Organization of the macaque extrastriate visual cortex re-examined using the principle of spatial continuity of function.

How is the macaque monkey extrastriate cortex organized? Is vision divisible into separate tasks, such as object recognition and spatial processing, each emphasized in a different anatomical stream? If so, how many streams exist? What are the hierarchical relationships among areas? The present study approached the organization of the extrastriate cortex in a novel manner. A principled relationship exists between cortical function and cortical topography. Similar functions tend to be located near each other, within the constraints of mapping a highly dimensional space of functions onto the two-dimensional space of the cortex. We used this principle to re-examine the functional organization of the extrastriate cortex given current knowledge about its topographic organization. The goal of the study was to obtain a model of the functional relationships among the visual areas, including the number of functional streams into which they are grouped, the pattern of informational overlap among the streams, and the hierarchical relationships among areas. To test each functional description, we mapped it to a model cortex according to the principle of optimal continuity and assessed whether it accurately reconstructed a version of the extrastriate topography. Of the models tested, the one that best reconstructed the topography included four functional streams rather than two, six levels of hierarchy per stream, and a specific pattern of informational overlap among streams and areas. A specific mixture of functions was predicted for each visual area. This description matched findings in the physiological literature, and provided predictions of functional relationships that have yet to be tested physiologically.

Four-dimensional spatial reasoning in humans.

Human subjects practiced navigation in a virtual, computer-generated maze that contained 4 spatial dimensions rather than the usual 3. The subjects were able to learn the spatial geometry of the 4-dimensional maze as measured by their ability to perform path integration, a standard test of spatial ability. They were able to travel down a winding corridor to its end and then point back accurately toward the occluded origin. One interpretation is that the brain substrate for spatial navigation is not a built-in map of the 3-dimensional world. Instead it may be better described as a set of general rules for manipulating spatial information that can be applied with practice to a diversity of spatial frameworks.

Is reaching eye-centered, body-centered, hand-centered, or a combination?

There are currently three main views on the neural basis of visually guided reaching: 1) neurons in the superior parietal lobe guide arm movements in a spatial framework that is centered on the body; 2) neurons in the intraparietal sulcus guide arm movements in a spatial framework that is centered on the eye; 3) neurons in the caudal part of premotor cortex guide arm movements in a spatial framework that is centered on the arm and hand. The three viewpoints are mutually compatible and may fit into a larger pattern. Eye-centered representations of target position, and body-centered representations of arm and hand position, may be integrated to form a hand-centered representation close to the output stage in caudal premotor and primary motor cortex.

Location of the polysensory zone in the precentral gyrus of anesthetized monkeys.

Neurons in the premotor cortex of macaques respond to tactile, visual and auditory stimuli. The distribution of these responses was studied in five anesthetized monkeys. In each monkey, multiunit activity was studied at a grid of locations across the precentral gyrus. A cluster of sites with polysensory responses was found posterior to the genu of the arcuate sulcus. Tactile and visual responses were represented in all five monkeys, while auditory responses were rarer and found in only two monkeys. This polysensory zone (PZ) was located in the caudal part of premotor cortex. It varied in extent among the monkeys. It was mainly ventral to the genu of the arcuate, in the dorsal and caudal part of the ventral premotor cortex (PMv). In some monkeys it extended more dorsally, into the caudal part of dorsal premotor cortex (PMd). Sensory responses were almost never found in the rostral part of PMd. We suggest that the polysensory zone may contribute to the guidance of movement on the basis of tactile, visual and auditory signals.

Coding the location of the arm by sight.

Area 5 in the parietal lobe of the primate brain is thought to be involved in monitoring the posture and movement of the body. In this study, neurons in monkey area 5 were found to encode the position of the monkey's arm while it was covered from view. The same neurons also responded to the position of a visible, realistic false arm. The neurons were not sensitive to the sight of unrealistic substitutes for the arm and were able to distinguish a right from a left arm. These neurons appear to combine visual and somatosensory signals in order to monitor the configuration of the limbs. They could form the basis of the complex body schema that we constantly use to adjust posture and guide movement.

Neurogenesis in the neocortex of adult primates.

In primates, prefrontal, inferior temporal, and posterior parietal cortex are important for cognitive function. It is shown that in adult macaques, new neurons are added to these three neocortical association areas, but not to a primary sensory area (striate cortex). The new neurons appeared to originate in the subventricular zone and to migrate through the white matter to the neocortex, where they extended axons. These new neurons, which are continually added in adulthood, may play a role in the functions of association neocortex.

Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position.

A central problem in motor control, in the representation of space, and in the perception of body schema is how the brain encodes the relative positions of body parts. According to psychophysical studies, this sense of limb position depends heavily on vision. However, almost nothing is currently known about how the brain uses vision to determine or represent the location of the arm or any other body part. The present experiment shows that the position of the arm is represented in the premotor cortex of the monkey (Macaca fascicularis) brain by means of a convergence of visual cues and proprioceptive cues onto the same neurons. These neurons respond to the felt position of the arm when the arm is covered from view. They also respond in a similar fashion to the seen position of a false arm.

