, the pharmacologically isolated NMDA component gave a pronounced build-up of depolarization through temporal summation of the NMDA receptor mediated EPSPs. This depolarization could provide sustained firing, the frequency of which depended on the holding potential. We suggest that the variation of sustained response in vivo is caused mainly by the state-dependent modulation of the membrane potential of TC neurons which shifts the NMDA receptor mediated depolarization closer to or further away from the firing threshold. The pharmacologically isolated AMPA receptor EPSPs were rather ineffective in spike generation. However, together with the depolarization evoked by the NMDA component, the AMPA component contributed significantly to spike generation, and was necessary for the precise timing of the generated spikes.     

Linear integration of convergent visual inputs in an oculomotor reflex pathway

The functional connectivity between identified visual interneurons [sustaining fibers (SF)] and oculomotor neurons was assessed by simultaneous recording and cross-correlation analysis. A small group of SFs exhibit excitatory functional connections to an identified tonic oculomotor neuron. The excitatory interactions are found exclusively between SFs and oculomotor neurons with similar and/or overlapping excitatory receptive fields. A second group of SFs exhibit inhibitory connections to motor neurons. The excitatory receptive fields of these SFs correspond to the inhibitory receptive fields of the motor neurons. The collective action of the SFs is sufficient to produce all of the steady-state visual behavior of the motor neurons including the increment in firing rate elicited by illumination, unique features of the motor neuron receptive field, and differential sensitivity to blue light and polarized light. Pairs of SFs that converge on the same motor neuron sum their effects linearly. Thus the joint interaction of two SFs on a motor neuron is equal to the sum of the two postsynaptic effects taken separately. Coactivation of excitatory and inhibitory SF inputs to a motor neuron results in a partial cancellation of their postsynaptic effects on the motor neuron's firing rate. The antagonistic interactions protect the system from perturbations by stray light, visual adaptation, and variations in the central excited state. The ensemble information code, at the SF level of the optomotor pathway, is a set of differentially weighted mean firing rates. The weightings reflect differences in the strengths of the several SF-to- motor neuron interactions. One consequence of these differences is a selective weighting of the effects of illumination (in different regions of visual space) on the compensatory eye reflex.     

Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes

1. We have identified a visually driven output from the flocculus of the monkey by studying the simple-spike responses of Purkinje cells (P-cells) during the initiation of smooth-pursuit eye movements. We report on two groups of P-cells that appear to be the horizontal and vertical gaze-velocity P-cells (GVP-cells) studied previously during periodic target and head motion. 2. During pursuit of periodic target motion, one group of P-cells prefers downward motion (down GVP-cells), and the other prefers motion toward the side of recording (ipsi GVP-cells). The two groups have mean directional preferences that are nearly orthogonal, but their responses during pursuit of sinusoidal target motion and sinusoidal vestibular stimulation are in other respects quantitatively similar. 3. During the initiation of pursuit to step-ramp target motion, GVP-cells show a large transient change in simple-spike firing rate followed by a sustained change in firing that persists during steady-state pursuit. 4. The transient response is directionally selective, so that GVP-cells show a pulse of simple spikes for pursuit in the ON-direction and a dip in simple-spike firing for pursuit in the OFF-direction. The amplitude of the transient response is too large to be explained by the sensitivity of GVP-cells to eye velocity measured during pursuit of sinusoidal target motion. 5. To test whether the transient change in simple-spike firing was related to a visual input or to an eye-acceleration input to the flocculus, we recorded the firing of ipsi GVP-cells during a rapid eye acceleration caused by a transient vestibular stimulus in darkness. Most GVP-cells showed little or no transient response under these conditions, even though eye acceleration was greater than during the initiation of pursuit. We conclude that the transient response at the initiation of pursuit is probably caused by visual mossy-fiber inputs to the flocculus. 6. The sustained change in simple-spike firing is also directionally selective, with large increases in simple-spike firing for pursuit in the ON-direction and smaller decreases for pursuit in the OFF-direction. For pursuit in the ON-direction, the amplitude of the sustained response is well predicted by the sensitivity of GVP-cells to eye velocity measured during pursuit of sinusoidal target motion. 7. To determine whether the sustained response was driven by visual inputs, we recorded simple-spike firing when image motion was prevented by electronically stabilizing the target image on the fovea during steady-state pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)     

Characteristics of the pupillary light reflex in the macaque monkey: discharge patterns of pretectal neurons

