Neurons In Area MT Research Articles

Spatial integration by MT pattern neurons: A closer look at pattern-to-component effects and the role of speed tuning

The primate visual system faces a difficult problem whenever it encounters the motion of an object moving over a patch of the retina. Objects typically contain a number of edges at different orientations and so a range of image velocities are generated within the receptive field of a neuron processing the object movement. It is still a mystery as to how these different velocities are combined into one unified and correct velocity. Neurons in area MT (V5) are considered to be the neural substrate for this motion integration process. Some MT neurons (pattern type) respond selectively to the correct global motion of an object, whereas others respond primarily to the individual components making up the pattern (component type). Recent findings from MT pattern cells tested with small patches of motion (N. J. Majaj, M. Carandini, & J. A. Movshon, 2007) have put further constraints on the possible mechanisms underlying MT pattern motion integration. We tested and refined an existing model of MT pattern neurons (J. A. Perrone, 2004) using these same small patch stimuli and found that it can accommodate these new findings. We also discovered that the speed of the test stimuli may have had an impact on the N. J. Majaj et al. (2007) results and that MT direction and speed tuning may be more closely linked than previously thought.

Speed perception during acceleration and deceleration

We have recently shown that stimulus acceleration affects subsequent preferred speed and tuning widths of macaque area MT neurons (A. Schlack, B. Krekelberg, & T. D. Albright, 2007). Given the close link between area MT and speed perception, this predicts that speed perception should depend on the acceleration context. Here, we show that this is indeed the case for both speed discrimination and speed perception. Specifically, speed discrimination thresholds improve in an acceleration context but absolute speeds are more underestimated than in a deceleration context. In line with our physiological data, these changes can be understood in terms of speed-dependent adaptation mechanisms in MT and do not require an explicit acceleration dependence of speed perception.

Responses to direction and transparent motion stimuli in area FST of the macaque

Motion transparency occurs when multiple object velocities are present within a local region of retinotopic space. Transparent signals can carry information useful in the segmentation of moving objects and in the extraction of three-dimensional structure from relative motion cues. However, the physiological substrate underlying the detection of motion transparency is poorly understood. Direction tuned neurons in area MT are suppressed by transparent stimuli, suggesting that other motion sensitive areas may be needed to represent this signal robustly. Recent neuroimaging evidence implicated two such areas in the macaque superior temporal sulcus. We studied one of these, FST, with electrophysiological methods and found that a large fraction of the neurons responded well to two opposite directions of motion and to transparent stimuli containing those same directions. A linear combination of MT-like responses qualitatively reproduces this behavior and predicts that FST neurons can be tuned for transparent motion containing specific direction and depth components. We suggest that FST plays a role in motion segmentation based on transparent signals.

Dynamics of neuronal adaptation in macaque MT

Event Abstract Back to Event Dynamics of neuronal adaptation in macaque MT Pascal Wallisch1* and J. Anthony Movshon1 1 University of New York , Center for Neural Science, United States Adaptation alters the sensitivity and selectivity of neuronal responses in visual thalamus and cortex, and is commonly used to probe perceptual and neuronal mechanisms. There is, however, little consistency across laboratories in the details of the design of adaptation experiments. In particular, the literature contains adaptation experiments with adapting periods as brief as 0.25 s and as long as 60 s or more, and we wondered whether the adaptation effects revealed by these designs was the same. At a more fundamental level, the process that transduces visually evoked activity into changes in neuronal function is poorly understood, and more information about its temporal dynamics should help to uncover the underlying mechanisms. We studied adaptation in recordings from single neurons in area MT of anesthetized, paralyzed macaques by presenting drifting sinusoidal gratings of varying contrast and duration and then measuring the resulting modification of neuronal responses. We analyzed two well-known effects of adaptation: the reduction in responsiveness and the alteration of tuning properties. To determine response reduction, we measured responses to varying contrast of otherwise optimal test gratings; to determine tuning shifts, we measured direction tuning for high contrast test gratings after adapting to gratings whose direction was 30 deg displaced from the preferred direction. We confirmed previous findings that prolonged adaptation (40 s with 4 s top-ups) to high contrast targets profoundly reduced neuronal responses to contrast, and shifted neuronal tuning curves about halfway toward the direction of the adapting grating. Brief adaptation (0.25 s) to high contrast targets produced qualitatively similar but quantitatively weaker effects, on average less than one third of those of prolonged adaptation. To probe the mechanisms of short-term adaptation, we varied both the duration and the contrast of the adapting stimuli so that the product of duration and contrast was constant - i.e. we adapted at 0.5 contrast for 0.5 s, 0.25 contrast for 1 s, and so forth. Up to durations of 4 s - the longest we tested - conditions whose time-contrast product was 0.25 produced similar effects on both responsiveness and selectivity. On the other hand, adapting stimuli arranged to evoke roughly the same number of spikes produced less adaptation. We conclude that the mechanisms underlying short- and long-term adaptation are similar in their effect on neuronal properties. The changes in neuronal function are not simply due to the total spiking activity during adaptation, but instead seem to reflect the integrated visual stimulation, as captured by the time-contrast product. Conference: Bernstein Symposium 2008, Munich, Germany, 8 Oct - 10 Oct, 2008. Presentation Type: Poster Presentation Topic: All Abstracts Citation: Wallisch P and Movshon J (2008). Dynamics of neuronal adaptation in macaque MT. Front. Comput. Neurosci. Conference Abstract: Bernstein Symposium 2008. doi: 10.3389/conf.neuro.10.2008.01.093 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 17 Nov 2008; Published Online: 17 Nov 2008. * Correspondence: Pascal Wallisch, University of New York, Center for Neural Science, New York, United States, pascal.wallisch@nyu.edu Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Pascal Wallisch J. Anthony Movshon Google Pascal Wallisch J. Anthony Movshon Google Scholar Pascal Wallisch J. Anthony Movshon PubMed Pascal Wallisch J. Anthony Movshon Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Recent History of Stimulus Speeds Affects the Speed Tuning of Neurons in Area MT

