MT Neurons Research Articles

Active Vision: Fixational Eye Movements Help Seeing Space in Time

The significance of the miniature eye movements that we make during visual fixation has been intensely debated for the last 80 years. Recent studies have revealed that these motions of the eyes fulfill an important functional role: helping to extract useful information from natural scenes.

Further Analysis of Efficient Portfolios with the USER Data

Primates can attentively track moving objects while keeping gaze stationary. The neural mechanisms underlying this ability are poorly understood. We investigated this issue by recording responses of neurons in area MT of two rhesus monkeys while they performed two different tasks. During the Attend-Fixation task, two moving random dot patterns (RDPs) translated across a screen at the same speed and in the same direction while the animals directed gaze to a fixation spot and detected a change in its luminance. During the Tracking task, the animals kept gaze on the fixation spot and attentively tracked the two RDPs to report a change in the local speed of one of the patterns9 dots. In both conditions, neuronal responses progressively increased as the RDPs entered the neurons9 receptive field (RF), peaked when they reached its center, and decreased as they translated away. This response profile was well described by a Gaussian function with its center of gravity indicating the RF center and its flanks the RF excitatory borders. During Tracking, responses were increased relative to Attend-Fixation, causing the Gaussian profiles to expand. Such increases were proportionally larger in the RF periphery than at its center, and were accompanied by a decrease in the trial-to-trial response variability (Fano factor) relative to Attend-Fixation. These changes resulted in an increase in the neurons9 performance at detecting targets at longer distances from the RF center. Our results show that attentive tracking dynamically changes MT neurons9 RF profiles, ultimately improving the neurons9 ability to encode the tracked stimulus features.

Tuned Normalization Explains the Size of Attention Modulations

The effect of attention on firing rates varies considerably within a single cortical area. The firing rate of some neurons is greatly modulated by attention while others are hardly affected. The reason for this variability across neurons is unknown. We found that the variability in attention modulation across neurons in area MT of macaques can be well explained by variability in the strength of tuned normalization across neurons. The presence of tuned normalization also explains a striking asymmetry in attention effects within neurons: when two stimuli are in a neuron's receptive field, directing attention to the preferred stimulus modulates firing rates more than directing attention to the nonpreferred stimulus. These findings show that much of the neuron-to-neuron variability in modulation of responses by attention depends on variability in the way the neurons process multiple stimuli, rather than differences in the influence of top-down signals related to attention.

Inferotemporal Cortex Subserves Three-Dimensional Structure Categorization

We perceive real-world objects as three-dimensional (3D), yet it is unknown which brain area underlies our ability to perceive objects in this way. The macaque inferotemporal (IT) cortex contains neurons that respond selectively to 3D structures defined by binocular disparity. To examine the causal role of IT in the categorization of 3D structures, we electrically stimulated clusters of IT neurons with a similar 3D-structure preference while monkeys performed a 3D-structure categorization task. Microstimulation of 3D-structure-selective IT clusters caused monkeys to choose the preferred structure of the 3D-structure-selective neurons considerably more often. Microstimulation in IT also accelerated the monkeys' choice for the preferred structure, while delaying choices corresponding to the nonpreferred structure of a given site. These findings reveal that 3D-structure-selective neurons in IT contribute to the categorization of 3D objects.

Effect of feature-selective attention on neuronal responses in macaque area MT

Attention influences visual processing in striate and extrastriate cortex, which has been extensively studied for spatial-, object-, and feature-based attention. Most studies exploring neural signatures of feature-based attention have trained animals to attend to an object identified by a certain feature and ignore objects/displays identified by a different feature. Little is known about the effects of feature-selective attention, where subjects attend to one stimulus feature domain (e.g., color) of an object while features from different domains (e.g., direction of motion) of the same object are ignored. To study this type of feature-selective attention in area MT in the middle temporal sulcus, we trained macaque monkeys to either attend to and report the direction of motion of a moving sine wave grating (a feature for which MT neurons display strong selectivity) or attend to and report its color (a feature for which MT neurons have very limited selectivity). We hypothesized that neurons would upregulate their firing rate during attend-direction conditions compared with attend-color conditions. We found that feature-selective attention significantly affected 22% of MT neurons. Contrary to our hypothesis, these neurons did not necessarily increase firing rate when animals attended to direction of motion but fell into one of two classes. In one class, attention to color increased the gain of stimulus-induced responses compared with attend-direction conditions. The other class displayed the opposite effects. Feature-selective activity modulations occurred earlier in neurons modulated by attention to color compared with neurons modulated by attention to motion direction. Thus feature-selective attention influences neuronal processing in macaque area MT but often exhibited a mismatch between the preferred stimulus dimension (direction of motion) and the preferred attention dimension (attention to color).

