Cone signal interactions in direction-selective neurons in the middle temporal visual area (MT)

The true receptive field of more than 90% of neurons in the middle temporal visual area (MT) extends well beyond the classical receptive field (crf), as mapped with conventional bar or spot stimuli, and includes a surrounding region that is 50 to 100 times the area of the crf. These extensive surrounds are demonstrated by simultaneously stimulating the crf and the surround with moving stimuli. The surrounds commonly have directional and velocity-selective influences that are antagonistic to the response from the crf. The crfs of MT neurons are organized in a topographic representation of the visual field. Thus MT neurons are embedded in an orderly visuotopic array, but are capable of integrating local stimulus conditions within a global context. The extensive surrounds of MT neurons may be involved in figure-ground discrimination, preattentive vision, perceptual constancies, and depth perception through motion cues.

The function of smooth pursuit is to keep the fovea pointed at a small visual target that moves smoothly across a patterned background. Chemical lesions, single cell recordings, and behavioral measures have shown that the cortical motion processing pathways form the afferent limb for pursuit. Important areas include at least the striate cortex and the middle temporal visual area, and probably the medial superior temporal visual area and the posterior parietal cortex. We argue that the visual inputs are transmitted through a simple sensory motor interface in the pons, to the efferent limb in the brain stem and cerebellum. The efferent limb uses neural velocity memory to maintain pursuit automatically. We present evidence that the velocity memory is provided, at least in part, by eye velocity positive feedback between the flocculus of the cerebellum and the brain stem. Finally, we use a computer model to show how the maintenance of pursuit can be simulated on a millisecond time scale. The structure and internal elements of the model are based on the biological experiments reviewed in our paper. In the past five years, progress on the neural basis of pursuit eye movements has been rapid. Several areas of research have made substantial contributions, by using combinations of new and conventional methods. Many of the pathways that contribute to pursuit have been identified, and their physiological activity and functions are becoming understood. Continuing progress promises to yield an understanding of one specific form of visually guided movement, at the level of neuronal circuits and behavior, in the primate.

We previously showed that human subjects are better able to discriminate the direction of a motion signal in dynamic noise when the signal is distinguished (segmented) from the noise by color. This finding suggested a hitherto unexplored avenue of interaction between motion and color pathways in the primate visual system. To examine whether chromatic segmentation exerts a similar influence on cortical neurons that contribute to motion direction discrimination, we have now compared the discriminative capacity of single MT neurons and psychophysical observers viewing motion signals with and without chromatic segmentation. All data were obtained from rhesus monkeys trained to discriminate motion direction in dynamic stimuli containing varying proportions of coherently moving (signal) and randomly moving (noise) dots. We obtained psychophysical and neurophysiological data in the same animals, on the same trials, and using the same visual display. Chromatic segmentation of the signal from the noise enhanced both neuronal and psychophysical sensitivity to the motion signal but had a smaller influence on neuronal than on psychophysical sensitivity. Hence the ratio of neuronal to psychophysical thresholds, one measure of the relation between neuronal and psychophysical performance, depended on chromatic segmentation. Increased neuronal sensitivity to chromatically segmented displays stemmed from larger and less noisy responses to motion in the preferred directions of the neurons, suggesting that specialized mechanisms influence responses in the motion pathway when color segments motion signal in visual scenes. These findings lead us to reevaluate potential mechanisms for pooling of MT responses and the role of MT in motion perception.

A critical step in the interpretation of the visual world is the integration of the various local motion signals generated by moving objects. This process is complicated by the fact that local velocity measurements can differ depending on contour orientation and spatial position. Specifically, any local motion detector can measure only the component of motion perpendicular to a contour that extends beyond its field of view. This "aperture problem" is particularly relevant to direction-selective neurons early in the visual pathways, where small receptive fields permit only a limited view of a moving object. Here we show that neurons in the middle temporal visual area (known as MT or V5) of the macaque brain reveal a dynamic solution to the aperture problem. MT neurons initially respond primarily to the component of motion perpendicular to a contour's orientation, but over a period of approximately 60 ms the responses gradually shift to encode the true stimulus direction, regardless of orientation. We also report a behavioural correlate of these neural responses: the initial velocity of pursuit eye movements deviates in a direction perpendicular to local contour orientation, suggesting that the earliest neural responses influence the oculomotor response.

