Segregation of global and local motion processing in primate middle temporal visual area.

The early stages of primate visual processing appear to be divided up into several component parts so that, for example, colour, form and motion are analysed by anatomically distinct streams. We have found that further subspecialization occurs within the motion processing stream. Neurons representing two different kinds of information about visual motion are segregated in columnar fashion within the middle temporal area of the owl monkey. These columns can be distinguished by labelling with 2-deoxyglucose in response to large-field random-dot patterns. Neurons in lightly labelled interbands have receptive fields with antagonistic surrounds: the response to a centrally placed moving stimulus is suppressed by motion in the surround. Neurons in more densely labelled bands have surrounds that reinforce the centre response so that they integrate motion cues over large areas of the visual field. Interband cells carry information about local motion contrast that may be used to detect motion boundaries or to indicate retinal slip during visual tracking. Band cells encode information about global motion that might be useful for orienting the animal in its environment.     

Motion streaks provide a spatial code for motion direction.

Although many neurons in the primary visual cortex (V1) of primates are direction selective, they provide ambiguous information about the direction of motion of a stimulus. There is evidence that one of the ways in which the visual system resolves this ambiguity is by computing, from the responses of V1 neurons, velocity components in two or more spatial orientations and then combining these velocity components. Here I consider another potential neural mechanism for determining motion direction. When a localized image feature moves fast enough, it should become smeared in space owing to temporal integration in the visual system, creating a spatial signal-a 'motion streak'-oriented in the direction of the motion. The orientation masking and adaptation experiments reported here show that these spatial signals for motion direction exist in the human visual system for feature speeds above about 1 feature width per 100 ms. Computer simulations show that this psychophysical finding is consistent with the known response properties of V1 neurons, and that these spatial signals, when appropriately processed, are sufficient to determine motion direction in natural images.     

Parallel processing of motion and colour information

When the two eyes are confronted with sufficiently different versions of the visual environment, one or the other eye dominates perception in alternation. A similar situation may be created in the laboratory by presenting images to the left and right eyes which differ in orientation or colour. Although perception is dominated by one eye during rivalry, there are a number of instances in which visual processes nevertheless continue to integrate information from the suppressed eye. For example the interocular transfer of the motion after-effect is undiminished when induced during binocular rivalry. Thus motion information processing may occur in parallel with the rivalry process. Here we describe a novel example in which the visual system simultaneously exhibits binocular rivalry and vision that integrates signals from both eyes. This apparent contradiction is resolved by postulating parallel visual processes devoted to the analyses of colour and motion information. Counterphased gratings are viewed dichoptically such that for one eye the grating is composed of alternating yellow and black stripes (luminance) while for the other it is composed of alternating red and green stripes (chrominance). When the gratings are fused, a moving grating is perceived. A consistent direction of motion can only be achieved if left and right monocular signals are integrated by the nervous system. Yet the apparent colour of the binocular percept alternates between red-green and yellow-black. These observations demonstrate the segregation of processing by the early motion system from that affording the perception of colour. Although, in this stimulus, colour information in itself can play no part in the cyclopean perception of motion direction, colour is carried along perceptually (filled in) by the moving pattern which is integrated from both eyes.     

Gaze direction controls response gain in primary visual-cortex neurons

To localize objects in space, the brain needs to combine information about the position of the stimulus on the retinae with information about the location of the eyes in their orbits. Interaction between these two types of information occurs in several cortical areas, but the role of the primary visual cortex (area V1) in this process has remained unclear. Here we show that, for half the cells recorded in area V1 of behaving monkeys, the classically described visual responses are strongly modulated by gaze direction. Specifically, we find that selectivity for horizontal retinal disparity-the difference in the position of a stimulus on each retina which relates to relative object distance-and for stimulus orientation may be present at a given gaze direction, but be absent or poorly expressed at another direction. Shifts in preferred disparity also occurred in several neurons. These neural changes were most often present at the beginning of the visual response, suggesting a feedforward gain control by eye position signals. Cortical neural processes for encoding information about the three-dimensional position of a stimulus in space therefore start as early as area V1.     

