Two-dimensional substructure of MT receptive fields.

Neurons at progressively higher levels of the visual system have progressively larger, more complicated receptive fields, presumably constructed from simpler antecedent receptive fields. To study this hierarchical organization, we used sparse white noise to map receptive-field substructure (second order Wiener-like kernels) in an extrastriate motion processing area (MT) of alert monkeys. The maps revealed a clear substructure, on a spatial scale comparable to the receptive fields of the V1 inputs. There were both facilitatory and suppressive interactions that differed in spatial organization and time course. Directional interactions were remarkably precise over a very small spatial range, and reversed when successive stimuli reversed contrast--a neural correlate of "reverse phi" motion perception. The maps of some cells had an unexpected, curved shape, which challenges existing models for direction selectivity.

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.

Visual processing: parallel-er and parallel-er.

The mammalian visual system processes many different aspects of the visual scene in separate, parallel channels. Recent experiments suggest that the visual cortex, like the retina, forms parallel circuits even at very fine spatial scales.

Specificity of projections from wide-field and local motion-processing regions within the middle temporal visual area of the owl monkey.

The middle temporal visual area (MT) of the owl monkey is anatomically organized with respect to both preferred direction of motion and different types of center-surround interaction. The latter organization consists of clusters of neurons whose receptive fields have antagonistic surrounds that render them unresponsive to wide-field motion (local motion columns) interdigitated with groups of neurons whose receptive fields have additive surrounds and thus respond best to wide-field motion (wide-field motion columns). To learn whether the information in these regions remained segregated further along the visual pathways, we made injections of retrograde tracers into two visual areas to which MT projects [the medial superior temporal area (MST) and fundus of the superior temporal sulcus (FST)] and then labeled the wide-field and local organization using 2-deoxyglucose. In complementary experiments, we injected anterograde tracers into regions of MT that we had mapped using microelectrode recordings. Injections into both dorsal FST and ventral MST labeled clusters of cell bodies in MT that were concentrated within wide-field motion columns, whereas injections into dorsal MST labeled neurons predominantly within local motion columns. Results from the anterograde tracer experiments corroborated these findings. The high degree of specificity in the connections reinforces a model of functional organization for wide-field versus local motion processing within MT. Our data support the previously reported division of FST into separate dorsal and ventral areas, and they also suggest that MST of the owl monkey is, like MST of the macaque, functionally organized with respect to local versus wide-field motion processing.

In vivo microelectrode track reconstruction using magnetic resonance imaging.

To obtain more precise anatomical information about cortical sites of microelectrode recording and microstimulation experiments in alert animals, we have developed a non-invasive, magnetic resonance imaging (MRI) technique for reconstructing microelectrode tracks. We made microelectrode penetrations in the brains of anesthetized rats and marked sites along them by depositing metal, presumably iron, with anodic monophasic or biphasic current from the tip of a stainless steel microelectrode. The metal deposits were clearly visible in the living animal as approximately 200 microm wide hypointense punctate marks using gradient echo sequences in a 4.7T MRI scanner. We confirmed the MRI findings by comparing them directly to the postmortem histology in which the iron in the deposits could be rendered visible with a Prussian blue reaction. MRI-visible marks could be created using currents as low as 1 microA (anodic) for 5 s, and they remained stable in the brains of living rats for up to nine months. We were able to make marks using either direct current or biphasic current pulses. Biphasic pulses caused less tissue damage and were similar to those used by many laboratories for functional microstimulation studies in the brains of alert monkeys.

Center-surround interactions in the middle temporal visual area of the owl monkey.

