Middle Temporal Neurons Research Articles

Estimates of the Contribution of Single Neurons to Perception Depend on Timescale and Noise Correlation

The sensitivity of a population of neurons, and therefore the amount of sensory information available to an animal, is limited by the sensitivity of single neurons in the population and by noise correlation between neurons. For decades, therefore, neurophysiologists have devised increasingly clever and rigorous ways to measure these critical variables (Parker and Newsome, 1998). Previous studies examining the relationship between the responses of single middle temporal (MT) neurons and direction-discrimination performance uncovered an apparent paradox. Sensitivity measurements from single neurons suggested that small numbers of neurons may account for a monkey's psychophysical performance (Britten et al., 1992), but trial-to-trial variability in activity of single MT neurons are only weakly correlated with the monkey's behavior, suggesting that the monkey's decision must be based on the responses of many neurons (Britten et al., 1996). We suggest that the resolution to this paradox lies (1) in the long stimulus duration used in the original studies, which led to an overestimate of neural sensitivity relative to psychophysical sensitivity, and (2) mistaken assumptions (because no data were available) about the level of noise correlation in MT columns with opposite preferred directions. We therefore made new physiological and psychophysical measurements in a reaction time version of the direction-discrimination task that matches neural measurements to the actual decision time of the animals. These new data, considered together with our recent data on noise correlation in MT (Cohen and Newsome, 2008), provide a substantially improved account of psychometric performance in the direction-discrimination task.

Dynamic Readout of Behaviorally Relevant Signals from Area MT during Task Switching

The processes underlying dynamic changes in human behavior during real situations contain much irrelevant information and represent a key issue facing neuroscientists. Although the roles played by the frontal cortex in this switching behavior have been well documented, little is known regarding how neural pathways governing sensorimotor associations accomplish such a switch. We addressed this question by recording activities of middle temporal (MT) neurons in monkeys switching between direction versus depth discrimination tasks. Although the monkeys successfully switched between the tasks, neural sensitivity did not change as a function of task. More importantly, neurons that signaled the same motor output showed trial-to-trial covariation between neuronal responses and perceptual judgments during both tasks, whereas neurons that signaled the opposite motor output showed no covariation in either task. These results suggest that task switching is accomplished via communication from distinct populations of neurons when sensorimotor associations switch within a short time period.

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.

The Effect of Middle Temporal Spike Phase on Sensory Encoding and Correlates with Behavior during a Motion-Detection Task

Previous studies have shown that sensory neurons that are the most informative of the stimulus tend to be the best correlated with the subject's perceptual decision. We wanted to know whether this relationship might also apply to short time segments of a neuron's response. We asked whether spikes that conveyed more information about a motion stimulus were also more tightly linked to the perceptual behavior. We examined single-neuron activity in middle temporal (MT) area while monkeys performed a motion-detection task. Because of a slow stimulus update (every 27 ms), activity in many MT neurons was entrained and phase-locked to the stimulus. These stimulus-entrained neuronal oscillations allowed us to separate spikes based on phase. We observed a large amount of variability in how spikes at different phases of the oscillation encoded the stimulus, as revealed by the spike-triggered average of the motion. Spikes during certain phases of the cycle were much more informative about the presence of coherent motion than others. Importantly, we found that the phases that were the most informative about the motion stimulus were also more correlated with the behavioral performance and reaction time of the animal. Our results suggest that the relationship between a neuron's spikes, the stimulus, and behavior can vary on a time scale of tens of milliseconds.

Effect of Vertical Disparities on Depth Representation in Macaque Monkeys: MT Physiology and Behavior

Horizontal binocular disparities provide information about the distance of objects relative to the point of ocular fixation and must be combined with an estimate of viewing distance to recover the egocentric distance of an object. Vergence angle and the gradient of vertical disparities across the visual field are thought to provide independent sources of viewing distance information based on human behavioral studies. Although the effect of vergence angle on horizontal disparity selectivity in early visual cortex has been examined (with mixed results), the effect of the vertical disparity field has not been explored. We manipulated the vertical disparities in a large random-dot stimulus to simulate different viewing distances, and we examined the effect of this manipulation on both the responses of neurons in the middle temporal (MT) area and on the psychophysical performance of the animal in a curvature discrimination task. We report here that alterations to the vertical disparity field have no effect on the horizontal disparity tuning of MT neurons. However, the same manipulation strongly and systematically biases the monkey's judgments of curvature, consistent with previous human studies. We conclude that monkeys, like humans, make use of the vertical disparity field to estimate viewing distance, but that the physiological mechanisms for this effect occur either downstream of MT or in a different pathway.