Cortical and subcortical connections of V1 and V2 in early postnatal macaque monkeys

Connections of primary (V1) and secondary (V2) visual areas were revealed in macaque monkeys ranging in age from 2 to 16 weeks by injecting small amounts of cholera toxin subunit B (CTB). Cortex was flattened and cut parallel to the surface to reveal injection sites, patterns of labeled cells, and patterns of cytochrome oxidase (CO) staining. Projections from the lateral geniculate nucleus and pulvinar to V1 were present at 4 weeks of age, as were pulvinar projections to thin and thick CO stripes in V2. Injections into V1 in 4- and 8-week-old monkeys labeled neurons in V2, V3, middle temporal area (MT), and dorsolateral area (DL)/V4. Within V1 and V2, labeled neurons were densely distributed around the injection sites, but formed patches at distances away from injection sites. Injections into V2 labeled neurons in V1, V3, DL/V4, and MT of monkeys 2-, 4-, and 8-weeks of age. Injections in thin stripes of V2 preferentially labeled neurons in other V2 thin stripes and neurons in the CO blob regions of V1. A likely thick stripe injection in V2 at 4 weeks of age labeled neurons around blobs. Most labeled neurons in V1 were in superficial cortical layers after V2 injections, and in deep layers of other areas. Although these features of adult V1 and V2 connectivity were in place as early as 2 postnatal weeks, labeled cells in V1 and V2 became more restricted to preferred CO compartments after 2 weeks of age.

Multifocal Attention Filters Targets from Distracters within and beyond Primate MT Neurons' Receptive Field Boundaries

Visual attention has been classically described as a spotlight that enhances the processing of a behaviorally relevant object. However, in many situations, humans and animals must simultaneously attend to several relevant objects separated by distracters. To account for this ability, various models of attention have been proposed including splitting of the attentional spotlight into multiple foci, zooming of the spotlight over a region of space, and switching of the spotlight among objects. We investigated this controversial issue by recording neuronal activity in visual area MT of two macaques while they attended to two translating objects that circumvented a third distracter object located inside the neurons' receptive field. We found that when the attended objects passed through or nearby the receptive field, neuronal responses to the distracter were either decreased or remained unaltered. These results demonstrate that attention can split into multiple spotlights corresponding to relevant objects while filtering out interspersed distracters.

Dissociation of Neuronal and Psychophysical Responses to Local and Global Motion

Most neurons in cortical area MT (V5) are strongly direction selective, and their activity is closely associated with the perception of visual motion. These neurons have large receptive fields built by combining inputs with smaller receptive fields that respond to local motion. Humans integrate motion over large areas and can perceive what has been referred to as global motion. The large size and direction selectivity of MT receptive fields suggests that MT neurons may represent global motion. We have explored this possibility by measuring responses to a stimulus in which the directions of simultaneously presented local and global motion are independently controlled. Surprisingly, MT responses depended only on the local motion and were unaffected by the global motion. Yet, under similar conditions, human observers perceive global motion and are impaired in discriminating local motion. Although local motion perception might depend on MT signals, global motion perception depends on mechanisms qualitatively different from those in MT. Motion perception therefore does not depend on a single cortical area but reflects the action and interaction of multiple brain systems.

Mechanisms of Selective Attention: Response Enhancement, Noise Reduction, and Efficient Pooling of Sensory Responses

In this issue of Neuron, Pestilli and coworkers provide evidence that response gain and noise reduction are insufficient to account for attention-induced changes in perception. Instead, selection may critically depend on the biased pooling of sensory signals during decision making.