Anatomical and physiological data have implicated the pretectal olivary nucleus (PON) as the midbrain relay for the pupillary light reflex in a variety of species. To determine the nature of the discharge of pretectal light reflex relay neurons, we recorded their activity in monkeys that were fixating a stationary spot while a full-field random-dot stimulus was flashed on for 1 s. Based on their discharge patterns, neurons in or near the PON came in two varieties. The most prevalent neuron discharged a burst of spikes 56 ms (on average) after the light came on followed by a sustained rate for the duration of the stimulus (burst-sustained neurons). When the light went off, nearly all neurons (33/34) ceased firing, and then all the neurons with a resting response in the dark (n = 15) resumed firing. Both the firing rate within the burst and the sustained discharge rate increased with log light intensity and the latency of the burst decreased. The burst and cessation of firing were better aligned with the stimulus occurrence than with the onset of pupillary constriction or dilation. Taken together, these data suggest that burst-sustained neurons respond to the visual stimulus eliciting the pupillary change rather than dictating the metrics of the subsequent pupillary response. Electrical stimulation at the site of four of five burst-sustained neurons elicited pupillary constriction at low stimulus strengths after a latency of approximately 100 ms. When the electrode was moved 250 microm away from the burst-sustained neuron, the elicited response disappeared. Reconstructions of the locations of burst-sustained luminance neurons place them in the PON or its immediate vicinity. We suggest that PON burst-sustained neurons constitute the pretectal relay for the pupillary light reflex. A minority of our recorded pretectal neurons discharged a burst of spikes at both light onset and light offset. For most of these transient neurons, neither the burst rate nor the interburst rate was significantly related to light intensity. We conclude that these neurons are not involved in the light reflex but subserve some other pretectal function.     

Aging affects contrast response functions and adaptation of middle temporal visual area neurons in rhesus monkeys

In the present study we studied the effects of aging on the coding of contrast in area V1 (primary visual cortex) and MT (middle temporal visual area) of the macaque monkey using single-neuron in vivo electrophysiology. Our results show that both MT and V1 neurons in old monkeys are less sensitive to contrast than those in young monkeys. Generally, contrast sensitivity is affected by aging more severely in MT cells than in V1 cells. Specifically, MT cells were affected more severely than motion direction selective V1 cells. Particularly, we found that MT neurons in old monkeys exhibited enhanced maximum visual responses, higher levels of spontaneous activity and decreased signal-to-noise ratios. In addition, we also found age-related changes in neuronal adaptation to visual motion in MT. Compared with young animals, the contrast gain of MT neurons in old monkeys is less affected, but the response gain by adaptation of MT neurons is more affected. Our results suggest that there may be an anomalous visual processing in both the magnocellular and parvocellular pathways. The neural changes described here are consistent with an age-related degeneration of intracortical inhibition and could underlie some deficits in visual function during normal aging.     

Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT

Mechanisms of direction selectivity and speed selectivity were studied in single neurons of the middle temporal visual area (MT) of behaving macaque monkeys. Visual stimuli were presented in both smooth and stroboscopic motion within a neuron's receptive field as the monkey fixated a stationary point of light. Direction selectivity, speed selectivity, and the spontaneous discharge characteristics of MT neurons in behaving monkeys were similar to those reported in previous studies in anesthetized monkeys. Stroboscopic motion stimuli were sequences of flashes characterized by the spatial and temporal intervals between each flash. The spatial and temporal intervals were systematically varied so that suppressive and facilitatory interactions could be studied in both the preferred and null directions. Suppression and facilitation were measured by subtracting the peak discharge rate elicited by a single flash from the peak discharge rate elicited by a stroboscopic train of flashes. The dominant mechanism of direction selectivity in MT was a pronounced suppression of discharge for motion in the null direction which we interpreted as inhibition. The inhibition was sufficiently potent to abolish the responses to single flashed stimuli when they were embedded in a series of flashes in the null direction, and it frequently reduced the neuronal discharge to a level below the spontaneous firing rate. Facilitation in the preferred direction was a prominent feature of the responses of some, but not all, MT neurons. The peak discharge rate for stroboscopic motion in the preferred direction was more than twice the peak rate to a single flash for approximately 50% of the neurons in our sample. The direction selectivity of most MT neurons showed the effects of both inhibitory and facilitatory mechanisms, and it was not possible to segregate MT neurons into distinct groups on the basis of these measures. Suppressive mechanisms contributed to speed tuning as well as direction tuning. The low-speed cutoff for motion in the preferred direction resulted from suppression in 82% of the neurons tested. The high-speed cutoff resulted from suppression in 32% of the neurons tested. The latter mechanism appeared to be distinct from the inhibitory mechanism which acted in the null direction in that large spatial intervals were required for its activation.     

