Ventral intraparietal area of the macaque: anatomic location and visual response properties

1. The middle temporal area (MT) projects to the intraparietal sulcus in the macaque monkey. We describe here a discrete area in the depths of the intraparietal sulcus containing neurons with response properties similar to those reported for area MT. We call this area the physiologically defined ventral intraparietal area, or VIP. In the present study we recorded from single neurons in VIP of alert monkeys and studied their visual and oculomotor response properties. 2. Area VIP has a high degree of selectivity for the direction of a moving stimulus. In our sample 72/88 (80%) neurons responded at least twice as well to a stimulus moving in the preferred direction compared with a stimulus moving in the null direction. The average response to stimuli moving in the preferred direction was 9.5 times as strong as the response to stimuli moving in the opposite direction, as compared with 10.9 times as strong for neurons in area MT. 3. Many neurons were also selective for speed of stimulus motion. Quantitative data from 25 neurons indicated that the distribution of preferred speeds ranged from 10 to 320 degrees/s. The degree of speed tuning was on average twice as broad as that reported for area MT. 4. Some neurons (22/41) were selective for the distance at which a stimulus was presented, preferring a stimulus of equivalent visual angle and luminance presented near (within 20 cm) or very near (within 5 cm) the face. These neurons maintained their preference for near stimuli when tested monocularly, suggesting that visual cues other than disparity can support this response. These neurons typically could not be driven by small spots presented on the tangent screen (at 57 cm). 5. Some VIP neurons responded best to a stimulus moving toward the animal. The absolute direction of visual motion was not as important for these cells as the trajectory of the stimulus: the best stimulus was one moving toward a particular point on the face from any direction. 6. VIP neurons were not active in relation to saccadic eye movements. Some neurons (10/17) were active during smooth pursuit of a small target. 7. The predominance of direction and speed selectivity in area VIP suggests that it, like other visual areas in the dorsal stream, may be involved in the analysis of visual motion.     

Neuronal responses in visual areas MT and MST during smooth pursuit target selection

We recorded the activity of single neurons in the middle temporal (MT) and middle superior temporal (MST) visual areas in two macaque monkeys while the animals performed a smooth pursuit target selection task. The monkeys were presented with two moving stimuli of different colors and were trained to initiate smooth pursuit to the stimulus that matched the color of a previously given cue. We designed these experiments so that we could separate the component of the neuronal response that was driven by the visual stimulus from an extraretinal component that predicted the color or direction of the selected target. We found that for all cells in MT and MST the response was primarily determined by the visual stimulus. However, 14% (8 of 58) of MT neurons and 26% (22 of 84) of MST neurons had a small predictive component that was significant at the P < or = 0.05 level. In some cells, the predictive component was clearly related to the color of the intended target, but more often it was correlated with the direction of the target. We have previously documented a systematic shift in the latency of smooth pursuit that depends on the relative direction of motion of the two stimuli. We found that neither the latency nor the amplitude of neuronal responses in MT or MST was correlated with behavioral latency. These results are consistent with a model for target selection in which a weak selection bias for the intended target is amplified by a competitive network that suppresses motion signals related to the nonintended stimulus. It is possible that the predictive component of neuronal responses in MT and MST contributes to the selection bias. However, the strength of the selection bias in MT and MST is not sufficient to account for the high degree of selectivity shown by pursuit behavior.     

Optic flow processing in monkey STS: a theoretical and experimental approach

How does the brain process visual information about self-motion? In monkey cortex, the analysis of visual motion is performed by successive areas specialized in different aspects of motion processing. Whereas neurons in the middle temporal (MT) area are direction-selective for local motion, neurons in the medial superior temporal (MST) area respond to motion patterns. A neural network model attempts to link these properties to the psychophysics of human heading detection from optic flow. It proposes that populations of neurons represent specific directions of heading. We quantitatively compared single-unit recordings in area MST with single-neuron simulations in this model. Predictions were derived from simulations and subsequently tested in recorded neurons. Neuronal activities depended on the position of the singular point in the optic flow. Best responses to opposing motions occurred for opposite locations of the singular point in the visual field. Excitation by one type of motion is paired with inhibition by the opposite motion. Activity maxima often occur for peripheral singular points. The averaged recorded shape of the response modulations is sigmoidal, which is in agreement with model predictions. We also tested whether the activity of the neuronal population in MST can represent the directions of heading in our stimuli. A simple least-mean-square minimization could retrieve the direction of heading from the neuronal activities with a precision of 4.3 degrees. Our results show good agreement between the proposed model and the neuronal responses in area MST and further support the hypothesis that area MST is involved in visual navigation.     