Visual motion processing plays a key role in enabling primates' successful interaction with their dynamic environments. Although in natural environments the speed of visual stimuli continuously varies, speed tuning of neurons in the prototypical motion area MT has traditionally been assessed with stimuli that moved at constant speeds. We investigated whether the representation of speed in a continuously varying stimulus context differs from the representation of constant speeds. We recorded from individual MT neurons of fixating macaques while stimuli moved either at a constant speed or in a linearly accelerating or decelerating manner. We found clear speed tuning even when the stimulus consisted of visual motion with gradual speed changes. There were, however, important differences with the speed tuning as measured with constant stimuli: the stimulus context affected neuronal preferred speed as well as the associated tuning width of the speed tuning curves. These acceleration-dependent changes in response lead to an accurate representation of the acceleration of these stimuli in the MT cells. To elucidate the mechanistic basis of this signal, we constructed a stochastic firing rate model based on the constant speed response profiles. This model incorporated each cell's speed tuning and response adaptation dynamics and accurately predicted the response to constant speeds as well as accelerating and decelerating stimuli. Because the response of the model neurons had no explicit acceleration dependence, we conclude that speed-dependent adaptation creates a strong influence of temporal context on the MT response and thereby results in the representation of acceleration signals.

Reconstructing the World: Switching from Segmentation to Integration Allows Neurons in Area MT to Make “Sense” of the Visual Scene

Huang et al. in this issue of Neuron show that primate area MT neurons exploit contextual cues to adequately interpret motion information. MT neurons switch from segmentation to integration when motion arises from single rather than multiple objects. This switching may help solve the aperture problem and bind distant object components into a perceptual whole.

How MT cells analyze the motion of visual patterns

Neurons in area MT (V5) are selective for the direction of visual motion. In addition, many are selective for the motion of complex patterns independent of the orientation of their components, a behavior not seen in earlier visual areas. We show that the responses of MT cells can be captured by a linear-nonlinear model that operates not on the visual stimulus, but on the afferent responses of a population of nonlinear V1 cells. We fit this cascade model to responses of individual MT neurons and show that it robustly predicts the separately measured responses to gratings and plaids. The model captures the full range of pattern motion selectivity found in MT. Cells that signal pattern motion are distinguished by having convergent excitatory input from V1 cells with a wide range of preferred directions, strong motion opponent suppression and a tuned normalization that may reflect suppressive input from the surround of V1 cells.

Microsaccades Counteract Visual Fading during Fixation

Our eyes move continually, even while we fixate our gaze on an object. If fixational eye movements are counteracted, our perception of stationary objects fades completely, due to neural adaptation. Some studies have suggested that fixational microsaccades refresh retinal images, thereby preventing adaptation and fading. However, other studies disagree, and so the role of microsaccades remains unclear. Here, we correlate visibility during fixation to the occurrence of microsaccades. We asked subjects to indicate when Troxler fading of a peripheral target occurs, while simultaneously recording their eye movements with high precision. We found that before a fading period, the probability, rate, and magnitude of microsaccades decreased. Before transitions toward visibility, the probability, rate, and magnitude of microsaccades increased. These results reveal a direct link between suppression of microsaccades and fading and suggest a causal relationship between microsaccade production and target visibility during fixation.

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.