Corticogeniculate neurons, corticotectal neurons, and suspected interneurons in visual cortex of awake rabbits: receptive-field properties, axonal properties, and effects of EEG arousal

The intrinsic stability of the rabbit eye was exploited to enable receptive-field analysis of antidromically identified corticotectal (CT) neurons (n = 101) and corticogeniculate (CG) neurons (n = 124) in visual area I of awake rabbits. Eye position was monitored to within 1/5 degrees. We also studied the receptive-field properties of neurons synaptically activated via electrical stimulation of the dorsal lateral geniculate nucleus (LGNd). Whereas most CT neurons had either complex (59%) or motion/uniform (15%) receptive fields, we also found CT neurons with simple (9%) and concentric (4%) receptive fields. Most complex CT cells were broadly tuned to both stimulus orientation and velocity, but only 41% of these cells were directionally selective. We could elicit no visual responses from 6% of CT cells, and these cells had significantly lower conduction velocities than visually responsive CT cells. The median spontaneous firing rates for all classes of CT neurons were 4-8 spikes/s. CG neurons had primarily simple (60%) and concentric (9%) receptive fields, and none of these cells had complex receptive fields. CG simple cells were more narrowly tuned to both stimulus orientation and velocity than were complex CT cells, and most (85%) were directionally selective. Axonal conduction velocities of CG neurons (mean = 1.2 m/s) were much lower than those of CT neurons (mean = 6.4 m/s), and CG neurons that were visually unresponsive (23%) had lower axonal conduction velocities than did visually responsive CG neurons. Some visually unresponsive CG neurons (14%) responded with saccadic eye movements. The median spontaneous firing rates for all classes of CG neurons were less than 1 spike/s. All neurons synaptically activated via LGNd stimulation at latencies of less than 2.0 ms had receptive fields that were not orientation selective (89% motion/uniform, 11% concentric), whereas most cells with orientation-selective receptive fields had considerably longer synaptic latencies. Most short-latency motion/uniform neurons responded to electrical stimulation of the LGNd (and visual area II) with a high-frequency burst (500-900 Hz) of three or more spikes. Action potentials of these neurons were of short duration, thresholds of synaptic activation were low, and spontaneous firing rates were the highest seen in rabbit visual cortex. These properties are similar to those reported for interneurons in several regions in mammalian central nervous system. Nonvisual sensory stimuli that resulted in electroencephalographic arousal (hippocampal theta activity) had a profound effect on the visual responses of many visual cortical neurons.(ABSTRACT TRUNCATED AT 400 WORDS)     

Local precision of visuotopic organization in the middle temporal area (MT) of the macaque

Summary The representation of the visual field in the middle temporal area (MT) was examined by recording from single neurons in anesthetized, immobilized macaques. Measurements of receptive field size, variability of receptive field position (scatter) and magnification factor were obtained within the representation of the central 25°. Over at least short distances (less than 3 mm), the visual field representation in MT is surprisingly orderly. Receptive field size increases as a linear function of eccentricity and is about ten times larger than in V1 at all eccentricities. Scatter in receptive field position at any point in the visual field representation is equal to about one-third of the receptive field size at that location, the same relationship that has been found in V1. Magnification factor in MT is only about onefifth that reported in V1 within the central 5° but appears to decline somewhat less steeply than in V1 with increasing eccentricity. Because the smaller magnification factor in MT relative to V1 is complemented by larger receptive field size and scatter, the point-image size (the diameter of the region of cortex activated by a single point in the visual field) is roughly comparable in the two areas. On the basis of these results, as well as on our previous finding that 180° of axis of stimulus motion in MT are represented in about the same amount of tissue as 180° of stimulus orientation in V1, we suggest that a stimulus at one point in the visual field activates at least as many functional modules in MT as in V1.     