A recurrent theme in the organization of vertebrate visual cortex is that of receptive fields with an associated "silent" opponency component. In the middle temporal area (area MT), a cortical visual area involved in the analysis of retinal motion in primates, this opponency appears in the form of a region outside the classical receptive field (CRF) that in itself gives no response but suppresses responses to motion evoked within the CRF. This antagonistic motion surround has been described as very large and symmetrically arrayed around the CRF. On the basis of this view, the primary function of the surround has long been thought to consist of simple figure-ground segregation based on movement. We have made use of small stimulus patches to map the form and extent of the surround and find evidence that the surround inhibition of many MT cells is in fact confined to restricted regions on one side or on opposite sides of the CRF. Such regions endow MT cells with the ability to make local-to-local motion comparisons, capable of extracting more complex features from the visual environment, and as such, may be better viewed as intrinsic parts of the receptive field, rather than as separate entities responsible for local-to-global comparisons.

BackgroundPatients with bilateral vestibular failure (BVF) suffer from oscillopsia during head movements. This is secondary to the loss of the vestibulo-ocular reflex which is responsible for stabilising retinal images during...

The visual system is continually inundated with information received by the eyes. Only a fraction of this information appears to reach visual awareness. This process of selection is one of the functions ascribed to visual attention. Although many studies have investigated the role of attention in shaping neuronal representations in cortical areas, few have focused on attentional modulation of neuronal signals related to visual motion. We recorded from 89 direction-selective neurons in middle temporal (MT) and medial superior temporal (MST) visual cortical areas of two macaque monkeys using identical sensory stimulation under various attentional conditions. Neural responses in both areas were greatly influenced by attention. When attention was directed to a stimulus inside the receptive field of a neuron, responses in MT and MST were enhanced an average of 20 and 40% compared with a condition in which attention was directed outside the receptive field. Even stronger average enhancements (70% in MT and 100% in MST) were observed when attention was switched from a stimulus moving in the nonpreferred direction inside the receptive field to another stimulus in the receptive field that was moving in the preferred direction. These findings show that attention modulates motion processing from stages early in the dorsal visual pathway by selectively enhancing the representation of attended stimuli and simultaneously reducing the influence of unattended stimuli.

Neurons selective for binocular disparity are found in a number of visual cortical areas in primates, but there is little evidence that any of these areas are specialized for disparity processing. We have examined the organization of disparity-selective neurons in the middle temporal visual area (MT), an area shown previously to contain an abundance of disparity-sensitive neurons. We recorded extracellularly from MT neurons at regularly spaced intervals along electrode penetrations that passed through MT either normal to the cortical surface or at a shallow oblique angle. Comparison of multiunit and single-unit recordings shows that neurons are clustered in MT according to their disparity selectivity. Across the surface of MT, disparity-selective neurons are found in discrete patches that are separated by regions of MT that exhibit poor disparity tuning. Within disparity-selective patches of MT, we typically observe a smooth progression of preferred disparities (e.g. , near to far) as our electrode travels parallel to the cortical surface. In electrode penetrations normal to the cortical surface, on the other hand, MT neurons generally have similar disparity tuning, with little variation from one recording site to the next. Thus disparity-tuned neurons are organized into cortical columns by preferred disparity, and preferred disparity is mapped systematically within larger, disparity-tuned patches of MT. Combined with other recent findings, the data suggest that MT plays an important role in stereoscopic depth perception in addition to its well known role in motion perception.

We recorded behavioral, perceptual, and neural responses to targets that provided apparent visual motion consisting of a sequence of stationary flashes. Increasing the flash separation degrades the quality of motion, but for some separations evoked larger smooth pursuit responses from both humans and monkeys than did smooth motion. The same flash separations also produced an increase in perceived speed in humans. Recordings from single neurons in the middle temporal visual area (MT) of awake monkeys revealed a potential basis for the illusion in the population response. Apparent motion produced diminished neural responses relative to smooth motion. However, neurons with slow preferred speeds were more affected than were those with fast preferred speeds. Increasing the flash separation thus caused the population response to become diminished in amplitude and to shift so that the most active neurons had higher preferred speeds. The entire constellation of effects of apparent motion on the magnitude and latency of the initial pursuit response was accounted for if the MT population response was decoded by (1) creating an opponent motion signal for each neuron by treating its preferred and opposite direction responses as those of a pair of oppositely tuned neurons and (2) computing the vector average of these opponent motion signals. Other ways of decoding the population response recorded in MT failed to account for one or more aspects of behavior. We conclude that the effects of apparent motion on both pursuit and perception can be accounted for if target speed is estimated from the MT population response by a neural computation that implements a vector average based on opponent motion.