Neural mechanisms for forming a perceptual decision

Cognitive and behavioral responses to environmental stimuli depend on an evaluation of sensory signals within the cerebral cortex. The mechanism by which this occurs in a specific visual task was investigated with a combination of physiological and psychophysical techniques. Rhesus monkeys discriminated among eight possible directions of motion while directional signals were manipulated in visual area MT. One directional signal was generated by a visual stimulus and a second signal was introduced by electrically stimulating neurons that encoded a specific direction of motion. The decisions made by the monkeys in response to the two signals allowed a distinction to be made between two possible mechanisms for interpreting directional signals in MT. The monkeys tended to cast decisions in favor of one or the other signal, indicating that the signals exerted independent effects on performance and that an interactive mechanism such as vector averaging of the two signals was not operative. Thus, the data suggest a mechanism in which monkeys chose the direction encoded by the largest signal in the representation of motion direction, a "winner-take-all" decision process.     

Auditory motion induces directionally dependent receptive field shifts in inferior colliculus neurons

This research focused on the response of neurons in the inferior colliculus of the unanesthetized mustached bat, Pteronotus parnelli, to apparent auditory motion. We produced the apparent motion stimulus by broadcasting pure-tone bursts sequentially from an array of loudspeakers along horizontal, vertical, or oblique trajectories in the frontal hemifield. Motion direction had an effect on the response of 65% of the units sampled. In these cells, motion in opposite directions produced shifts in receptive field locations, differences in response magnitude, or a combination of the two effects. Receptive fields typically were shifted opposite the direction of motion (i.e., units showed a greater response to moving sounds entering the receptive field than exiting) and shifts were obtained to horizontal, vertical, and oblique motion orientations. Response latency also shifted as a function of motion direction, and stimulus locations eliciting greater spike counts also exhibited the shortest neural latency. Motion crossing the receptive field boundaries appeared to be both necessary and sufficient to produce receptive field shifts. Decreasing the silent interval between successive stimuli in the apparent motion sequence increased both the probability of obtaining a directional effect and the magnitude of receptive field shifts. We suggest that the observed directional effects might be explained by "spatial masking," where the response of auditory neurons after stimulation from particularly effective locations in space would be diminished. The shift in auditory receptive fields would be expected to shift the perceived location of a moving sound and may explain shifts in localization of moving sources observed in psychophysical studies. Shifts in perceived target location caused by auditory motion might be exploited by auditory predators such as Pteronotus in a predictive tracking strategy to capture moving insect prey.     

Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT

We have used optical imaging based on intrinsic signals to explore the functional architecture of owl monkey area MT, a cortical region thought to be involved primarily in visual motion processing. As predicted by previous single-unit reports, we found cortical maps specific for the direction of moving visual stimuli. However, these direction maps were not distributed uniformly across all of area MT. Within the direction-specific regions, the activation produced by stimuli moving in opposite directions overlapped significantly. We also found that stimuli of differing shapes, moving in the same direction, activated different cortical regions within area MT, indicating that direction of motion is not the only parameter according to which area MT of owl monkey is organized. Indeed, we found clear evidence for a robust organization for orientation in area MT. Across all of MT, orientation preference changes smoothly, except at isolated line- or point-shaped discontinuities. Generally, paired regions of opposing direction preference were encompassed within a single orientation domain. The degree of segregation in the orientation maps was 3-5 times that found in direction maps. These results suggest that area MT, like V1 and V2, has a rich and multidimensional functional organization, and that orientation, a shape variable, is one of these dimensions.     

