Neural mechanisms of tactile motion integration in somatosensory cortex

How are local motion signals integrated to form a global motion percept? We investigate the neural mechanisms of tactile motion integration by presenting tactile gratings and plaids to the fingertips of monkeys, using the tactile analogue of a visual monitor and recording the responses evoked in somatosensory cortical neurons. The perceived directions of the gratings and plaids are measured in parallel psychophysical experiments. We identify a population of somatosensory neurons that exhibit integration properties comparable to those induced by analogous visual stimuli in area MT and find that these neural responses account for the perceived direction of the stimuli across all stimulus conditions tested. The preferred direction of the neurons and the perceived direction of the stimuli can be predicted from the weighted average of the directions of the individual stimulus features, highlighting that the somatosensory system implements a vector average mechanism to compute tactile motion direction that bears striking similarities to its visual counterpart.     

Mathematical model for self-organization of direction columns in the primate middle temporal area

We attempted to reproduce modular structures for direction selectivity characteristic of the primate middle temporal area (MT) based on our thermodynamic model for the activity-dependent self-organization of neural networks. We assumed that excitatory afferent input to MT neurons arises from V1 and/or V2 neurons which are selective to both orientation of a visual stimulus and direction of its motion, and that such input is modifiable and becomes selectively connected through the process of self-organization. By contrast, local circuit connections within MT are unmodifiable and remain nonselectively connected (isotropic). The present simulations reproduced characteristic patterns of organization in the cortex of MT in that: (1) preferred directions of the afferent input gradually shifted, except for singularity lines where direction abruptly changed by 180°; (2) model MT neurons located between the singularity lines responded to unidirectionally moving stimuli, closely reflecting preferred direction of the afferent input; (3) neurons responding to stimuli moving in two opposite directions were located along the singularity lines; and (4) neurons responding to stimuli moving in any direction were clustered at the ends of the singularity lines. When the strength of the lateral inhibition was decreased, direction selectivity of MT neurons was reduced. Therefore, the lateral inhibition, even if isotropic, strengthens the direction selectivity of MT neurons. Expression of singularities changed depending on a parameter that represents the relative dominance of the direction selectivity to the orientation selectivity of the afferent input. When the direction selectivity was predominant, singularity points were formed, while when the orientation selectivity prevailed, the MT was covered by two-dimensional singularity networks. Line singularities similar to those experimentally observed were reproduced when these two types of selectivity were in balance. Received: 15 October 1992/Accepted in revised form: 27 June 1993     

Feature-based attention increases the selectivity of population responses in primate visual cortex

BACKGROUND: Attending to the spatial location or to nonspatial features of visual stimuli can modulate neuronal responses in primate visual cortex. The modulation by spatial attention changes the gain of sensory neurons and strengthens the representation of attended locations without changing neuronal selectivities such as directionality, i.e., the ratio of responses to preferred and anti-preferred directions of motion. Whether feature-based attention acts in a similar manner is unknown. RESULTS: To clarify this issue, we recorded the responses of 135 direction-selective neurons in the middle temporal area (MT) of two macaques to an unattended moving random dot pattern (the distractor) positioned inside a neuron's receptive field while the animals attended to a second moving pattern positioned in the opposite hemifield. Responses to different directions of the distractor were modulated by the same factor (approximately 12%) as long as the attended direction remained unchanged. On the other hand, systematically changing the attended direction from a neuron's preferred to its anti-preferred direction caused a systematic change of the attentional modulation from an enhancement to a suppression, increasing directionality by about 20%. CONCLUSIONS: The results show that (1) feature-based attention exerts a multiplicative modulation upon neuronal responses and that the strength of this modulation depends on the similarity between the attended feature and the cell's preferred feature, in line with the feature-similarity gain model, and (2) at the level of the neuronal population, feature-based attention increases the selectivity for attended features by increasing the responses of neurons preferring this feature value while decreasing responses of neurons tuned to the opposite feature value.     

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

To track a moving object, its motion must first be distinguished from that of the background. The center-surround properties of neurons in the middle temporal visual area (MT) may be important for signaling the relative motion between object and background. To test this, we microstimulated within MT and measured the effects on monkeys' eye movements to moving targets. We found that stimulation at "local motion" sites, where receptive fields possessed antagonistic surrounds, shifted pursuit in the preferred direction of the neurons, whereas stimulation at "wide-field motion" sites shifted pursuit in the opposite, or null, direction. We propose that activating wide-field sites simulated background motion, thus inducing a target motion signal in the opposite direction. Our results support the hypothesis that neuronal center-surround mechanisms contribute to the behavioral segregation of objects from the background.     