Hearing visual motion in depth

Auditory spatial perception is strongly affected by visual cues. For example, if auditory and visual stimuli are presented synchronously but from different positions, the auditory event is mislocated towards the locus of the visual stimulus-the ventriloquism effect. This 'visual capture' also occurs in motion perception in which a static auditory stimulus appears to move with the visual moving object. We investigated how the human perceptual system coordinates complementary inputs from auditory and visual senses. Here we show that an auditory aftereffect occurs from adaptation to visual motion in depth. After a few minutes of viewing a square moving in depth, a steady sound was perceived as changing loudness in the opposite direction. Adaptation to a combination of auditory and visual stimuli changing in a compatible direction increased the aftereffect and the effect of visual adaptation almost disappeared when the directions were opposite. On the other hand, listening to a sound changing in intensity did not affect the visual changing-size aftereffect. The results provide psychophysical evidence that, for processing of motion in depth, the auditory system responds to both auditory changing intensity and visual motion in depth.     

Perceptual consequences of centre-surround antagonism in visual motion processing

Centre-surround receptive field organization is a ubiquitous property in mammalian visual systems, presumably tailored for extracting image features that are differentially distributed over space. In visual motion, this is evident as antagonistic interactions between centre and surround regions of the receptive fields of many direction-selective neurons in visual cortex. In a series of psychophysical experiments we make the counterintuitive observation that increasing the size of a high-contrast moving pattern renders its direction of motion more difficult to perceive and reduces its effectiveness as an adaptation stimulus. We propose that this is a perceptual correlate of centre-surround antagonism, possibly within a population of neurons in the middle temporal visual area. The spatial antagonism of motion signals observed at high contrast gives way to spatial summation as contrast decreases. Evidently, integration of motion signals over space depends crucially on the visibility of those signals, thereby allowing the visual system to register motion information efficiently and adaptively.     

A neural representation of depth from motion parallax in macaque visual cortex

Perception of depth is a fundamental challenge for the visual system, particularly for observers moving through their environment. The brain makes use of multiple visual cues to reconstruct the three-dimensional structure of a scene. One potent cue, motion parallax, frequently arises during translation of the observer because the images of objects at different distances move across the retina with different velocities. Human psychophysical studies have demonstrated that motion parallax can be a powerful depth cue, and motion parallax seems to be heavily exploited by animal species that lack highly developed binocular vision. However, little is known about the neural mechanisms that underlie this capacity. Here we show, by using a virtual-reality system to translate macaque monkeys (Macaca mulatta) while they viewed motion parallax displays that simulated objects at different depths, that many neurons in the middle temporal area (area MT) signal the sign of depth (near versus far) from motion parallax in the absence of other depth cues. To achieve this, neurons must combine visual motion with extra-retinal (non-visual) signals related to the animal's movement. Our findings suggest a new neural substrate for depth perception and demonstrate a robust interaction of visual and non-visual cues in area MT. Combined with previous studies that implicate area MT in depth perception based on binocular disparities, our results suggest that area MT contains a more general representation of three-dimensional space that makes use of multiple cues.     

Representation of a perceptual decision in developing oculomotor commands

Behaviour often depends on the ability to make categorical judgements about sensory information acquired over time. Such judgements require a comparison of the evidence favouring the alternatives, but how the brain forms these comparisons is unknown. Here we show that in a visual discrimination task, the accumulating balance of sensory evidence favouring one interpretation over another is evident in the neural circuits that generate the behavioural response. We trained monkeys to make a direction judgement about dynamic random-dot motions and to indicate their judgement with an eye movement to a visual target. We interrupted motion viewing with electrical microstimulation of the frontal eye field and analysed the resulting, evoked eye movements for evidence of ongoing activity associated with the oculomotor response. Evoked eye movements deviated in the direction of the monkey's judgement. The magnitude of the deviation depended on motion strength and viewing time. The oculomotor signals responsible for these deviations reflected the accumulated motion information that informed the monkey's choices on the discrimination task. Thus, for this task, decision formation and motor preparation appear to share a common level of neural organization.     

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.     