Dynamic representation of eye position in the parieto-occipital sulcus.

Dynamic representation of eye position in the parieto-occipital sulcus. Area V6A, on the anterior bank of the parieto-occipital sulcus of the monkey brain, contains neurons sensitive both to visual stimulation and to the position and movement of the eyes. We examined the effects of eye position and eye movement on the activity of V6A neurons in monkeys trained to saccade to and fixate on target locations. Forty-eight percent of the neurons responded during these tasks. The responses were not caused by the visual stimulation of the fixation light because extinguishing the fixation light had no effect. Instead the neurons responded in relation to the position of the eye during fixation. Some neurons preferred a restricted range of eye positions, whereas others had more complex and distributed eye-position fields. None of these eye-related neurons responded before or during saccades. They all responded postsaccadically during fixation on the target location. However, the neurons did not simply encode the static position of the eyes. Instead most (88%) responded best after the eye saccaded into the eye-position field and responded significantly less well when the eye made a saccade that was entirely contained within the eye-position field. Furthermore, for many eye-position cells (45%), the response was greatest immediately after the eye reached the preferred position and was significantly reduced after 500 ms of fixation. Thus these neurons preferentially encoded the initial arrival of the eye into the eye-position field rather than the continued presence or the movement of the eye within the eye-position field. Area V6A therefore contains a representation of the position of the eye in the orbit, but this representation appears to be dynamic, emphasizing the arrival of the eye at a new position.

A neuronal representation of the location of nearby sounds.

Humans can accurately perceive the location of a sound source-not only the direction, but also the distance. Sounds near the head, within ducking or reaching distance, have a special saliency. However, little is known about this perception of auditory distance. The direction to a sound source can be determined by interaural differences, and the mechanisms of direction perception have been studied intensively; but except for studies on echolocation in the bat, little is known about how neurons encode information on auditory distance. Here we describe neurons in the brain of macaque monkeys (Macaca fascicularis) that represent the auditory space surrounding the head, within roughly 30 cm. These neurons, which are located in the ventral premotor cortex, have spatial receptive fields that extend a limited distance outward from the head.

Spatial maps for the control of movement.

Neurons in the ventral premotor cortex of the monkey encode the locations of visual, tactile, auditory and remembered stimuli. Some of these neurons encode the locations of stimuli with respect to the arm, and may be useful for guiding movements of the arm. Others encode the locations of stimuli with respect to the head, and may be useful for guiding movements of the head. We suggest that a general principle of sensory-motor integration is that the space surrounding the body is represented in body-part-centered coordinates. That is, there are multiple coordinate systems used to guide movement, each one attached to a different part of the body. This and other recent evidence from both monkeys and humans suggest that the formation of spatial maps in the brain and the guidance of limb and body movements do not proceed in separate stages but are closely integrated in both the parietal and frontal lobes.

Visual responses with and without fixation: neurons in premotor cortex encode spatial locations independently of eye position.

The ventral premotor cortex (PMv) of the macaque monkey contains neurons that respond both to visual and to tactile stimuli. For almost all of these "bimodal" cells, the visual receptive field is anchored to the tactile receptive field on the head or the arms, and remains stationary when the eyes fixate different locations. This study compared the responses of bimodal PMv neurons to a visual stimulus when the monkey was required to fixate a spot of light and when no fixation was required. Even when the monkey was not fixating and the eyes were moving, the visual receptive fields remained in the same location, near the associated tactile receptive field. For many of the neurons, the response to the visual stimulus was significantly larger when the monkey was not performing the fixation task. In control tests, the presence or absence of the fixation spot itself had little or no effect on the response to the visual stimulus. These results show that even when the monkey's eye position is continuously changing, the neurons in PMv have visual receptive fields that are stable and fixed to the relevant body part. The reduction in response during fixation may reflect a shift of attention from the visual stimulus to the demands of the fixation task.

Coding the locations of objects in the dark.

The ventral premotor cortex in primates is thought to be involved in sensory-motor integration. Many of its neurons respond to visual stimuli in the space near the arms or face. In this study on the ventral premotor cortex of monkeys, an object was presented within the visual receptive fields of individual neurons, then the lights were turned off and the object was silently removed. A subset of the neurons continued to respond in the dark as if the object were still present and visible. Such cells exhibit "object permanence," encoding the presence of an object that is no longer visible. These cells may underlie the ability to reach toward or avoid objects that are no longer directly visible.

Visuospatial properties of ventral premotor cortex.