Stimulus encoding and correlates with behavior in area MT of visual cortex is dependent on spike phase

How is the activity of neurons in the sensory areas of cortex related to our perceptual abilities? Past studies have suggested that sensory neurons that best encode a visual stimulus are also more influential in forming the perception of the stimulus. We wanted to know if this relationship also extended to individual action potentials. If some spikes encode the stimulus better than others, then would these same spikes have more weight in supporting the perceptual behavior? To address this question, data from a past motion detection experiment was analyzed [1]. In this study, two monkeys were trained to detect the onset of coherent motion in a random dot patch that initially contained 0% coherent motion. The coherent motion signal occurred at a random time and the animals were rewarded for responding within a 750 ms window. Extracellular recordings were made from single neurons in the Middle Temporal (MT) area. The random dot patch overlapped the receptive field of the neuron and the coherent motion was matched to the neuron's preferred direction and speed. Importantly, the position of the random dots was only updated once every 27 ms. Because of the slow motion update rate, the neural activity of many of the MT neurons oscillated at the same frequency as the motion updates. It was these oscillations that allowed us to ask if some spikes were more influential than others by measuring how sensory and choice related information varied as a function of the phase of the oscillation. To determine whether some spikes encoded the stimulus better than others, we examined the difference between spikes on the rising phase of the oscillation (from the trough to the peak) compared to spikes on the falling phase (peak to trough). Using the spike-triggered average of the motion stimulus, we found that spikes did not equally represent sensory information. Spikes occurring during the rising phase of the stimulus-induced oscillation encoded stronger motion than spikes occurring during the falling phase. Importantly, the same spikes that encoded stronger motion were also more correlated with the animal's behavioral performance and reaction time. This suggests that the spikes carrying the most reliable task related information are more strongly linked to the behavioral decision. In addition, these results support the hypothesis that phase could be used as a possible encoding scheme during neuronal oscillations.

Attention to Surfaces Modulates Motion Processing in Extrastriate Area MT

In the visual system, early atomized representations are grouped into higher-level entities through processes of perceptual organization. Here we present neurophysiological evidence that a representation of a simple object, a surface defined by color and motion, can be the unit of attentional selection at an early stage of visual processing. Monkeys were cued by the color of a fixation spot to attend to one of two transparent random-dot surfaces, one red and one green, which occupied the same region of space. Motion of the attended surface drove neurons in the middle temporal (MT) visual area more strongly than physically identical motion of the non-attended surface, even though both occurred within the spotlight of attention. Surface-based effects of attention persisted even without differential surface coloring, but attentional modulation was stronger with color. These results show that attention can select surface representations to modulate visual processing as early as cortical area MT.

MST Neurons Code for Visual Motion in Space Independent of Pursuit Eye Movements

When a person tracks a small moving object, the visual images in the background of the visual scene move across his/her retina. It, however, is possible to estimate the actual motion of the images despite the eye-movement-induced motion. To understand the neural mechanism that reconstructs a stable visual world independent of eye movements, we explored areas MT (middle temporal) and MST (medial superior temporal) in the monkey cortex, both of which are known to be essential for visual motion analysis. We recorded the responses of neurons to a moving textured image that appeared briefly on the screen while the monkeys were performing smooth pursuit or stationary fixation tasks. Although neurons in both areas exhibited significant responses to the motion of the textured image with directional selectivity, the responses of MST neurons were mostly correlated with the motion of the image on the screen independent of pursuit eye movement, whereas the responses of MT neurons were mostly correlated with the motion of the image on the retina. Thus these MST neurons were more likely than MT neurons to distinguish between external and self-induced motion. The results are consistent with the idea that MST neurons code for visual motion in the external world while compensating for the counter-rotation of retinal images due to pursuit eye movements.

A Single Mechanism Can Explain the Speed Tuning Properties of MT and V1 Complex Neurons

A recent study by Priebe et al., (2006) has shown that a small proportion (27%) of primate directionally selective, complex V1 neurons are tuned for the speed of image motion. In this study, I show that the weighted intersection mechanism (WIM) model, which was previously proposed to explain speed tuning in middle temporal neurons, can also explain the tuning found in complex V1 neurons. With the addition of a contrast gain mechanism, this model is able to replicate the effects of contrast on V1 speed tuning, a phenomenon that was recently discovered by Priebe et al., (2006). The WIM model simulations also indicate that V1 neuron spatiotemporal frequency response maps may be asymmetrical in shape and hence poorly characterized by the symmetrical two-dimensional Gaussian fitting function used by Priebe et al., (2006) to classify their cells. Therefore, the actual proportion of speed tuning among directional complex V1 cells may be higher than the 27% estimate suggested by these authors.