Voice-selective areas in human auditory cortex

The human voice contains in its acoustic structure a wealth of information on the speaker's identity and emotional state which we perceive with remarkable ease and accuracy. Although the perception of speaker-related features of voice plays a major role in human communication, little is known about its neural basis. Here we show, using functional magnetic resonance imaging in human volunteers, that voice-selective regions can be found bilaterally along the upper bank of the superior temporal sulcus (STS). These regions showed greater neuronal activity when subjects listened passively to vocal sounds, whether speech or non-speech, than to non-vocal environmental sounds. Central STS regions also displayed a high degree of selectivity by responding significantly more to vocal sounds than to matched control stimuli, including scrambled voices and amplitude-modulated noise. Moreover, their response to stimuli degraded by frequency filtering paralleled the subjects' behavioural performance in voice-perception tasks that used these stimuli. The voice-selective areas in the STS may represent the counterpart of the face-selective areas in human visual cortex; their existence sheds new light on the functional architecture of the human auditory cortex.     

Robust judgement of inter-object distance by an arthropod

Animals use several strategies for depth vision, reflecting the constraints imposed by body size, the structure of the visual system and the visual geometry of the environment. Arthropods in particular have restricted depth perception, because they are small and possess closely set, low-resolution compound eyes. Yet, here we show that fiddler crabs defending their burrows from conspecifics can judge how close other crabs are to their burrow. When confronted with small dummy crabs, the burrow owners assess the dummy's position and motion relative to their burrow and not relative to themselves--in other words, by using an allocentric rather than an egocentric frame of reference. Irrespective of their own distance from the dummy, the likelihood that the crabs rush back to defend their burrow increases strongly as the dummy approaches the burrow. In addition, the mean dummy-burrow distance at which the crabs respond is constant and independent of the dummy's direction of approach. We propose that to solve this sophisticated task of relative distance judgement, the crabs combine visual information on dummy position and direction with information on burrow location acquired during path integration. In doing so, the crabs, like humans, make clever use of the visual geometry of their environment.     

Motion direction, speed and orientation in binocular matching

The spatial differences between the images seen by the two eyes, called binocular disparities, can be used to recover the volumetric (three-dimensional) aspects of a scene. The computation of disparity depends upon the correct identification of corresponding features in the two images. Understanding what image features are used by the brain to solve this matching problem is one of the main issues in stereoscopic vision. Many cortical neurons in visual areas V1 (ref. 2), MT (refs 3, 4) and MST (refs 5, 6) that are tuned to binocular disparity are also tuned to orientation, motion direction and speed. Although psychophysical work has shown that motion direction can facilitate binocular matching, the psychophysical literature on the role of orientation is mixed, and it has been argued that speed differences are ineffective in aiding correspondence. Here we use a different psychophysical paradigm to show that the visual system uses similarities in orientation, motion direction and speed to achieve binocular correspondence. These results indicate that cells that multiplex orientation, motion direction, speed and binocular disparity may help to solve the binocular matching problem.     

Perceptual learning without perception.

The brain is able to adapt rapidly and continually to the surrounding environment, becoming increasingly sensitive to important and frequently encountered stimuli. It is often claimed that this adaptive learning is highly task-specific, that is, we become more sensitive to the critical signals in the tasks we attend to. Here, we show a new type of perceptual learning, which occurs without attention, without awareness and without any task relevance. Subjects were repeatedly presented with a background motion signal so weak that its direction was not visible; the invisible motion was an irrelevant background to the central task that engaged the subject's attention. Despite being below the threshold of visibility and being irrelevant to the central task, the repetitive exposure improved performance specifically for the direction of the exposed motion when tested in a subsequent suprathreshold test. These results suggest that a frequently presented feature sensitizes the visual system merely owing to its frequency, not its relevance or salience.     

Neurons compute internal models of the physical laws of motion

A critical step in self-motion perception and spatial awareness is the integration of motion cues from multiple sensory organs that individually do not provide an accurate representation of the physical world. One of the best-studied sensory ambiguities is found in visual processing, and arises because of the inherent uncertainty in detecting the motion direction of an untextured contour moving within a small aperture. A similar sensory ambiguity arises in identifying the actual motion associated with linear accelerations sensed by the otolith organs in the inner ear. These internal linear accelerometers respond identically during translational motion (for example, running forward) and gravitational accelerations experienced as we reorient the head relative to gravity (that is, head tilt). Using new stimulus combinations, we identify here cerebellar and brainstem motion-sensitive neurons that compute a solution to the inertial motion detection problem. We show that the firing rates of these populations of neurons reflect the computations necessary to construct an internal model representation of the physical equations of motion.     

