Carol L. Colby

Every eye movement produces a shift in the visual image on the retina. The receptive field, or retinal response area, of an individual visual neuron moves with the eyes so that after an eye movement it covers a new portion of visual space. For some parietal neurons, the location of the receptive field is shown to shift transiently before an eye movement. In addition, nearly all parietal neurons respond when an eye movement brings the site of a previously flashed stimulus into the receptive field. Parietal cortex both anticipates the retinal consequences of eye movements and updates the retinal coordinates of remembered stimuli to generate a continuously accurate representation of visual space.

The space around us is represented not once but many times in parietal cortex. These multiple representations encode locations and objects of interest in several egocentric reference frames. Stimulus representations are transformed from the coordinates of receptor surfaces, such as the retina or the cochlea, into the coordinates of effectors, such as the eye, head, or hand. The transformation is accomplished by dynamic updating of spatial representations in conjunction with voluntary movements. This direct sensory-to-motor coordinate transformation obviates the need for a single representation of space in environmental coordinates. In addition to representing object locations in motoric coordinates, parietal neurons exhibit strong modulation by attention. Both top-down and bottom-up mechanisms of attention contribute to the enhancement of visual responses. The saliance of a stimulus is the primary factor in determining the neural response to it. Although parietal neurons represent objects in motor coordinates, visual responses are independent of the intention to perform specific motor acts.

In a previous report, we described the visual response properties in the ventral intraparietal area (area VIP) of the awake macaque. Here we describe the somatosensory response properties in area VIP and the patterns of correspondence between the responses of single neurons to independently administered tactile and visual stimulation. VIP neurons responded to visual stimulation only or to visual and tactile stimulation. Of 218 neurons tested, 153 (70%) were bimodal in the sense that they responded to stimuli that were independently applied in either sensory modality. Unimodal visual and bimodal neurons were intermingled within the recording area and could not be distinguished on the basis of their visual response properties alone. Most of the cells with a tactile receptive field (RF) responded well to light touch or air puffs. The distribution of RF locations principally emphasized the head (85%), with approximately equivalent representations of the upper and lower face areas. The tactile and visual RFs were aligned in a congruent manner, with the intersection of the visual vertical and horizontal meridian having its tactile counterpart in the nose/mouth area. Small foveal visual RFs were paired with small tactile RFs on the muzzle, and peripheral visual RFs were associated with tactile RFs on the side of the head or body. Most cells showed a strong sensitivity to moving stimuli, and the preferred directions of visual and tactile motion coincided in 85% of bimodal cells. In some cases, bimodal responses patterns were complementary: cells responding to motion in depth toward the monkey had responses, whereas cells responding to motion in depth away form the monkey had responses. Other forms of bimodal response congruence included orientation selectivity, and , , and / response types. The large proportion of bimodal tactile and visual neurons with congruent response properties in area VIP indicates that there are important functional differences between area VIP and other dorsal stream areas involved in the analysis of motion. We suggest that VIP is involved in the construction of a multisensory, head-centered representation of near extrapersonal space.

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.

1. Posterior parietal cortex contains neurons that are visually responsive and active in relation to saccadic eye movements. We recorded from single neurons in a subregion of parietal cortex, the lateral intraparietal area (LIP), in alert rhesus monkeys. To characterize more completely the circumstances under which LIP neurons are responsive, we used five tasks designed to test the impact of sensory, motor, and cognitive factors. We obtained quantitative data in multiple tasks in 91 neurons. We measured neural activity during central fixation and in relation to stimulus onset and saccade onset. 2. LIP neurons have visual responses to the onset of a stationary stimulus in the receptive field. These visual responses occurred both in tasks that require a subsequent eye movement toward the stimulus and in tasks in which eye movements are not permitted, indicating that this activity is sensory rather than presaccadic. 3. Visual responses were enhanced when the monkey had to use information provided by the stimulus to guide its behavior. The amplitude of the sensory response to a given stimulus was increased in a task in which the monkey would subsequently make a saccade to the location signaled by the stimulus, as compared with the amplitude of the visual response in a simple fixation task. 4. The visual response was also enhanced when the monkey attended to the stimulus without looking at it. This result shows that enhancement does not reflect saccade preparation because the response is enhanced even when the monkey is not permitted to make a saccade. Instead, enhancement reflects the allocation of attention to the spatial locus of the receptive field. 5. Many LIP neurons had saccade-related activity in addition to their visual responses. The visual response for most neurons was stronger than the saccade-related activation. 6. Saccade-related activity was independent of visual activity. Similar presaccadic activity was observed in trials that included a recent visual stimulus (memory-guided saccade task) and in trials with no visual stimulus (learned saccade task). 7. We observed increases in activity during fixation in tasks in which the monkey could anticipate the onset of a behaviorally significant stimulus. LIP neurons usually showed low levels of background firing in the fixation task during the period before stimulus onset. This background activity was increased in the peripheral attention and memory-guided saccade tasks during the period when the monkey was waiting for a behaviorally relevant stimulus to appear. 8. The results from these several tasks indicate that LIP neurons are activated in a variety of circumstances and are not involved exclusively in sensory processing or motor planning. The modulation of sensory responses by attention and anticipation suggests that cognitive factors play a major role in parietal function.