Responses of Neurons in the Medial Superior Temporal Visual Area to Apparent Motion Stimuli in Macaque Monkeys

Monkeys fixated a stationary spot during presentation of dot textures that moved in apparent motion defined by the spatial and temporal separations, Deltax and Deltat, between successive flashes of each dot. For each neuron, we assessed the speed tuning for smooth motion (Deltat = 2 or 4 ms) at speeds < or =128 degrees /s and the effect of varying the value of Deltat at speeds of 16 and 32 degrees /s. Many medial superior temporal (MST) neurons, like middle temporal (MT) neurons, were tuned for the speed of smooth motion and showed decreases in firing rate as the value of Deltat increased at a constant speed. A subset of MST neurons, however, showed monotonically increasing firing rates as a function of smooth stimulus speed and responses to apparent motion that paralleled a previously discovered illusion where estimates of target speed increase with the value of Deltat. Opponent firing rate, defined as the difference between responses for motion in the preferred and opposite directions, peaked at values of Deltat that were consistent with the behavioral illusion. Comparison with a new sample of MT neurons recorded with the same stimuli failed to reveal comparable effects. Attempts to map the population responses in MT and MST onto the behavioral illusion of increased speed succeeded by averaging the opponent response across MST neurons, but only by applying vector averaging to determine the preferred speed of the most active MT neurons. We suggest that a vector-averaging computation transforms MT's place code for target speed into the rate code of some MST neurons.

Experience-dependent representation of visual categories in parietal cortex

Categorization is a process by which the brain assigns meaning to sensory stimuli. Through experience, we learn to group stimuli into categories, such as 'chair', 'table' and 'vehicle', which are critical for rapidly and appropriately selecting behavioural responses. Although much is known about the neural representation of simple visual stimulus features (for example, orientation, direction and colour), relatively little is known about how the brain learns and encodes the meaning of stimuli. We trained monkeys to classify 360 degrees of visual motion directions into two discrete categories, and compared neuronal activity in the lateral intraparietal (LIP) and middle temporal (MT) areas, two interconnected brain regions known to be involved in visual motion processing. Here we show that neurons in LIP--an area known to be centrally involved in visuo-spatial attention, motor planning and decision-making-robustly reflect the category of motion direction as a result of learning. The activity of LIP neurons encoded directions of motion according to their category membership, and that encoding shifted after the monkeys were retrained to group the same stimuli into two new categories. In contrast, neurons in area MT were strongly direction selective but carried little, if any, explicit category information. This indicates that LIP might be an important nexus for the transformation of visual direction selectivity to more abstract representations that encode the behavioural relevance, or meaning, of stimuli.

Linking Neural Representation to Function in Stereoscopic Depth Perception: Roles of the Middle Temporal Area in Coarse versus Fine Disparity Discrimination

Neurons selective for binocular disparity form the neural substrate for stereoscopic depth perception and are found in several areas of primate visual cortex. Presumably, multiple representations of disparity exist to serve different functions, but the specific contributions of different visual areas to depth perception remain poorly understood. We examine this issue by comparing the contributions of the middle temporal (MT) area to performance of two depth discrimination tasks: a "coarse" task that involves discrimination between absolute disparities in the presence of noise, and a "fine" task that involves discrimination of very small differences in relative disparity between two stimuli in the absence of noise. In the fine task, we find that electrical microstimulation of MT does not affect perceptual decisions, although many individual MT neurons have sufficient sensitivity to account for behavioral performance. In contrast, microstimulation at the same recording sites does bias depth percepts in the coarse task. We hypothesized that these results may be explained by the fact that MT neurons do not represent relative disparity signals that are thought to be essential for the fine task. This hypothesis was supported by single-unit recordings that show that MT neurons signal absolute, but not relative, disparities in a stimulus configuration similar to that used in the fine task. This work establishes a link between the neural representation of disparity in MT and the functional contributions of this area to depth perception.