Visual motion integration by neurons in the middle temporal area of a New World monkey, the marmoset

The middle temporal area (MT/V5) is an anatomically distinct region of primate visual cortex that is specialized for the processing of image motion. It is generally thought that some neurons in area MT are capable of signalling the motion of complex patterns, but this has only been established in the macaque monkey. We made extracellular recordings from single units in area MT of anaesthetized marmosets, a New World monkey. We show through quantitative analyses that some neurons (35 of 185; 19%) are capable of signalling pattern motion ('pattern cells'). Across several dimensions, the visual response of pattern cells in marmosets is indistinguishable from that of pattern cells in macaques. Other neurons respond to the motion of oriented contours in a pattern ('component cells') or show intermediate properties. In addition, we encountered a subset of neurons (22 of 185; 12%) insensitive to sinusoidal gratings but very responsive to plaids and other two-dimensional patterns and otherwise indistinguishable from pattern cells. We compared the response of each cell class to drifting gratings and dot fields. In pattern cells, directional selectivity was similar for gratings and dot fields; in component cells, directional selectivity was weaker for dot fields than gratings. Pattern cells were more likely to have stronger suppressive surrounds, prefer lower spatial frequencies and prefer higher speeds than component cells. We conclude that pattern motion sensitivity is a feature of some neurons in area MT of both New and Old World monkeys, suggesting that this functional property is an important stage in motion analysis and is likely to be conserved in humans.

Representation of Perceptually Invisible Image Motion in Extrastriate Visual Area MT of Macaque Monkeys

Why does the world appear stable despite the visual motion induced by eye movements during fixation? We find that the answer must reside in how visual motion signals are interpreted by perception, because MT neurons in monkeys respond to the image motion caused by eye drifts in the presence of a stationary stimulus. Several features suggest a visual origin for the responses of MT neurons during fixation: spike-triggered averaging yields a peak image velocity in the preferred direction that precedes spikes by ∼60 ms; image velocity during fixation and firing rate show similar peaks in power at 4-5 Hz; and average MT firing during a period of fixation is related monotonically to the image speed along the preferred axis of the neurons 60 ms earlier. The percept caused by the responses of MT neurons during fixation depends on the distribution of activity across the population of neurons of different preferred speeds. For imposed stimulus motion, the population response peaks for neurons that prefer the actual target speed. For small image motions caused by eye drifts during fixation, the population response is large, but is noisy and does not show a clear peak. This representation of image motion in MT would be ignored if perception interprets the population response in the context of a prior of zero speed. Then, we would see a stable scene despite MT responses caused by eye drifts during fixation.

Expansion of MT Neurons Excitatory Receptive Fields during Covert Attentive Tracking

Primates can attentively track moving objects while keeping gaze stationary. The neural mechanisms underlying this ability are poorly understood. We investigated this issue by recording responses of neurons in area MT of two rhesus monkeys while they performed two different tasks. During the Attend-Fixation task, two moving random dot patterns (RDPs) translated across a screen at the same speed and in the same direction while the animals directed gaze to a fixation spot and detected a change in its luminance. During the Tracking task, the animals kept gaze on the fixation spot and attentively tracked the two RDPs to report a change in the local speed of one of the patterns' dots. In both conditions, neuronal responses progressively increased as the RDPs entered the neurons' receptive field (RF), peaked when they reached its center, and decreased as they translated away. This response profile was well described by a Gaussian function with its center of gravity indicating the RF center and its flanks the RF excitatory borders. During Tracking, responses were increased relative to Attend-Fixation, causing the Gaussian profiles to expand. Such increases were proportionally larger in the RF periphery than at its center, and were accompanied by a decrease in the trial-to-trial response variability (Fano factor) relative to Attend-Fixation. These changes resulted in an increase in the neurons' performance at detecting targets at longer distances from the RF center. Our results show that attentive tracking dynamically changes MT neurons' RF profiles, ultimately improving the neurons' ability to encode the tracked stimulus features.