Comparing Acceleration and Speed Tuning in Macaque MT: Physiology and Modeling

Studies of individual neurons in area MT have traditionally investigated their sensitivity to constant speeds. We investigated acceleration sensitivity in MT neurons by comparing their responses to constant steps and linear ramps in stimulus speed. Speed ramps constituted constant accelerations and decelerations between 0 and 240 degrees /s. Our results suggest that MT neurons do not have explicit acceleration sensitivity, although speed changes affected their responses in three main ways. First, accelerations typically evoked higher responses than the corresponding deceleration rate at all rates tested. We show that this can be explained by adaptation mechanisms rather than differential processing of positive and negative speed gradients. Second, we inferred a cell's preferred speed from the responses to speed ramps by finding the stimulus speed at the latency-adjusted time when response amplitude peaked. In most cells, the preferred speeds inferred from deceleration were higher than those for accelerations of the same rate or from steps in stimulus speed. Third, neuron responses to speed ramps were not well predicted by the transient or sustained responses to steps in stimulus speed. Based on these findings, we developed a model incorporating adaptation and a neuron's speed tuning that predicted the higher inferred speeds and lower spike rates for deceleration responses compared with acceleration responses. This model did not predict acceleration-specific responses, in accordance with the lack of acceleration sensitivity in the neurons. The outputs of this single-cell model were passed to a population-vector-based model used to estimate stimulus speed and acceleration. We show that such a model can accurately estimate relative speed and acceleration using information from the population of neurons in area MT.

Rapid Processing of Retinal Slip During Saccades in Macaque Area MT

The primate middle temporal area (MT) is involved in the analysis and perception of visual motion, which is generated actively by eye and body movements and passively when objects move. We studied the responses of single cells in area MT of awake macaques, comparing the direction tuning and latencies of responses evoked by wide-field texture motion during fixation (passive viewing) and during rewarded, target-directed saccades and non-rewarded, spontaneous saccades over the same stationary texture (active viewing). We found that MT neurons have similar motion sensitivity and direction-selectivity for retinal slip associated with active and passive motion. No cells showed reversals in direction tuning between the active and passive viewing conditions. However, mean latencies were significantly different for saccade-evoked responses (30 ms) and stimulus-evoked responses (67 ms). Our results demonstrate that neurons in area MT retain their direction-selectivity and display reduced processing times during saccades. This rapid, accurate processing of peri-saccadic motion may facilitate post-saccadic ocular following reflexes or corrective saccades.

Dynamics of motion signaling by neurons in macaque area MT

Most neurons in macaque area MT are selective for the direction of stimulus motion. By comparing direction selectivity for gratings and plaids, we classified MT neurons as pattern direction selective (PDS) or component direction selective (CDS). We compared the time course of responses in CDS and PDS neurons in opiate-anesthetized macaques, using a rapid pseudorandom sequence of gratings and plaids that moved in different directions. On average, responses began 6 ms earlier in CDS neurons than in PDS neurons. More importantly, the pattern-selective responses of PDS neurons did not reach their fully selective state until 50-75 ms after the responses of CDS neurons had stabilized. The population motion response of MT is therefore initially dominated by component motion signals, and does not completely represent pattern motion until substantially later. The circuits that compute pattern motion take more time to finish their work than those signaling component motion.

Encoding of dynamic visual stimuli by primate area MT neurons

Neural stimulus selectivity is thought to be optimized for the representation of real-world stimuli. Neural coding properties, therefore, may adapt to different environments. Here, we address the question if tuning curves depend on the statistics of visual stimuli. This is done by studying the directional tuning of macaque area MT neurons exposed to dynamic motion stimuli of two different direction progression statistics. Despite an apparent difference of tuning curves across stimulus conditions, our results support the view that the underlying encoding system is robust and subject to only restricted malleability by stimulus statistics.

The influence of sustained selective attention on stimulus selectivity in macaque visual area MT.

Remarkable alterations of perception during long-lasting attentional processes have been described in several recent studies. Although these findings have gained much interest, almost nothing is known about the modulation of neuronal responses during sustained attention. Therefore, we investigated the effect of prolonged selective attention on neuronal feature selectivity. Awake macaque monkeys were trained to perform a motion-tracking task that required attending one of two simultaneously presented moving bars for up to 15 sec. Extracellular recordings were obtained from neurons in macaque motion-sensitive middle temporal visual area (MT/V5). Under conditions of attention, we found high and constant direction selectivity over time. This was expressed by a strong and persistent response contrast between presentations of preferred and nonpreferred stimuli in successive motion cycles. With attention directed to another moving bar, neuronal responses to the behaviorally irrelevant stimulus became continuously less specific for the direction of motion. In particular, increasingly higher firing rates for motion in null direction caused a strong reduction of direction selectivity, which further increased with enhanced proximity between target and distracter bar. A passive condition experiment revealed that this reduction occurred only when motion remained the behaviorally relevant feature but disappeared when attention was withdrawn from this feature domain. Thus, sustained attention seems to stabilize direction selectivity of neurons in area MT against a time and competition-dependent degradation, whereas nonattended objects suffer from a reduced neuronal representation.