Neural population code for fine perceptual decisions in area MT

In the middle temporal (MT) area of primates, many motion-sensitive neurons with a wide range of preferred directions respond to a stimulus moving in a single direction. These neurons are involved in direction perception, but it is not clear how perceptual decisions are related to the population response. We recorded the activities of MT neurons in rhesus monkeys while they discriminated closely related directions, and examined the relationship between the activities of neurons tuned to different directions and the monkeys' choices. Perceptual decisions were significantly correlated with the activities of the highest-precision neurons but not with those of the lowest-precision neurons. The combined performance of the high-precision neurons matched the monkeys' behavior, whereas the ability to predict behavior based on the entire active population was poor. These results suggest that fine discrimination decisions are crucially dependent on the activities of the most informative neurons.

Attentional modulation of motion integration of individual neurons in the middle temporal visual area.

We examined how spatially directed attention affected the integration of motion in neurons of the middle temporal (MT) area of visual cortex. We recorded from single MT neurons while monkeys performed a motion detection task under two attentional states. Using 0% coherent random dot motion, we estimated the optimal linear transfer function (or kernel) between the global motion and the neuronal response. This linear kernel filtered the random dot motion across direction, speed, and time. Slightly less than one-half of the neurons produced reasonably well defined kernels that also tended to account for both the directional selectivity and responses to coherent motion of different strengths. This subpopulation of cells had faster, more transient, and more robust responses to visual stimuli than neurons with kernels that did not contain well defined regions of integration. For those neurons that had large attentional modulation and produced well defined kernels, we found attention scaled the temporal profile of the transfer function with no appreciable shift in time or change in shape. Thus, for MT neurons described by a linear transfer function, attention produced a multiplicative scaling of the temporal integration window.

A visual motion sensor based on the properties of V1 and MT neurons

The motion response properties of neurons increase in complexity as one moves from primary visual cortex (V1), up to higher cortical areas such as the middle temporal (MT) and the medial superior temporal area (MST). Many of the features of V1 neurons can now be replicated using computational models based on spatiotemporal filters. However until recently, relatively little was known about how the motion analysing properties of MT neurons could originate from the V1 neurons that provide their inputs. This has constrained the development of models of the MT–MST stages which have been linked to higher level motion processing tasks such as self-motion perception and depth estimation. I describe the construction of a motion sensor built up in stages from two spatiotemporal filters with properties based on V1 neurons. The resulting composite sensor is shown to have spatiotemporal frequency response profiles, speed and direction tuning responses that are comparable to MT neurons. The sensor is designed to work with digital images and can therefore be used as a realistic front-end to models of MT and MST neuron processing; it can be probed with the same two-dimensional motion stimuli used to test the neurons and has the potential to act as a building block for more complex models of motion processing.

Contribution of Area MT to Stereoscopic Depth Perception: Choice-Related Response Modulations Reflect Task Strategy

Due to the diversity of tuning properties in sensory cortex, only a fraction of neurons are engaged in a particular task. Characterizing the tuning properties of neurons that are functionally linked to behavior is essential for understanding how activity is “read out” from sensory maps to guide decisions. We recorded from middle temporal (MT) neurons while monkeys performed a depth discrimination task, and we characterized the linkage between MT responses and behavioral choices. Trial-to-trial response fluctuations of MT neurons with odd-symmetric (“Near,” “Far”) disparity tuning were predictive of monkeys' choices, whereas responses of neurons with even-symmetric tuning were not. This result cannot be explained by neuronal sensitivity or any other response property of MT neurons that we examined but is simply explained by the task strategy that monkeys learned during training. We suggest that this approach provides a physiological means to explore how task strategies are implemented in the brain.

Perceptual "read-out" of conjoined direction and disparity maps in extrastriate area MT.

Cortical neurons are frequently tuned to several stimulus dimensions, and many cortical areas contain intercalated maps of multiple variables. Relatively little is known about how information is “read out” of these multidimensional maps. For example, how does an organism extract information relevant to the task at hand from neurons that are also tuned to other, irrelevant stimulus dimensions? We addressed this question by employing microstimulation techniques to examine the contribution of disparity-tuned neurons in the middle temporal (MT) visual area to performance on a direction discrimination task. Most MT neurons are tuned to both binocular disparity and the direction of stimulus motion, and MT contains topographic maps of both parameters. We assessed the effect of microstimulation on direction judgments after first characterizing the disparity tuning of each stimulation site. Although the disparity of the stimulus was irrelevant to the required task, we found that microstimulation effects were strongly modulated by the disparity tuning of the stimulated neurons. For two of three monkeys, microstimulation of nondisparity-selective sites produced large biases in direction judgments, whereas stimulation of disparity-selective sites had little or no effect. The binocular disparity was optimized for each stimulation site, and our result could not be explained by variations in direction tuning, response strength, or any other tuning property that we examined. When microstimulation of a disparity-tuned site did affect direction judgments, the effects tended to be stronger at the preferred disparity of a stimulation site than at the nonpreferred disparity, indicating that monkeys can selectively monitor direction columns that are best tuned to an appropriate conjunction of parameters. We conclude that the contribution of neurons to behavior can depend strongly upon tuning to stimulus dimensions that appear to be irrelevant to the current task, and we suggest that these findings are best explained in terms of the strategy used by animals to perform the task.