A Three-Dimensional Spatiotemporal Receptive Field Model Explains Responses of Area MT Neurons to Naturalistic Movies

Area MT has been an important target for studies of motion processing. However, previous neurophysiological studies of MT have used simple stimuli that do not contain many of the motion signals that occur during natural vision. In this study we sought to determine whether views of area MT neurons developed using simple stimuli can account for MT responses under more naturalistic conditions. We recorded responses from macaque area MT neurons during stimulation with naturalistic movies. We then used a quantitative modeling framework to discover which specific mechanisms best predict neuronal responses under these challenging conditions. We find that the simplest model that accurately predicts responses of MT neurons consists of a bank of V1-like filters, each followed by a compressive nonlinearity, a divisive nonlinearity, and linear pooling. Inspection of the fit models shows that the excitatory receptive fields of MT neurons tend to lie on a single plane within the three-dimensional spatiotemporal frequency domain, and suppressive receptive fields lie off this plane. However, most excitatory receptive fields form a partial ring in the plane and avoid low temporal frequencies. This receptive field organization ensures that most MT neurons are tuned for velocity but do not tend to respond to ambiguous static textures that are aligned with the direction of motion. In sum, MT responses to naturalistic movies are largely consistent with predictions based on simple stimuli. However, models fit using naturalistic stimuli reveal several novel properties of MT receptive fields that had not been shown in prior experiments.

Decoding the motion aftereffect in human visual cortex

Abstract In the motion aftereffect (MAE), adapting to a moving stimulus causes a subsequently presented stationary stimulus to appear to move in the opposite direction. Recently, the neural basis of the motion aftereffect has received considerable interest, and a number of brain areas have been implicated in the generation of the illusory motion. Here, we use functional magnetic resonance imaging in combination with multivariate pattern classification to directly compare the neural activity evoked during the observation of both real and illusory motions. We show that the perceived illusory motion is not encoded in the same way as real motion in the same direction. Instead, suppression of the adapted direction of motion results in a shift of the population response of motion sensitive neurons in area MT +, resulting in activation patterns that are in fact more similar to real motion in orthogonal, rather than opposite directions. Although robust motion selectivity was observed in visual areas V1, V2, V3, and V4, this MAE-specific modulation of the population response was only observed in area MT +. Implications for our understanding of the motion aftereffect, and models of motion perception in general, are discussed.

Receptive Field Positions in Area MT during Slow Eye Movements

Perceptual stability requires the integration of information across eye movements. We first tested the hypothesis that motion signals are integrated by neurons whose receptive fields (RFs) do not move with the eye but stay fixed in the world. Specifically, we measured the RF properties of neurons in the middle temporal area (MT) of macaques (Macaca mulatta) during the slow phase of optokinetic nystagmus. Using a novel method to estimate RF locations for both spikes and local field potentials, we found that the location on the retina that changed spike rates or local field potentials did not change with eye position; RFs moved with the eye. Second, we tested the hypothesis that neurons link information across eye positions by remapping the retinal location of their RFs to future locations. To test this, we compared RF locations during leftward and rightward slow phases of optokinetic nystagmus. We found no evidence for remapping during slow eye movements; the RF location was not affected by eye-movement direction. Together, our results show that RFs of MT neurons and the aggregate activity reflected in local field potentials are yoked to the eye during slow eye movements. This implies that individual MT neurons do not integrate sensory information from a single position in the world across eye movements. Future research will have to determine whether such integration, and the construction of perceptual stability, takes place in the form of a distributed population code in eye-centered visual cortex or is deferred to downstream areas.

Effects of Stimulus Direction on the Correlation between Behavior and Single Units in Area MT during a Motion Detection Task

Trial-to-trial variations in the firing rates of neurons in the middle temporal visual area (MT) are correlated with the behavior of macaque monkeys performing motion detection and motion discrimination tasks. Here we examine how these correlations depend on the direction of motion used for a detection task relative to the preferred direction of the neuron under study. There was a robust correlation between the firing rate of MT neurons and the animal's detection of motion when the direction of that motion was within ∼ 45° of the preferred direction of the neuron. This correlation was undetectable using motions that were ∼ 90° away from the preferred direction, and an inverse correlation between activity and behavior was found for motion in the null direction. Correlation between reaction times and single-cell activity in MT followed a similar pattern. Although motion detection could have been based solely on the activity of neurons preferring the expected direction, these results suggest that it depends on the relative activity of neurons preferring opposite directions of motion. They furthermore show that the subset of neurons used to guide behavior can vary from trial to trial based on task requirements.