Postnatal development of spike generation in rat medial vestibular nucleus neurons

Image stability during self motion depends on the combined actions of the vestibuloocular and optokinetic reflexes (VOR and OKR, respectively). Neurons in the medial vestibular nucleus (MVN) participate in the VOR and OKR by firing in response to both head and image motion. Their intrinsic spike-generating properties enable MVN neurons to modulate firing rates linearly over a broad range of input amplitudes and frequencies such as those that occur during natural head and image motion. This study examines the postnatal development of the intrinsic spike-generating properties of rat MVN neurons with respect to maturation of peripheral vestibular and visual function. Spike generation was studied in a brain stem slice preparation by recording firing responses to current injected intracellularly through whole cell patch electrodes. MVN neurons fired spontaneously and modulated their firing rate in response to injected current at all postnatal ages. However, the input-output properties of the spike generator changed dramatically during the first two postnatal weeks. Neurons younger than postnatal day 10 could not fire faster than 80 spikes/s, modulated their firing rates over a limited range of input amplitudes, and tended to exhibit a nonlinear relationship between input current and mean evoked firing rate. In response to sustained depolarization, firing rates declined significantly in young neurons. Response gains tended to be highest in the first few postnatal days but varied widely across neurons and were not correlated with age. By about the beginning of the third postnatal week, MVN neurons could fire faster than 100 spikes/s in response to a broad range of input amplitudes, exhibited predominantly linear current-firing rate relationships, and adapted little in response to sustained depolarization. Concomitant decreases in action potential width and the time course of the afterhyperpolarization suggest that changes in potassium currents contribute to the maturation of the MVN neuronal spike generator. The results demonstrate that developmental changes in intrinsic membrane properties enable MVN neurons to fire linearly in response to a broad range of stimuli in time for the onset of visual function at the beginning of the third postnatal week.     

Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys

When viewing a stationary object, we unconsciously make small, involuntary eye movements or 'microsaccades'. If displacements of the retinal image are prevented, the image quickly fades from perception. To understand how microsaccades sustain perception, we studied their relationship to the firing of cells in primary visual cortex (V1). We tracked eye movements and recorded from V1 cells as macaque monkeys fixated. When an optimally oriented line was centered over a cell's receptive field, activity increased after microsaccades. Moreover, microsaccades were better correlated with bursts of spikes than with either single spikes or instantaneous firing rate. These findings may help explain maintenance of perception during normal visual fixation.     

Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties

1. In fully awake rabbits the stability of the two eyes was monitored and was sufficient to enable receptive-field analysis of antidromically identified efferent neurons and suspected interneurons in the binocular segment of visual area 1. Efferent neurons analyzed included callosal efferent neurons (CC neurons, n = 52), neurons projecting to visual area 2 (CV2 neurons, n = 35), corticotectal neurons (CT neurons, n = 43), and corticogeniculate neurons (CG neurons, n = 51). Six additional neurons projected a branching axon to both the corpus callosum and visual area 2. 2. Most CC and CV2 neurons were found in layer 2-3 and had receptive fields of the simple type. Only two corticocortical neurons with complex receptive fields were found. Orientation tuning ranges of CC and CV2 simple cells were similar and end stopping was prevalent in both CC (62%) and CV2 (45%) neurons. Axonal conduction velocities of CC and CV2 neurons were low (mean = 3.5 and 1.4 m/s, respectively) and visually nonresponsive CC neurons (19%) had conduction velocities that were significantly lower than visually responsive neurons. Spontaneous firing rates of corticocortical neurons were low (mean less than 1 spike/s) and these neurons responded to a lower range of stimulus velocities than did corticofugal neurons. 3. Most CG neurons had simple receptive fields and none had a complex field. Orientation tuning ranges of these neurons were comparable to those of CC and CV2 neurons, but a significantly smaller proportion (12%) were end stopped. Both spontaneous firing rates (mean = less than 1 spike/s) and axonal conduction velocities (mean = 2.4 m/s) of CG neurons were low and, as was found for CC neurons, visually nonresponsive CG neurons (25%) had significantly lower conduction velocities than did visually responsive neurons. 4. CT neurons had receptive fields that were predominantly complex (37%), motion/uniform (28%), or simple (26%). Conduction velocities (mean = 10.9 m/s) and spontaneous firing rates (mean = 7 spikes/s) of CT neurons of all receptive-field types were much higher than those of CC, CV2, and CG neurons. 5. An additional class of neurons was studied that responded synaptically at a short latency to electrical stimulation of the dorsal lateral geniculate nucleus (LGNd) with a burst of three or more spikes at frequencies of 600-900 Hz. These neurons showed a high degree of synaptic convergence, also responding synaptically with a high-frequency burst of spikes to stimulation of both visual area 2 and the corpus callosum.(ABSTRACT TRUNCATED AT 400 WORDS)     