It remains unclear how attention affects the tuning of individual neurons in visual cerebral cortex. Some observations suggest that attention preferentially enhances responses to low contrast stimuli, whereas others suggest that attention proportionally affects responses to all stimuli. Resolving how attention affects responses to different stimuli is essential for understanding the mechanism by which it acts. To explore the effects of attention on stimuli of different contrasts, we recorded from individual neurons in the middle temporal visual area (MT) of rhesus monkeys while shifting their attention between preferred and nonpreferred stimuli within their receptive fields. This configuration results in robust attentional modulation that makes it possible to readily distinguish whether attention acts preferentially on low contrast stimuli. We found no evidence for greater enhancement of low contrast stimuli. Instead, the strong attentional modulations were well explained by a model in which attention proportionally enhances responses to stimuli of all contrasts. These data, together with observations on the effects of attention on responses to other stimulus dimensions, suggest that the primary effect of attention in visual cortex may be to simply increase the strength of responses to all stimuli by the same proportion.

Human speed discrimination thresholds follow Weber's law over a large range of reference (i.e., pedestal) speeds, that is, the just-noticeable-difference in speed scales in proportion to the reference speed. We analyzed the neural representation of speed information in macaque middle temporal visual area (MT) to determine whether this representation can account for the basic form of psychophysical data. Based on theoretical considerations, we hypothesized: (1) that the speed tuning curves of MT neurons should be bell-shaped (Gaussian) as a function of the logarithm of speed, (2) that the set of speed-tuning curves should be approximately scale-invariant, (3) that the distribution of speed preferences should be approximately uniform in log speed, and (4) that response variability should be independent of speed preference. Our quantitative analysis of data from 501 MT neurons shows that the neural representation of speed approximately obeys these constraints, with modest deviations particularly at slow speeds. We then used the MT data to predict how speed discrimination thresholds should depend on pedestal speed. The shape of this prediction matches very closely to that of human psychophysical data, accounting for constant Weber fractions over a large range of intermediate speeds as well as a marked departure from Weber's law at slow speeds. Moreover, we show that deviations of the MT representation from the above constraints are important for predicting how psychophysical thresholds depart from Weber's law at slow speeds. These findings support the notion that a logarithmic, approximately scale-invariant representation of speed in area MT limits perceptual speed discrimination.

The neural basis of smooth pursuit eye movements in the rhesus monkey brain

A fundamental question concerning representation of the visual world in our brain is how a cortical cell responds when presented with more than a single stimulus. We find supportive evidence that most cells presented with a pair of stimuli respond predominantly to one stimulus at a time, rather than a weighted average response. Traditionally, the firing rate is assumed to be a weighted average of the firing rates to the individual stimuli (response-averaging model) (Bundesen et al., 2005). Here, we also evaluate a probability-mixing model (Bundesen et al., 2005), where neurons temporally multiplex the responses to the individual stimuli. This provides a mechanism by which the representational identity of multiple stimuli in complex visual scenes can be maintained despite the large receptive fields in higher extrastriate visual cortex in primates. We compare the two models through analysis of data from single cells in the middle temporal visual area (MT) of rhesus monkeys when presented with two separate stimuli inside their receptive field with attention directed to one of the two stimuli or outside the receptive field. The spike trains were modeled by stochastic point processes, including memory effects of past spikes and attentional effects, and statistical model selection between the two models was performed by information theoretic measures as well as the predictive accuracy of the models. As an auxiliary measure, we also tested for uni- or multimodality in interspike interval distributions, and performed a correlation analysis of simultaneously recorded pairs of neurons, to evaluate population behavior.

The origins and terminations of the amygdaloid connections with the modality-specific visual cortical areas TEa (anterior TE area), TEp (posterior TE area), TEO, V4, V2, MST (medial superior temporal visual area), MT (middle temporal visual area), and V1 were studied in macaques. These were compared with the amygdaloid connections of a vision-related polysensory area TG by making cortical injections of horseradish peroxidase (HRP) and incubating the sections with tetramethylbenzidine (TMB) as the chromogen. Both areas TEa and TEp receive a major projection from the lateral basal nucleus and a minor one from the accessory basal nucleus of the amygdaloid complex, whereas these areas send a major projection to the lateral nucleus and a minor one to the lateral basal nucleus. Areas TEO, V4, V2, MST, MT, and V1 receive projections only from the lateral basal nucleus; none of them project to any amygdaloid nucleus. Thus, the amygdalofugal projections are more widespread and more complex than the amygdalopetal projections. These findings indicate that the connections between the amygdaloid nuclei and the visual areas are generally nonreciprocal and underlie the importance of a feedback mechanism from the amygdala to the visual cortical areas in visual information processing. There appears to be a caudorostral (occipitotemporal) gradient in the distribution and density of the amygdaloid projections, which become progressively more widespread and heavier among the progressively more rostral visual areas (from area V1 to area TEa). The amygdaloid connections with area TG are distinctly different from the connections with the visual areas. Area TG is reciprocally connected mainly with the periamygdaloid cortex, and with the lateral, accessory basal, and medial basal nuclei of the amygdala as well.

Segregation of object and background motion in visual area MT: effects of microstimulation on eye movements.