Microelectrode recording and 2-deoxyglucose (2dg) labeling were used to investigate center-surround interactions in the middle temporal visual area (MT) of the owl monkey. These techniques revealed columnar groups of neurons whose receptive fields had opposite types of center-surround interaction with respect to moving visual stimuli. In one type of column, neurons responded well to objects such as a single bar or spot but poorly to large textured stimuli such as random dots. This was often due to the fact that the receptive fields had antagonistic surrounds: surround motion in the same direction as that preferred by the center suppressed responses, thus rendering these neurons unresponsive to wide-field motion. In the second set of complementary, interdigitated columns, neuronal receptive fields had reinforcing surrounds and responded optimally to wide-field motion. This functional organization could not be accounted for by systematic differences in binocular disparity. Within both column types, neurons whose receptive fields exhibited center-surround interactions were found less frequently in the input layers compared with the other layers. Additional tests were done on single units to examine the nature of the center-surround interactions. The direction tuning of the surround was broader than that of the center, and the preferred direction, with respect to that of the center, tended to be either in the same or opposite direction and only rarely in orthogonal directions. Surround motion at various velocities modulated the overall responsiveness to centrally placed moving stimuli, but it did not produce shifts in the peaks of the center's tuning curves for either direction or speed. In layers 3B and 5 of the local motion processing columns, a number of neurons responded only to local motion contrast but did so over a region of the visual field that was much larger than the optimal stimulus size. The central feature of this receptive field type was the generalization of surround antagonism over retinotopic space-a property similar to other "complex" receptive fields described previously. The columnar organization of different types of center-surround interactions may reflect the initial segregation of visual motion information into wide-field and local motion contrast systems that serve complementary functions in visual motion processing. Such segregation appears to occur at later stages of the macaque motion processing stream, in the medial superior temporal area (MST), and has also been described in invertebrate visual systems where it appears to be involved in the important function of distinguishing background motion from object motion.

Spatial frequency tuning of single units in macaque supragranular striate cortex.

2-Deoxyglucose experiments have raised the possibility of a functional organization for spatial frequency in macaque striate cortex. To analyze this possibility with better spatial resolution, we made tangential microelectrode penetrations at constant eccentricity through supragranular striate cortex in 7 anesthetized, paralyzed macaque monkeys. We recorded from 121 single units. The data fell into two distinct populations with respect to mean preferred spatial frequency: (i) interblob cells (3.8 +/- 2.0 cycles/degree, n = 83) and (ii) blob cells (1.1 +/- 0.8 cycles/degree, n = 38; P less than 0.001). Beyond this, we found no evidence for an orderly mapping of spatial frequency optima. At blob-interblob borders, we observed abrupt shifts from low, relatively uniform spatial frequency optima (blobs) to higher optima that varied unsystematically (interblobs). The spatial frequency optima (low vs. high) and nature of the tuning curves (low-pass vs. band-pass) in blob vs. interblob cells correlate well with psychophysical measures of the same differences for the chrominance vs. luminance channels. These data are consistent with a functional subdivision of striate cortex in which blob cells carry information concerned predominantly with color and interblob neurons carry information important for form analysis.

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.

Single-unit and 2-deoxyglucose studies of side inhibition in macaque striate cortex.

In the course of studies to map spatial frequency tuning of neurons in layers 2 and 3 of macaque striate cortex, we found that a high proportion (70%) of cells in the interblob regions responded poorly to full-field gratings, compared with responses to single bars, edges, or delimited gratings. This was most often due to side inhibition, in which increasing the number of cycles of a grating placed within the cell's receptive field causes progressive inhibition of response. Quantitative receptive-field mappings showed, however, that the inhibition can occur within the region activated by a bar, as well as beyond it. The inhibition appears to be orientation-selective, in that a surround grating was more effective at inhibiting the response to a center grating patch if it was of similar orientation. 2-Deoxyglucose experiments confirmed that side inhibition is very widespread in the interblobs of layers 2 and 3 and suggested that it is reduced or lacking in layers 4A through 6. Since layers 2 and 3 of striate cortex are the major source of cortical projections to area V2 and beyond, the prevalence of side stopping in these laminae has implications for theories of cortical visual function. Side-stopped interblob cells may be acting as "contour-pass filters" that filter out redundant information in textured or noisy surfaces, focusing subsequent form processing on contrasts corresponding to object boundaries.

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.

Dynamic properties of neurons in cortical area MT in alert and anaesthetized macaque monkeys.

In order to see the world with high spatial acuity, an animal must sample the visual image with many detectors that restrict their analyses to extremely small regions of space. The visual cortex must then integrate the information from these localized receptive fields to obtain a more global picture of the surrounding environment. We studied this process in single neurons within the middle temporal visual area (MT) of macaques using stimuli that produced conflicting local and global information about stimulus motion. Neuronal responses in alert animals initially reflected predominantly the ambiguous local motion features, but gradually converged to an unambiguous global representation. When the same animals were anaesthetized, the integration of local motion signals was markedly impaired even though neuronal responses remained vigorous and directional tuning characteristics were intact. Our results suggest that anaesthesia preferentially affects the visual processing responsible for integrating local signals into a global visual representation.