Spatiotopic selectivity of BOLD responses to visual motion in human area MT

Many neurons in the monkey visual extrastriate cortex have receptive fields that are affected by gaze direction. In humans, psychophysical studies suggest that motion signals may be encoded in a spatiotopic fashion. Here we use functional magnetic resonance imaging to study spatial selectivity in the human middle temporal cortex (area MT or V5), an area that is clearly implicated in motion perception. The results show that the response of MT is modulated by gaze direction, generating a spatial selectivity based on screen rather than retinal coordinates. This area could be the neurophysiological substrate of the spatiotopic representation of motion signals.     

Spatial and temporal determinants of directionally selective velocity preference in cat striate cortex neurons

1. Direction-selective properties of neurons in cat striate cortex (area 17) were studied with flashed and continuously moving bar stimuli. Receptive fields were characterized by measurement of static and dynamic parameters, which were correlated with the velocity preference exhibited by the same cells. 2. Each neuron was found to be direction selective to a limited range of velocities. This behavior was characterized by measuring the optimal velocity (Vopt) to elicit responses in the preferred and null directions that were maximally distinct. 3. A bar stimulus flashed sequentially at two nearby locations in the receptive field also produced direction-selective behavior, which was characterized by an optimal displacement (Dopt) to drive maximally distinct responses in the preferred versus null directions. 4. The static spatial receptive field properties were quantified by measurement of the receptive field size (2 sigma) and the spatial subunit wavelength (lambda). The latter quantity was measured as twice the separation between adjacent ON and OFF regions in simple cells and as twice the optimal separation for lateral inhibition between two simultaneously flashed bars in complex cells. 5. Direction-selective velocity preference for continuously moving stimuli, Vopt, was found to be highly correlated with lambda and with the Dopt for 2-flash motion; Vopt was also correlated to a lesser degree with 2 sigma. These results suggest a fundamental linkage between spatial frequency preference, velocity preference, and spatial tuning to 2-flash motion. 6. The range of measured direction-selective velocity preference values (Vopt) spanned about a 100-fold range, whereas the corresponding values of Dopt or lambda spanned substantially smaller ranges. This discrepancy suggested that the dynamic range of velocity preference among cortical neurons might be determined jointly by the measured spatial properties and by a temporal property that covaries with the measured spatial properties. 7. Temporal properties of striate cortical neurons were assessed from responses to flashed stimuli having a prolonged duration ("step responses"). Neurons typically responded in the following manner: after some latency (L), a transient rise in spike frequency occurred, which then adapted to some sustained level. The adaptation dynamics (extent of sustained vs. transient behavior) were quantified by the first-order time constant (AT) of the adaptation decay, and by the ratio of initial transient rise to final sustained level [adaptation ratio (AR)].(ABSTRACT TRUNCATED AT 400 WORDS)     

Area MT neurons respond to visual motion distant from their receptive fields

Neurons in cortical area MT have localized receptive fields (RF) representing the contralateral hemifield and play an important role in processing visual motion. We recorded the activity of these neurons during a behavioral task in which two monkeys were required to discriminate and remember visual motion presented in the ipsilateral hemifield. During the task, the monkeys viewed two stimuli, sample and test, separated by a brief delay and reported whether they contained motion in the same or in opposite directions. Fifty to 70% of MT neurons were activated by the motion stimuli presented in the ipsilateral hemifield at locations far removed from their classical receptive fields. These responses were in the form of excitation or suppression and were delayed relative to conventional MT responses. Both excitatory and suppressive responses were direction selective, but the nature and the time course of their directionality differed from the conventional excitatory responses recorded with stimuli in the RF. Direction selectivity of the excitatory remote response was transient and early, whereas the suppressive response developed later and persisted after stimulus offset. The presence or absence of these unusual responses on error trials, as well as their magnitude, was affected by the behavioral significance of stimuli used in the task. We hypothesize that these responses represent top-down signals from brain region(s) accessing information about stimuli in the entire visual field and about the behavioral state of the animal. The recruitment of neurons in the opposite hemisphere during processing of behaviorally relevant visual signals reveals a mechanism by which sensory processing can be affected by cognitive task demands.     