Estimating target speed from the population response in visual area MT.

To guide behavior, perceptual and motor systems must estimate properties of the sensory environment from the responses of populations of cortical neurons. In the domain of visual motion, estimates of target speed are derived from the responses of motion-sensitive neurons in the middle temporal (MT) area of the extrastriate visual cortex and are used to drive smooth pursuit eye movements and perceptual judgments of speed. We have asked how these behavioral systems estimate target speed from the population response in area MT. We found that increasing the spatial frequency of a sine wave grating caused decreases in the target speed estimated by both pursuit and perception and commensurate changes in the identity of the active neurons in area MT. Decreasing the contrast of a sine wave grating caused decreases in the target speed estimated by both pursuit and perception, while altering only the response amplitude of MT neurons and not the identity of the active neurons. Applying a modified vector-averaging computation to the population response measured in area MT allowed us to predict the effects of both spatial frequency and contrast on speed estimation for both perception and pursuit. The modification biased the speed estimation toward low target speeds when responses across the population of neurons were small.

Macaque Middle Temporal Neurons Signal Depth in the Absence of Motion

The middle temporal (MT) visual area is widely accepted to play important roles in motion processing. It is unclear, however, whether MT contributes to visual perception during the viewing of static scenes, when there is little retinal image motion during the interval between saccades. Some previous studies suggest that MT neurons give little or no response to stationary stimuli that are flashed onto the receptive field, but no previous study has directly examined the fidelity with which MT neurons code visual information in moving versus stationary stimuli. In this study, we compare the ability of MT neurons to signal binocular disparity in moving versus stationary random-dot stereograms. Although responses to moving stimuli are typically stronger, many MT neurons give robust responses to stationary stereograms, and some MT neurons actually prefer stationary patterns to those moving at any tested speed. These responses to stationary stimuli are not caused by monitor refresh or microsaccades. Disparity tuning curves for moving and stationary stimuli are nearly identical in shape for most neurons. Although the disparity discriminability of MT neurons is generally higher for moving stereograms when responses are averaged over the entire 1.5 sec trial epoch, discriminability is comparable for moving and stationary stimuli during the first 200-300 msec of the response. Thus, in a normal time interval between saccades, MT neurons signal the binocular disparity of stationary stimuli with high fidelity. These findings show that MT can be a reliable source of visual information during the viewing of static scenes.

Disparity-Based Coding of Three-Dimensional Surface Orientation by Macaque Middle Temporal Neurons

Gradients of binocular disparity across the visual field provide a potent cue to the three-dimensional (3-D) orientation of surfaces in a scene. Neurons selective for 3-D surface orientation defined by disparity gradients have recently been described in parietal cortex, but little is known about where and how this selectivity arises within the visual pathways. Because the middle temporal area (MT) has previously been implicated in depth perception, we tested whether MT neurons could signal the 3-D orientation (as parameterized by tilt and slant) of planar surfaces that were depicted by random-dot stereograms containing a linear gradient of horizontal disparities. We find that many MT neurons are tuned for 3-D surface orientation, and that tilt and slant generally have independent effects on MT responses. This separable coding of tilt and slant is reminiscent of the joint coding of variables in other areas (e.g., orientation and spatial frequency in V1). We show that tilt tuning remains unchanged when all coherent motion is removed from the visual stimuli, indicating that tilt selectivity is not a byproduct of 3-D velocity coding. Moreover, tilt tuning is typically insensitive to changes in the mean disparity (depth) of gradient stimuli, indicating that tilt tuning cannot be explained by conventional tuning for frontoparallel disparities. Finally, we explore the receptive field mechanisms underlying selectivity for 3-D surface orientation, and we show that tilt tuning arises through heterogeneous disparity tuning within the receptive fields of MT neurons. Our findings show that MT neurons carry high-level signals about 3-D surface structure, in addition to coding retinal image velocities.