‘Vector white noise’: a technique for mapping the motion receptive fields of direction-selective visual neurons

A technique is described and tested for mapping the sensitivities and preferred directions of motion at different locations within the receptive fields of direction-selective motion-detecting visual neurons. The procedure is to record the responses to a number of visual stimuli, each stimulus presentation consisting of a set of short, randomly-oriented, moving bars arranged in a square grid. Each bar moves perpendicularly to its long axis. The vector describing the sensitivity and preferred direction of motion at each grid location is obtained as a sum of the unit vectors defining the directions of motion of the bars in each of the stimuli at that location, weighted by the strengths of the corresponding responses. The resulting vector field specifies the optimum flow field for the neuron. The advantage of this technique over the conventional approach of probing the receptive field sequentially at each grid location is that the parallel nature of the stimulus is sensitive to nonlinear interactions (such as shunting inhibition for mutual facilitation) between different regions of the visual field. The technique is used to determine accurately the motion receptive fields of direction-selective motion detecting neurons in the optic lobes of insects. It is potentially applicable to motion-sensitive neurons with highly structured receptive fields, such as those in the optic tectum of the pigeon or in area MST of the monkey.     

Neural Mechanisms of Cortical Motion Computation Based on a Neuromorphic Sensory System

The visual cortex analyzes motion information along hierarchically arranged visual areas that interact through bidirectional interconnections. This work suggests a bio-inspired visual model focusing on the interactions of the cortical areas in which a new mechanism of feedforward and feedback processing are introduced. The model uses a neuromorphic vision sensor (silicon retina) that simulates the spike-generation functionality of the biological retina. Our model takes into account two main model visual areas, namely V1 and MT, with different feature selectivities. The initial motion is estimated in model area V1 using spatiotemporal filters to locally detect the direction of motion. Here, we adapt the filtering scheme originally suggested by Adelson and Bergen to make it consistent with the spike representation of the DVS. The responses of area V1 are weighted and pooled by area MT cells which are selective to different velocities, i.e. direction and speed. Such feature selectivity is here derived from compositions of activities in the spatio-temporal domain and integrating over larger space-time regions (receptive fields). In order to account for the bidirectional coupling of cortical areas we match properties of the feature selectivity in both areas for feedback processing. For such linkage we integrate the responses over different speeds along a particular preferred direction. Normalization of activities is carried out over the spatial as well as the feature domains to balance the activities of individual neurons in model areas V1 and MT. Our model was tested using different stimuli that moved in different directions. The results reveal that the error margin between the estimated motion and synthetic ground truth is decreased in area MT comparing with the initial estimation of area V1. In addition, the modulated V1 cell activations shows an enhancement of the initial motion estimation that is steered by feedback signals from MT cells.     

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.     

Color signals in area MT of the macaque monkey

The relationship between the neural processing of color and motion information has been a contentious issue in visual neuroscience. We examined this relationship directly by measuring neural responses to isoluminant S cone signals in extrastriate area MT of the macaque monkey. S cone stimuli produced robust, direction-selective responses at most recording sites, indicating that color signals are present in MT. While these responses were unequivocal, S cone contrast sensitivity was, on average, 1.0-1.3 log units lower than luminance contrast sensitivity. The presence of S cone responses and the relative sensitivity of MT neurons to S cone and luminance signals agree with functional magnetic resonance imaging (fMRI) measurements in human MT+. The results are consistent with the hypothesis that color signals in MT influence behavior in speed judgment tasks.     

Directional anisotropies reveal a functional segregation of visual motion processing for perception and action

Human exhibits an anisotropy in direction perception: discrimination is superior when motion is around horizontal or vertical rather than diagonal axes. In contrast to the consistent directional anisotropy in perception, we found only small idiosyncratic anisotropies in smooth pursuit eye movements, a motor action requiring accurate discrimination of visual motion direction. Both pursuit and perceptual direction discrimination rely on signals from the middle temporal visual area (MT), yet analysis of multiple measures of MT neuronal responses in the macaque failed to provide evidence of a directional anisotropy. We conclude that MT represents different motion directions uniformly, and subsequent processing creates a directional anisotropy in pathways unique to perception. Our data support the hypothesis that, at least for visual motion, perception and action are guided by inputs from separate sensory streams. The directional anisotropy of perception appears to originate after the two streams have segregated and downstream from area MT.     