Stimulus features eliciting visual responses from neurons in the nucleus lentiformis mesencephali in pigeons

The purpose of the present study was to find out what particular stimulus features, in addition to the direction and velocity of motion, specifically activate neurons in the nucleus lentiformis mesencephali (nLM) in pigeons. Visual responses of 60 nLM cells to a variety of computer-generated stimuli were extracellularly recorded and quantitatively analyzed. Ten recording sites were histologically verified to be localized within nLM with cobalt sulfide markings. It was shown that the pigeon nLM cells were specifically sensitive to the leading edge moving at the optimal velocity in the preferred direction through their excitatory receptive fields (ERFs). Generally speaking, nLM cells preferred black edges to white ones. However, this preference cannot be explained by OFF-responses to a light spot. The edge sharpness was also an essential factor influencing the responsive strength, with blurred edges producing little or no visual responses at all. These neurons vigorously responded to black edge orientated perpendicular to, and moved in, the preferred direction; the magnitude of visual responses was reduced with changing orientation. The spatial summation occurred in all neurons tested, characterized by the finding that neuronal firings increased as the leading edge was lengthened until saturation was reached. On the other hand, it appeared that nLM neurons could not detect any differences in the shape and area of stimuli with an identical edge. These data suggested that feature extraction characteristics of nLM neurons may be specialized for detecting optokinetic stimuli, but not for realizing pattern recognition. This seems to be at least one of the reasons why large-field gratings or random-dot patterns have been used to study visual responses of accessory optic neurons and optokinetic nystagmus, because many high-contrast edges in these stimuli can activate a neuron to periodically discharge, or groups of neurons to simultaneously fire to elicit optokinetic reflex.     

Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons

A single visual stimulus activates neurons in many different cortical areas. A major challenge in cortical physiology is to understand how the neural activity in these numerous active zones leads to a unified percept of the visual scene. The anatomical basis for these interactions is the dense network of connections that link the visual areas. Within this network, feedforward connections transmit signals from lower-order areas such as V1 or V2 to higher-order areas. In addition, there is a dense web of feedback connections which, despite their anatomical prominence, remain functionally mysterious. Here we show, using reversible inactivation of a higher-order area (monkey area V5/MT), that feedback connections serve to amplify and focus activity of neurons in lower-order areas, and that they are important in the differentiation of figure from ground, particularly in the case of stimuli of low visibility. More specifically, we show that feedback connections facilitate responses to objects moving within the classical receptive field; enhance suppression evoked by background stimuli in the surrounding region; and have the strongest effects for stimuli of low salience.     

Tuning bandwidths for near-threshold stimuli in area MT

It is not known whether psychophysical performance depends primarily on small numbers of neurons optimally tuned to specific visual stimuli, or on larger populations of neurons that vary widely in their properties. Tuning bandwidths of single cells can provide important insight into this issue, yet most bandwidth measurements have been made using suprathreshold visual stimuli, whereas psychophysical measurements are frequently obtained near threshold. We therefore examined the directional tuning of cells in the middle temporal area (MT, or V5) using perithreshold, stochastic motion stimuli that we have employed extensively in combined psychophysical and physiological studies. The strength of the motion signal (coherence) in these displays can be varied independently of its direction. For each MT neuron, we characterized the directional bandwidth by fitting Gaussian functions to directional tuning data obtained at each of several motion coherences. Directional bandwidth increased modestly as the coherence of the stimulus was reduced. We then assessed the ability of MT neurons to discriminate opposed directions of motion along six equally spaced axes of motion spanning 180 degrees. A signal detection analysis yielded neurometric functions for each axis of motion, from which neural thresholds could be extracted. Neural thresholds remained surprisingly low as the axis of motion diverged from the neuron's preferred-null axis, forming a plateau of high to medium sensitivity that extended approximately 45 degrees on either side of the preferred-null axis. We conclude that directional tuning remains broad in MT when motion signals are reduced to near-threshold values. Thus directional information is widely distributed in MT, even near the limits of psychophysical performance. These observations support models in which relatively large numbers of signals are pooled to inform psychophysical decisions.     