Correlated firing in rabbit retinal ganglion cells

A ganglion cell's receptive field is defined as that region on the retinal surface in which a light stimulus will produce a response. While neighboring ganglion cells may respond to the same stimulus in a region where their receptive fields overlap, it generally has been assumed that each cell makes an independent decision about whether to fire. Recent recordings from cat and salamander retina using multiple electrodes have challenged this view of independent firing by showing that neighboring ganglion cells have an increased tendency to fire together within +/-5 ms. However, there is still uncertainty about which types of ganglion cells fire together, the mechanisms that produce coordinated spikes, and the overall function of coordinated firing. To address these issues, the responses of up to 80 rabbit retinal ganglion cells were recorded simultaneously using a multielectrode array. Of the 11 classes of rabbit ganglion cells previously identified, coordinated firing was observed in five. Plots of the spike train cross-correlation function suggested that coordinated firing occurred through two mechanisms. In the first mechanism, a spike in an interneuron diverged to produce simultaneous spikes in two ganglion cells. This mechanism predominated in four of the five classes including the ON brisk transient cells. In the second mechanism, ganglion cells appeared to activate each other reciprocally. This was the predominant pattern of correlated firing in OFF brisk transient cells. By comparing the receptive field profiles of ON and OFF brisk transient cells, a peripheral extension of the OFF brisk transient cell receptive field was identified that might be produced by lateral spike spread. Thus an individual OFF brisk transient cell can respond both to a light stimulus directed at the center of its receptive field and to stimuli that activate neighboring OFF brisk transient cells through their receptive field centers.     

Motion selectivity in macaque visual cortex. III. Psychophysics and physiology of apparent motion

We have conducted physiological and psychophysical experiments to identify possible neural substrates of the perception of apparent motion. We used identical sequences of flashed stimuli in both sets of experiments to better compare the responses of cortical neurons and psychophysical observers. Physiological data were obtained from two cortical visual areas, striate cortex (V1) and the middle temporal area (MT). In the previous paper we presented evidence that neuronal thresholds for direction selectivity in extrastriate area MT were similar to psychophysical thresholds for motion perception at the largest effective interflash interval, and thus speed, for a given eccentricity. We now examine physiological and psychophysical thresholds for a broad range of speeds to determine whether such a correspondence exists for speeds below the upper threshold considered in the previous paper. Stimuli were presented in stroboscopic motion of constant apparent speed while the spatial and temporal interflash intervals were systematically varied. For each neuron we measured the largest spatial interval that elicited directionally selective responses at each of several apparent speeds. We calculated the composite performance of neurons in both MT and V1 by averaging the spatial interval necessary for direction selectivity at each apparent speed. We employed the same apparent-motion stimuli for psychophysical experiments with human subjects in which we measured the spatial interval necessary for the perception of motion over a similar range of apparent speeds. We obtained a composite profile of psychophysical performance by averaging thresholds across subjects at each apparent speed. For high apparent speeds, physiological data from MT, but not V1, corresponded closely to the psychophysical data as suggested in the preceding paper. For low apparent speeds, however, physiological data from MT and V1 were similar to each other and to the psychophysical data. It would appear, therefore, that neurons in either V1 or MT could mediate the perceptual effect at low speeds, whereas MT is a stronger candidate for this role at high speeds. We suggest that the neuronal substrate for apparent motion may be distributed over multiple cortical areas, depending upon the speed and spatial interval of the stimulus.     

Temporal dynamics of shape analysis in macaque visual area V2

The firing rate of visual cortical neurons typically changes substantially during a sustained visual stimulus. To assess whether, and to what extent, the information about shape conveyed by neurons in visual area V2 changes over the course of the response, we recorded the responses of V2 neurons in awake, fixating monkeys while presenting a diverse set of static shape stimuli within the classical receptive field. We analyzed the time course of various measures of responsiveness and stimulus-related response modulation at the level of individual cells and of the population. For a majority of V2 cells, the response modulation was maximal during the initial transient response (40-80 ms after stimulus onset). During the same period, the population response was relatively correlated, in that V2 cells tended to respond similarly to specific subsets of stimuli. Over the ensuing 80-100 ms, the signal-to-noise ratio of individual cells generally declined, but to a lesser degree than the evoked-response rate during the corresponding time bins, and the response profiles became decorrelated for many individual cells. Concomitantly, the population response became substantially decorrelated. Our results indicate that the information about stimulus shape evolves dynamically and relatively rapidly in V2 during static visual stimulation in ways that may contribute to form discrimination.