A Network Model of Motion Processing in Area MT of Primates

A simple and biologically plausible model is proposed to simulatethe visual motion processing taking place in the middle temporal (MT) areaof the visual cortex in the primate brain. The model is ahierarchical neural network composed of multiple competitive learninglayers. The input layer of the network simulates the neurons in the primaryvisual cortex (V1), which are sensitive to the orientation and motionvelocity of the visual stimuli, and the middle and output layers of thenetwork simulate the component MT and pattern MT neurons, which areselectively responsive to local and global motions, respectively. Thenetwork model was tested with various simulated motion patterns (random dotsof different direction correlations, transparent motion, grating and plaidpatterns, and so on). The response properties of the model closely resemblemany of the known features of the MT neurons found neurophysiologically.These results show that the sophisticated response behaviors of the MTneurons can emerge naturally from some very simple models, such as acompetitive learning network.     

Direct evidence for encoding of motion streaks in human visual cortex

Temporal integration in the visual system causes fast-moving objects to generate static, oriented traces (‘motion streaks’), which could be used to help judge direction of motion. While human psychophysics and single-unit studies in non-human primates are consistent with this hypothesis, direct neural evidence from the human cortex is still lacking. First, we provide psychophysical evidence that faster and slower motions are processed by distinct neural mechanisms: faster motion raised human perceptual thresholds for static orientations parallel to the direction of motion, whereas slower motion raised thresholds for orthogonal orientations. We then used functional magnetic resonance imaging to measure brain activity while human observers viewed either fast (‘streaky’) or slow random dot stimuli moving in different directions, or corresponding static-oriented stimuli. We found that local spatial patterns of brain activity in early retinotopic visual cortex reliably distinguished between static orientations. Critically, a multivariate pattern classifier trained on brain activity evoked by these static stimuli could then successfully distinguish the direction of fast (‘streaky’) but not slow motion. Thus, signals encoding static-oriented streak information are present in human early visual cortex when viewing fast motion. These experiments show that motion streaks are present in the human visual system for faster motion.     

A multilayer neural network model for perception of rotational motion

A multilayer neural nerwork model for the perception of rotational motion has been developed usingReichardt's motion detector array of correlation type, Kohonen's self-organized feature map and Schuster-Wagner's oscillating neural network. It is shown that the unsupervised learning could make the neurons on the second layer of the network tend to be self-organized in a form resembling columnar organization of selective directions in area MT of the primate's visual cortex. The output layer can interpret rotation information and give the directions and velocities of rotational motion. The computer simulation results are in agreement with some psychophysical observations of rotation-al perception. It is demonstrated that the temporal correlation between the oscillating neurons would be powerful for solving the "binding problem" of shear components of rotational motion.     

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.     

Responses of tectal neurons to contrasting stimuli: an electrophysiological study in the barn owl

The saliency of visual objects is based on the center to background contrast. Particularly objects differing in one feature from the background may be perceived as more salient. It is not clear to what extent this so called "pop-out" effect observed in humans and primates governs saliency perception in non-primates as well. In this study we searched for neural-correlates of pop-out perception in neurons located in the optic tectum of the barn owl. We measured the responses of tectal neurons to stimuli appearing within the visual receptive field, embedded in a large array of additional stimuli (the background). Responses were compared between contrasting and uniform conditions. In a contrasting condition the center was different from the background while in the uniform condition it was identical to the background. Most tectal neurons responded better to stimuli in the contrsating condition compared to the uniform condition when the contrast between center and background was the direction of motion but not when it was the orientation of a bar. Tectal neurons also preferred contrasting over uniform stimuli when the center was looming and the background receding but not when the center was receding and the background looming. Therefore, our results do not support the hypothesis that tectal neurons are sensitive to pop-out per-se. The specific sensitivity to the motion contrasting stimulus is consistent with the idea that object motion and not large field motion (e.g., self-induced motion) is coded in the neural responses of tectal neurons.     

Context-dependent changes in functional circuitry in visual area MT

Animals can flexibly change their behavior in response to a particular sensory stimulus; the mapping between sensory and motor representations in the brain must therefore be flexible as well. Changes in the correlated firing of pairs of neurons may provide a metric of changes in functional circuitry during behavior. We studied dynamic changes in functional circuitry by analyzing the noise correlations of simultaneously recorded MT neurons in two behavioral contexts: one that promotes cooperative interactions between the two neurons and another that promotes competitive interactions. We found that identical visual stimuli give rise to differences in noise correlation in the two contexts, suggesting that MT neurons receive inputs of central origin whose strength changes with the task structure. The data are consistent with a mixed feature-based attentional strategy model in which the animal sometimes alternates attention between opposite directions of motion and sometimes attends to the two directions simultaneously.     