Two visual areas located in the middle suprasylvian gyrus (cytoarchitectonic field 7) of the cat's cortex

Neuronal properties and topographic organization of the middle suprasylvian gyrus (cortical cytoarchitectonic field 7) were studied in three behaving cats with painlessly fixed heads. Two main neuronal types were found within this field. Type 1 neurons occupied the lateral part of the field and bordered representation of directionally selective neurons of the lateral suprasylvian visual area by vertical retinal meridian. Type 1 neurons had elongated and radially oriented receptive fields located in the lower part of contralateral visual field. Type 1 neurons preferred stimuli moving out or to the centre of gaze at a low or moderate speed, and many of them were depth selective. The responses were enhanced by attention, oriented to the presented stimulus. Medial part of the field 7 along the border with the area V3 was occupied by neurons with not elongated receptive fields (type 2). These neurons preferred moderate and high speeds of motion, and gratings of proper spatial frequency and orientation were effective stimuli for them. Border between representations of type 2 and type 1 neurons coincided with projection of horizontal retinal meridian. At the rostral and caudal borders of the field 7 abrupt changes of neuronal properties took place. Neurons which abutted field 7 anteriorly and posteriorly resembled hypercomplex cells and their small receptive fields were located in the central part of the visual field. Topographical considerations and receptive field properties allowed us to conclude that the medial part of the field 7 (included type 2 neurons) is functionally equivalent to the area V4 in the cortex of primates, while the lateral part (type 1 neurons) may correspond to the area V4T.     

A model for encoding multiple object motions and self-motion in area MST of primate visual cortex

Many cells in the dorsal part of the medial superior temporal (MST) region of visual cortex respond selectively to specific combinations of expansion/contraction, translation, and rotation motions. Previous investigators have suggested that these cells may respond selectively to the flow fields generated by self-motion of an observer. These patterns can also be generated by the relative motion between an observer and a particular object. We explored a neurally constrained model based on the hypothesis that neurons in MST partially segment the motion fields generated by several independently moving objects. Inputs to the model were generated from sequences of ray-traced images that simulated realistic motion situations, combining observer motion, eye movements, and independent object motions. The input representation was based on the response properties of neurons in the middle temporal area (MT), which provides the primary input to area MST. After applying an unsupervised optimization technique, the units became tuned to patterns signaling coherent motion, matching many of the known properties of MST cells. The results of this model are consistent with recent studies indicating that MST cells primarily encode information concerning the relative three-dimensional motion between objects and the observer.     

The directional effects of passive eye movement on the directional visual responses of single units in the pigeon optic tectum

We have investigated the visual responses of 184 single units located in the superficial layers of the optic tectum (OT) of the decerebrate, paralysed pigeon. Visual responses were similar to those reported in non-decerebrate preparations; most units responded best to moving visual stimuli, 18% were directionally selective (they had a clear preference for a particular direction of visual stimulus movement), 76% were plane-selective (they responded to movement in either direction in a particular plane). However, we also found that a high proportion of units showed some sensitivity to the orientation of visual stimuli. We examined the effects of extraocular muscle (EOM) afferent signals, induced by passive eye movement (PEM), on the directional visual responses of units. Visual responses were most modified by particular directions of eye movement, although there was no unique relationship between the direction of visual stimulus movement to which an individual unit responded best and the direction of eye movement that caused the greatest modification of that visual response. The results show that EOM afferent signals, carrying information concerning the direction of eye movement, reach the superficial layers of the OT in the pigeon and there modify the visual responses of units in a manner that suggests some role for these signals in the processing of visual information.     

Reactions and properties of the receptive fields of neurons in the visual projection zone of the pigeon hyperstriatum

Impulse responses of neurons of the pigeon forebrain hyperstriatal part to stationary and moving visual stimuli were investigated. Particular attention was given to revealing a retinotopic projection in the region of visual representation in Wulst. It is shown that as the electrode moved gradually in the caudal direction in the region of visual projection of the hyperstriatum, the receptive fields of the neurons under observation displaced in the visual field in the opposite direction. The receptive fields of the ventral and dorsal hyperstriatum cells remain higher in the visual field and have larger diameters than the receptive fields of neurons of the accessory hyperstriatum. Neurons responses of the visual projection of the Wulst region depend on luminosity, size, speed and direction of the movement of the test-objects through the receptive field. The functional role of the retino-thalamo-telencephalic system in the visual integration in birds is discussed and a supposition is advanced on possibility to compare the Wulst region with striatal and frontal visual areas of the mammalian cortex.     