How is a sensory map read Out? Effects of microstimulation in visual area MT on saccades and smooth pursuit eye movements.

To generate behavioral responses based on sensory input, motor areas of the brain must interpret, or "read out," signals from sensory maps. Our experiments tested several algorithms for how the motor systems for smooth pursuit and saccadic eye movements might extract a usable signal of target velocity from the distributed representation of velocity in the middle temporal visual area (MT or V5). Using microstimulation, we attempted to manipulate the velocity information within MT while monkeys tracked a moving visual stimulus. We examined the effects of the microstimulation on smooth pursuit and on the compensation for target velocity shown by saccadic eye movements. Microstimulation could alter both the speed and direction of the motion estimates of both types of eye movements and could also cause monkeys to generate pursuit even when the visual target was actually stationary. The pattern of alterations suggests that microstimulation can introduce an additional velocity signal into MT and that the pursuit and saccadic systems usually compute a vector average of the visually evoked and microstimulation-induced velocity signals (pursuit, 55 of 122 experiments; saccades, 70 of 122). Microstimulation effects in a few experiments were consistent with vector summation of these two signals (pursuit, 6 of 122; saccades, 2 of 122). In the remainder of the experiments, microstimulation caused either an apparent impairment in motion processing (pursuit, 47 of 122; saccades, 41 of 122) or had no effect (pursuit, 14 of 122; saccades, 9 of 122). Within individual experiments, the effects on pursuit and saccades were usually similar, but the occasional striking exception suggests that the two eye movement systems may perform motion computations somewhat independently.

Maps of complex motion selectivity in the superior temporal cortex of the alert macaque monkey: a double-label 2-deoxyglucose study.

The superior temporal sulcus (STS) of the macaque monkey contains multiple visual areas. Many neurons within these regions respond selectively to motion direction and to more complex motion patterns, such as expansion, contraction and rotation. Single-unit recording and optical recording studies in MT/MST suggest that cells with similar tuning properties are clustered into columns extending through multiple cortical layers. In this study, we used a double-label 2-deoxyglucose technique in awake, behaving macaque monkeys to clarify this functional organization. This technique allowed us to label, in a single animal, two populations of neurons responding to two different visual stimuli. In one monkey we compared expansion with contraction; in a second monkey we compared expansion with clockwise rotation. Within the STS we found a patchy arrangement of cortical columns with alternating stimulus selectivity: columns of neurons preferring expansion versus contraction were more widely separated than those selective for expansion versus rotation. This mosaic of interdigitating columns on the floor and posterior bank of the STS included area MT and some neighboring regions of cortex, perhaps including area MST.

Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging.

Using noninvasive functional magnetic resonance imaging (fMRI) technique, we analyzed the responses in human area MT with regard to visual motion, color, and luminance contrast sensitivity, and retinotopy. As in previous PET studies, we found that area MT responded selectively to moving (compared to stationary) stimuli. The location of human MT in the present fMRI results is consistent with that of MT in earlier PET and anatomical studies. In addition we found that area MT has a much higher contrast sensitivity than that in several other areas, including primary visual cortex (V1). Functional MRI half-amplitudes in V1 and MT occurred at approximately 15% and 1% luminance contrast, respectively. High sensitivity to contrast and motion in MT have been closely associated with magnocellular stream specialization in nonhuman primates. Human psychophysics indicates that visual motion appears to diminish when moving color-varying stimuli are equated in luminance. Electrophysiological results from macaque MT suggest that the human percept could be due to decreases in firing of area MT cells at equiluminance. We show here that fMRI activity in human MT does in fact decrease at and near individually measured equiluminance. Tests with visuotopically restricted stimuli in each hemifield produced spatial variations in fMRI activity consistent with retinotopy in human homologs of macaque areas V1, V2, V3, and VP. Such activity in area MT appeared much less retinotopic, as in macaque. However, it was possible to measure the interhemispheric spread of fMRI activity in human MT (half amplitude activation across the vertical meridian = approximately 15 degrees).