Time course of information about motion direction in visual area MT of macaque monkeys.

We used the responses of neurons in extrastriate visual area MT to determine how well neural noise can be reduced by averaging the responses of neurons across time. For individual MT neurons, we calculated the time course of Shannon information about motion direction from sustained motion at constant velocities. Stimuli were random dot patterns moving at the preferred speed of the cell for 256 msec, in a direction chosen randomly with 15 degrees increments. Information about motion direction calculated from cumulative spike count rose rapidly from the onset of the neural response and then saturated, reaching 80% of maximum information in the first 100 msec. Most of the early saturation of information could be attributed to correlated fluctuations in the spike counts of individual neurons on time scales in excess of 100 msec. Thus, temporal correlations limit the benefits of averaging across time, much as correlations among the responses of different neurons limit the benefits of averaging across large populations. Although information about direction was available quickly from MT neurons, the direction discrimination by individual MT neurons was poor, with mean thresholds above 30 degrees in most neurons. We conclude that almost all available directional information could be extracted from the first few spikes of the response of the neuron, on a time scale comparable with the initiation of smooth pursuit eye movements. However, neural responses still must be pooled across the population in MT to account for the direction discrimination of the pursuit behavior.

Microstimulation of visual cortex affects the speed of perceptual decisions.

Direction-selective neurons in the middle temporal visual area (MT) are crucially involved in motion perception, although it is not known exactly how the activity of these neurons is interpreted by the rest of the brain. Here we report that in a two-alternative task, the activity of MT neurons is interpreted as evidence for one direction and against the other. We measured the speed and accuracy of decisions as rhesus monkeys performed a direction-discrimination task. On half of the trials, we stimulated direction-selective neurons in area MT, thereby causing the monkeys to choose the neurons' preferred direction more often. Microstimulation quickened decisions in favor of the preferred direction and slowed decisions in favor of the opposite direction. Even on trials in which microstimulation did not induce a preferred direction choice, it still affected response times. Our findings suggest that during the formation of a decision, sensory evidence for competing propositions is compared and accumulates to a decision-making threshold.

Neuronal synchrony does not correlate with motion coherence in cortical area MT.

Natural visual scenes are cluttered with multiple objects whose individual features must somehow be selectively linked (or 'bound') if perception is to coincide with reality. Recent neurophysiological evidence supports a 'binding-by-synchrony' hypothesis: neurons excited by features of the same object fire synchronously, while neurons excited by features of different objects do not. Moving plaid patterns offer a straightforward means to test this idea. By appropriate manipulations of apparent transparency, the component gratings of a plaid pattern can be seen as parts of a single coherently moving surface or as two non-coherently moving surfaces. We examined directional tuning and synchrony of area-MT neurons in awake, fixating primates in response to perceptually coherent and non-coherent plaid patterns. Here we show that directional tuning correlated highly with perceptual coherence, which is consistent with an earlier study. Although we found stimulus-dependent synchrony, coherent plaids elicited significantly less synchrony than did non-coherent plaids. Our data therefore do not support the binding-by-synchrony hypothesis as applied to this class of motion stimuli in area MT.

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.

Attentional Modulation Strength in Cortical Area MT Depends on Stimulus Contrast

The attentional modulation of sensory information processing in the visual system is the result of top-down influences, which can cause a multiplicative modulation of the firing rate of sensory neurons in extrastriate visual cortex, an effect reminiscent of the bottom-up effect of changes in stimulus contrast. This similarity could simply reflect the multiplicity of both effects. But, here we show that in direction-selective neurons in monkey visual cortical area MT, stimulus and attentional effects share a nonlinearity. These neurons show higher response gain for both contrast and attentional changes for intermediate contrast stimuli and smaller gain for low- and high-contrast stimuli. This finding suggests a close relationship between the neural encoding of stimulus contrast and the modulating effect of the behavioral relevance of stimuli.

Function of center-surround antagonism for motion in visual area MT/V5: a modeling study

Neurons in cortical area MT or V5 of primates have a large, modulatory region surrounding the classical receptive field. This ‘surround’ has been suggested to be involved in motion segmentation, as well as in shape-from-motion processing. Our hypothesis is that it plays a functional role in both. We verify this by modeling the electrophysiological data obtained by Orban and co-workers in the macaque, and by developing a novel stimulus paradigm. Our results indicate an almost perfect dichotomy between both functionalities: our model neurons code for the object's edge if present, and for the first-order shape otherwise. We further show that small populations of model neurons can code linearly for the orientation-in-depth of translating planes.