A model for the early stages of motion processing based on spatial and temporal edge detection by X-cells

A model for the early stages of motion processing in the visual cortex is presented. The 'building block' for this model is the 'rebound response', which is the neuronal response evoked when a sufficient inhibitory stimulus is turned off. This response enables detection of temporal changes when the stimulus involves spatial changes. The model suggests that adjacent subunits in primary cortical cells have different weight functions for rebound responses, and thus a synergistic type of response is evoked in the preferred direction, which is predicted for both light and dark stimuli. Predictions of the model for different stimuli and receptive field structures are discussed. It appears to be more economical than previous motion models.     

Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1

We examined the responsivity, orientation selectivity, and direction selectivity of a sample of neurons in cortical area V1 of the macaque using visual stimuli consisting of drifting oriented contours defined by each of two very different figural cues: luminance contrast and temporal texture. Comparisons of orientation and direction tuning elicited by the different cues were made in order to test the hypothesis that the neuronal representations of these parameters are form-cue invariant. The majority of the sampled cells responded to both stimulus types, although responses to temporal texture stimuli were generally weaker than those elicited by luminance-defined stimuli. Of those units exhibiting orientation selectivity when tested with the luminance-defined stimuli, more than half were also selective for the orientation of the temporal texture stimuli. There was close correspondence between the preferred orientations and tuning bandwidths revealed with the two stimulus types. Of those units exhibiting directional selectivity when tested with the luminance-defined stimuli, about two-thirds were also selective for the direction of the temporal texture stimuli. There was close correspondence between the preferred directions revealed with the two stimulus types, although bidirectional responses were somewhat more common when temporal texture stimuli were used. These results indicate that many V1 neurons encode orientation and direction of motion of retinal image features in a manner that is largely independent of whether the feature is defined by luminance or temporal texture contrast. These neurons may contribute to perceptual phenomena in which figural cue identity is disregarded.     

Influence of the presentation of remote visual stimuli on visual responses of cat area 17 and lateral suprasylvian area

Single units were recorded extracellularly from area 17 and lateral suprasylvian area (LSSA) in curarized cats. Visual stimuli, usually a 10 degree black spot, were introduced abruptly in the visual field remote from the discharge area of a neuron's receptive field and moved at a speed of about 30 degrees/sec. The effect of these remote stimuli (S2) on the reponse to a restricted visual stimulus (S1) crossing the discharge area was studied. It was found that most units in area 17 were not affected by the presentation of remote stimuli, the remainder being either slightly facilitated or slightly inhibited. In contrast the LSSA neurons were usually inhibited by the presentation of S2: this effect was strong, was present in all classes of LSSA neurons and was independent of the relative directions of movement of S1 and S2. On the basis of these data and those previously obtained from the superior colliculus it is concluded that the way the extrageniculate centres respond to a stimulus abruptly introduced in the visual field is substantially different from that of the striate cortex. Only in the extrageniculate centres a new stimulus, besides exciting the neurons which correspond to the position of the stimulus in the field, concomitantly decreases the responses of neurons located in positions of the visual field remote from that stimulus. Possible behavioral implications of the findings are discussed.     