In macaque ventral premotor cortex, we recorded the activity of neurons that responded to both visual and tactile stimuli. For these bimodal cells, the visual receptive field extended from the tactile receptive field into the adjacent space. Their tactile receptive fields were organized topographically, with the arms represented medially, the face represented in the middle, and the inside of the mouth represented laterally. For many neurons, both the visual and tactile responses were directionally selective, although many neurons also responded to stationary stimuli. In the awake monkeys, for 70% of bimodal neurons with a tactile response on the arm, the visual receptive field moved when the arm was moved. In contrast, for 0% the visual receptive field moved when the eye or head moved. Thus the visual receptive fields of most "arm + visual" cells were anchored to the arm, not to the eye or head. In the anesthetized monkey, the effect of arm position was similar. For 95% of bimodal neurons with a tactile response on the face, the visual receptive field moved as the head was rotated. In contrast, for 15% the visual receptive field moved with the eye and for 0% it moved with the arm. Thus the visual receptive fields of most "face + visual" cells were anchored to the head, not to the eye or arm. To construct a visual receptive field anchored to the arm, it is necessary to integrate the position of the arm, head, and eye. For arm + visual cells, the spontaneous activity, the magnitude of the visual response, and sometimes both were modulated by the position of the arm (37%), the head (75%), and the eye (58%). In contrast, to construct a visual receptive field that is anchored to the head, it is necessary to use the position of the eye, but not of the head or the arm. For face + visual cells, the spontaneous activity and/or response magnitude was modulated by the position of the eyes (88%), but not of the head or the arm (0%). Visual receptive fields anchored to the arm can encode stimulus location in "arm-centered" coordinates, and would be useful for guiding arm movements. Visual receptive fields anchored to the head can likewise encode stimuli in "head-centered" coordinates, useful for guiding head movements. Sixty-three percent of face + visual neurons responded during voluntary movements of the head. We suggest that "body-part-centered" coordinates provide a general solution to a problem of sensory-motor integration: sensory stimuli are located in a coordinate system anchored to a particular body part.

Coding of visual space by premotor neurons.

In primates, the premotor cortex is involved in the sensory guidance of movement. Many neurons in ventral premotor cortex respond to visual stimuli in the space adjacent to the hand or arm. These visual receptive fields were found to move when the arm moved but not when the eye moved; that is, they are in arm-centered, not retinocentric, coordinates. Thus, they provide a representation of space near the body that may be useful for the visual control of reaching.

Tuning of MST neurons to spiral motions.

Cells in the dorsal division of the medial superior temporal area (MSTd) have large receptive fields and respond to expansion/contraction, rotation, and translation motions. These same motions are generated as we move through the environment, leading investigators to suggest that area MSTd analyzes the optical flow. One influential idea suggests that navigation is achieved by decomposing the optical flow into the separate and discrete channels mentioned above, that is, expansion/contraction, rotation, and translation. We directly tested whether MSTd neurons perform such a decomposition by examining whether there are cells that are preferentially tuned to intermediate spiral motions, which combine both expansion/contraction and rotation components. The finding that many cells in MSTd are preferentially selective for spiral motions indicates that this simple three-channel decomposition hypothesis for MSTd does not appear to be correct. Instead, there is a continuum of patterns to which MSTd cells are selective. In addition, we find that MSTd cells maintain their selectivity when stimuli are moved to different locations in their large receptive fields. This position invariance indicates that MSTd cells selective for expansion cannot give precise information about the retinal location of the focus of expansion. Thus, individual MSTd neurons cannot code, in a precise fashion, the direction of heading by using the location of the focus of expansion. The only way this navigational information could be accurately derived from MSTd is through the use of a coarse, population encoding. Positional invariance and selectivity for a wide array of stimuli suggest that MSTd neurons encode patterns of motion per se, regardless of whether these motions are generated by moving objects or by motion induced by observer locomotion.

A bimodal map of space: somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields.

The macaque putamen contains neurons that respond to somatosensory stimuli such as light touch, joint movement, or deep muscle pressure. Their receptive fields are arranged to form a map of the body. In the face and arm region of this somatotopic map we found neurons that responded to visual stimuli. Some neurons were bimodal, responding to both visual and somatosensory stimuli, while others were purely visual, or purely somatosensory. The bimodal neurons usually responded to light cutaneous stimulation, rather than to joint movement or deep muscle pressure. They responded to visual stimuli near their tactile receptive field and were not selective for the shape or the color of the stimuli. For cells with tactile receptive fields on the face, the visual receptive field subtended a solid angle extending from the tactile receptive field to about 10 cm. For cells with tactile receptive fields on the arm, the visual receptive field often extended further from the animal. These bimodal properties provide a map of the visual space that immediately surrounds the monkey. The map is organized somatotopically, that is, by body part, rather than retinotopically as in most visual areas. It could function to guide movements in the animal's immediate vicinity. Cortical areas 6, 7b, and VIP contain bimodal cells with very similar properties to those in the putamen. We suggest that the bimodal cells in area 6, 7b, VIP, and the putamen form part of an interconnected system that represents extra personal space in a somatotopic fashion.