Testing Neuronal Accounts of Anisotropic Motion Perception with Computational Modelling

There is an over-representation of neurons in early visual cortical areas that respond most strongly to cardinal (horizontal and vertical) orientations and directions of visual stimuli, and cardinal- and oblique-preferring neurons are reported to have different tuning curves. Collectively, these neuronal anisotropies can explain two commonly-reported phenomena of motion perception – the oblique effect and reference repulsion – but it remains unclear whether neuronal anisotropies can simultaneously account for both perceptual effects. We show in psychophysical experiments that reference repulsion and the oblique effect do not depend on the duration of a moving stimulus, and that brief adaptation to a single direction simultaneously causes a reference repulsion in the orientation domain, and the inverse of the oblique effect in the direction domain. We attempted to link these results to underlying neuronal anisotropies by implementing a large family of neuronal decoding models with parametrically varied levels of anisotropy in neuronal direction-tuning preferences, tuning bandwidths and spiking rates. Surprisingly, no model instantiation was able to satisfactorily explain our perceptual data. We argue that the oblique effect arises from the anisotropic distribution of preferred directions evident in V1 and MT, but that reference repulsion occurs separately, perhaps reflecting a process of categorisation occurring in higher-order cortical areas.     

Tuning Properties of MT and MSTd and Divisive Interactions for Eye-Movement Compensation

The primate brain intelligently processes visual information from the world as the eyes move constantly. The brain must take into account visual motion induced by eye movements, so that visual information about the outside world can be recovered. Certain neurons in the dorsal part of monkey medial superior temporal area (MSTd) play an important role in integrating information about eye movements and visual motion. When a monkey tracks a moving target with its eyes, these neurons respond to visual motion as well as to smooth pursuit eye movements. Furthermore, the responses of some MSTd neurons to the motion of objects in the world are very similar during pursuit and during fixation, even though the visual information on the retina is altered by the pursuit eye movement. We call these neurons compensatory pursuit neurons. In this study we develop a computational model of MSTd compensatory pursuit neurons based on physiological data from single unit studies. Our model MSTd neurons can simulate the velocity tuning of monkey MSTd neurons. The model MSTd neurons also show the pursuit compensation property. We find that pursuit compensation can be achieved by divisive interaction between signals coding eye movements and signals coding visual motion. The model generates two implications that can be tested in future experiments: (1) compensatory pursuit neurons in MSTd should have the same direction preference for pursuit and retinal visual motion; (2) there should be non-compensatory pursuit neurons that show opposite preferred directions of pursuit and retinal visual motion.     

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.     

Shape Invariant Coding of Motion Direction in Somatosensory Cortex

Invariant representations of stimulus features are thought to play an important role in producing stable percepts of objects. In the present study, we assess the invariance of neural representations of tactile motion direction with respect to other stimulus properties. To this end, we record the responses evoked in individual neurons in somatosensory cortex of primates, including areas 3b, 1, and 2, by three types of motion stimuli, namely scanned bars and dot patterns, and random dot displays, presented to the fingertips of macaque monkeys. We identify a population of neurons in area 1 that is highly sensitive to the direction of stimulus motion and whose motion signals are invariant across stimulus types and conditions. The motion signals conveyed by individual neurons in area 1 can account for the ability of human observers to discriminate the direction of motion of these stimuli, as measured in paired psychophysical experiments. We conclude that area 1 contains a robust representation of motion and discuss similarities in the neural mechanisms of visual and tactile motion processing.     

Representation of moving stimuli by somatosensory neurons.

The findings obtained in neurophysiological and psychophysical investigations using tactile stimuli that move at constant velocity across the skin are reviewed. For certain neurons in the postcentral gyrus of the cerebral cortex (S-I) of macaque monkeys, direction of stimulus motion is a "trigger feature" i.e., moving tactile stimuli evoke vigorous discharge activity in these neurons only if the stimuli are moved in a particular direction across the receptive field. This directional selectivity is maximal when stimulus velocity is between 5 and 50 cm/sec, and falls off rapidly at lower or higher velocities. The capacity for human subjects to correctly identify the direction of stimulus motion on the skin exhibits a similar dependence on stimulus velocity. The similar effects of velocity on neural and psychophysical measures of directional sensitivity support the idea that direction of stimulus motion on the skin can only be recognized if the moving stimulus optimally activates the group of S-I neurons for which that directions of simulus motion is the trigger feature.