The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery

Echoplanar functional magnetic resonance imaging was used to monitor activation changes of brain areas while subjects viewed apparent motion stimuli and while they were engaged in motion imagery. Human cortical areas MT (V5) and MST were the first areas of the 'dorsal' processing stream which responded with a clear increase in signal intensity to apparent motion stimuli as compared with flickering control conditions. Apparent motion of figures defined by illusory contours evoked greater activation in V2 and MT/MST than appropriate control conditions. Several areas of the dorsal pathway (V3A, MT/MST, areas in the inferior and superior parietal lobule) as well as prefrontal areas including FEF and BA 9/46 responded strongly when subjects merely imagined moving stimuli which they had seen several seconds before. The activation during motion imagery increased with the synaptic distance of an area from V1 along the dorsal processing stream. Area MT/MST was selectively activated during motion imagery but not during a static imagery control condition. The comparison between the results obtained with objective motion, apparent motion and imagined motion provides further insights into a complex cortical network of motion-sensitive areas driven by bottom-up and top-down neural processes.     

Collinear stimuli regulate visual responses depending on cell's contrast threshold

Neurons in the primary visual cortex are selective for the size, orientation and direction of motion of patterns falling within a restricted region of visual space known as the receptive field. The response to stimuli presented within the receptive field can be facilitated or suppressed by other stimuli falling outside the receptive field which, when presented in isolation, fail to activate the cell. Whether this interaction is facilitative or suppressive depends on the relative orientation of pattern elements inside and outside the receptive field. Here we show that neuronal facilitation preferentially occurs when a near-threshold stimulus inside the receptive field is flanked by higher-contrast, collinear elements located in surrounding regions of visual space. Collinear flanks and orthogonally oriented flanks, however, both act to reduce the response to high-contrast stimuli presented within the receptive field. The observed pattern of facilitation and suppression may be the cellular basis for the observation in humans that the detectability of an oriented pattern is enhanced by collinear flanking elements. Modulation of neuronal responses by stimuli falling outside their receptive fields may thus represent an early neural mechanism for encoding objects and enhancing their perceptual saliency.     

The influence of stimulus properties on multisensory processing in the awake primate superior colliculus.

Evaluated the influence of physical properties of sensory stimuli (visual intensity, direction, and velocity; auditory intensity and location) on sensory activity and multisensory integration of superior colliculus (SC) neurons in awake, behaving primates. Two male monkeys were trained to fixate a central visual fixation point while visual and/or auditory stimuli were presented in the periphery. Visual stimuli were always presented within the contralateral receptive field of the neuron whereas auditory stimuli were presented at either ipsi- or contralateral locations. 66 of the 84 SC neurons responsive to these sensory stimuli had stronger responses when the visual and auditory stimuli were combined at contralateral locations than when the auditory stimulus was located on the ipsilateral side. This trend was significant across the population of auditory-responsive neurons. In addition, 31 SC neurons were presented a battery of tests in which the quality of one stimulus of a pair was systematically manipulated. Eight of these neurons showed preferential responses to stimuli with specific physical properties, and these preferences were not significantly altered when multisensory stimulus combinations were presented. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey

Extrastriate cortical area MT is thought to process behaviorally important visual motion signals. Psychophysical studies suggest that visual motion signals may be analyzed by multiple mechanisms, a "first-order" one based on luminance, and a "second-order" one based upon higher level cues (e.g. contrast, flicker). Second-order motion is visible to human observers, but should be invisible to first-order motion sensors. To learn if area MT is involved in the analysis of second-order motion, we measured responses to first- and second-order gratings of single neurons in area MT (and in one experiment, in area V1) in anesthetized, paralyzed macaque monkeys. For each neuron, we measured directional and spatio-temporal tuning with conventional first-order gratings and with second-order gratings created by spatial modulation of the flicker rate of a random texture. A minority of MT and V1 neurons exhibited significant selectivity for direction or orientation of second-order gratings. In nearly all cells, response to second-order motion was weaker than response to first-order motion. MT cells with significant selectivity for second-order motion tended to be more responsive and more sensitive to luminance contrast, but were in other respects similar to the remaining MT neurons; they did not appear to represent a distinct subpopulation. For those cells selective for second-order motion, we found a correlation between the preferred directions of first- and second-order motion, and weak correlations in preferred spatial frequency. These cells preferred lower temporal frequencies for second-order motion than for first-order motion. A small proportion of MT cells seemed to remain selective and responsive for second-order motion. None of our small sample of V1 cells did. Cells in this small population, but not others, may perform "form-cue invariant" motion processing (Albright, 1992).