Mapping multiple features in the population response of visual cortex

Stimulus features such as edge orientation, motion direction and spatial frequency are thought to be encoded in the primary visual cortex by overlapping feature maps arranged so that the location of neurons activated by a particular combination of stimulus features can be predicted from the intersections of these maps. This view is based on the use of grating stimuli, which limit the range of stimulus combinations that can be examined. We used optical imaging of intrinsic signals in ferrets to assess patterns of population activity evoked by the motion of a texture (a field of iso-oriented bars). Here we show that the same neural population can be activated by multiple combinations of orientation, length, motion axis and speed. Rather than reflecting the intersection of multiple maps, our results indicate that population activity in primary visual cortex is better described as a single map of spatiotemporal energy.     

Feature-based attention influences motion processing gain in macaque visual cortex.

Changes in neural responses based on spatial attention have been demonstrated in many areas of visual cortex, indicating that the neural correlate of attention is an enhanced response to stimuli at an attended location and reduced responses to stimuli elsewhere. Here we demonstrate non-spatial, feature-based attentional modulation of visual motion processing, and show that attention increases the gain of direction-selective neurons in visual cortical area MT without narrowing the direction-tuning curves. These findings place important constraints on the neural mechanisms of attention and we propose to unify the effects of spatial location, direction of motion and other features of the attended stimuli in a 'feature similarity gain model' of attention.     

Three-dimensional illusory contours and surfaces.

Under general viewing conditions, objects are often partially camouflaged, obscured or occluded, thereby limiting information about their three-dimensional position, orientation and shape to incomplete and variable image cues. When presented with such partial cues, observers report perceiving 'illusory' contours and surfaces (forms) in regions having no physical image contrast. Here we report that three-dimensional illusory forms share three fundamental properties with 'real' forms: (1) the same forms are perceived using either stereo or motion parallax cues (cue invariance); (2) they retain their shape over changes in position and orientation relative to an observer (view stability); and (3) they can take the shape of general contours and surfaces in three dimensions (morphic generality). We hypothesize that illusory contours and surfaces are manifestations of a previously unnoticed visual process which constructs a representation of three-dimensional position, orientation and shape of objects from available image cues.     

Molecular identification of a retinal cell type that responds to upward motion

The retina contains complex circuits of neurons that extract salient information from visual inputs. Signals from photoreceptors are processed by retinal interneurons, integrated by retinal ganglion cells (RGCs) and sent to the brain by RGC axons. Distinct types of RGC respond to different visual features, such as increases or decreases in light intensity (ON and OFF cells, respectively), colour or moving objects. Thus, RGCs comprise a set of parallel pathways from the eye to the brain. The identification of molecular markers for RGC subsets will facilitate attempts to correlate their structure with their function, assess their synaptic inputs and targets, and study their diversification. Here we show, by means of a transgenic marking method, that junctional adhesion molecule B (JAM-B) marks a previously unrecognized class of OFF RGCs in mice. These cells have asymmetric dendritic arbors aligned in a dorsal-to-ventral direction across the retina. Their receptive fields are also asymmetric and respond selectively to stimuli moving in a soma-to-dendrite direction; because the lens reverses the image of the world on the retina, these cells detect upward motion in the visual field. Thus, JAM-B identifies a unique population of RGCs in which structure corresponds remarkably to function.     

Linear processing of spatial cues in primary auditory cortex.

To determine the direction of a sound source in space, animals must process a variety of auditory spatial cues, including interaural level and time differences, as well as changes in the sound spectrum caused by the direction-dependent filtering of sound by the outer ear. Behavioural deficits observed when primary auditory cortex (A1) is damaged have led to the widespread view that A1 may have an essential role in this complex computational task. Here we show, however, that the spatial selectivity exhibited by the large majority of A1 neurons is well predicted by a simple linear model, which assumes that neurons additively integrate sound levels in each frequency band and ear. The success of this linear model is surprising, given that computing sound source direction is a necessarily nonlinear operation. However, because linear operations preserve information, our results are consistent with the hypothesis that A1 may also form a gateway to higher, more specialized cortical areas.     

Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain

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