Illusory Centrifugal Motion Direction Observed in Brief Stimuli: Psychophysics and Energy Model

All stationary stimuli of fixed duration have motion energy and the amount of motion energy increases with decreasing duration. Consequently, perception of motion direction could be biased if the readout mechanisms are unbalanced. Previous physiological study showed prefered direction of MT neurons in peripheral tend to be oriented away from fovea(Albright, 1989). Given the broadening of motion energy in brief stimuli, such effect should increase as the stimulus duration decreases. Here, we tested this hypothesis by presenting vertical gratings (0.5c/deg, raised cosine spatial envelope, radius = 5deg, 98% contrast) with different speeds(2,4,8 16deg/sec) and direction(moving towards fovea or moving away from fovea). And Stimuli were presented in a temporal Gaussian envelope with durations ranging between 5 and 500ms. Observers' task was to identify perceived motion direction (guessing when unsure). Results showed that as predicted, the observers were biased to perceive these stimuli as moving away from fovea. In summary, briefly presented stationary stimuli are perceived as moving in centrifugal direction when presented in visual periphery. One possible explanation for this illusion is that these stimuli, by virtue of their broad temporal frequency spectrum, stimulate centrifugally biased motion mechanisms in area MT.

Contributions of Indirect Pathways to Visual Response Properties in Macaque Middle Temporal Area MT

The primate visual cortex exhibits a remarkable degree of interconnectivity. Each visual area receives an average of 10 to 15 inputs, many of them from cortical areas with overlapping, but not identical, functional properties. In this study, we assessed the functional significance of this anatomical parallelism to the middle temporal area (MT) of the macaque visual cortex. MT receives major feedforward inputs from areas V1, V2, and V3, but little is known about the properties of each of these pathways. We previously demonstrated that reversible inactivation of V2 and V3 causes a disproportionate degradation of tuning for binocular disparity of MT neurons, relative to direction tuning (Ponce et al., 2008). Here we show that MT neurons continued to encode speed and size information during V2/3 inactivation; however, many became significantly less responsive to fast speeds and others showed a modest decrease in surround suppression. These changes resemble previously reported effects of reducing stimulus contrast (Pack et al., 2005; Krekelberg et al., 2006), but we show here that they differ in their temporal dynamics. We find no evidence that the indirect pathways selectively target different functional regions within MT. Overall, our findings suggest that the indirect pathways to MT primarily convey modality-specific information on binocular disparity, but that they also contribute to the processing of stimuli moving at fast speeds.

Modeling short-term adaptation processes of visual motion detectors

In the brain, both neural processing dynamics as well as the perceptual interpretation of a stimulus can depend on sensory history. The underlying principle is a sensory adaptation to the statistics of the input collected over some timespan, allowing the system to tune its detectors, e.g. by better sampling the input space and adjusting the response. Here, we show how a model for adaptation in visual motion processing can be set up from first principles using a generative formulation and casting the problem of adaptation in terms of optimal estimation over time. The model leads to an online adaptation of velocity tuning curves, inducing shifts in the velocity tuning and changes in the tuning curve widths that are compatible with observations from physiological experiments on macaque MT neurons. We also show how such an adaptation leads to a greater computational efficiency by a better sampling of the velocity space, requiring less motion detectors to achieve a desired level of estimation accuracy.

Spatial non-homogeneity of the antagonistic surround in motion perception

At high contrast, duration thresholds for motion direction discrimination deteriorate with increasing stimulus size. This counterintuitive result has been explained by the center-surround antagonism present in the neurons of visual area MT. Conversely, at very low contrast, direction discrimination improves with increasing size, a result that has been explained by spatial summation. In this investigation, we study the effects of stimulus shape and contrast on center-surround antagonism. Using adaptive Bayesian staircases, we measured duration thresholds of 5 subjects for vertically oriented Gabor patches of 1 cycle/deg with two types of oval Gaussian windows, one vertically elongated (Sx = 0.35, Sy = 2.5 deg) and other horizontally elongated (Sx = 2.5, Sy = 0.35 deg) moving rightward or leftward at a speed of 2 deg/s. We found that at high contrast (92%) duration thresholds were lower for vertically than horizontally elongated windows. However, at low contrast (2.8%), we found that duration thresholds were lower for horizontally than vertically elongated windows. These asymmetric results mirror the spatial non-homogeneity of the antagonistic surround found in MT neurons and suggest that the underlying center-surround antagonism is stronger along the direction of motion.