Encoding of movement in near extrapersonal space in primate area VIP

Abstract

Many neurons in the macaque ventral intraparietal area (VIP) are multimodal, i.e., they respond not only to visual but also to tactile, auditory and vestibular stimulation. Anatomical studies have shown distinct projections between area VIP and a region of premotor cortex controlling head movements. A specific function of area VIP could be to guide movements in order to head for and/or to avoid objects in near extrapersonal space. This behavioral role would require a consistent representation of visual motion within 3-D space and enhanced activity for nearby motion signals. Accordingly, in our present study we investigated whether neurons in area VIP are sensitive to moving visual stimuli containing depth signals from horizontal disparity. We recorded single unit activity from area VIP of two awake behaving monkeys (Macaca mulatta) fixating a central target on a projection screen. Sensitivity of neurons to horizontal disparity was assessed by presenting large field moving images (random dot fields) stereoscopically to the two eyes by means of LCD shutter goggles synchronized with the stimulus computer. During an individual trial, stimuli had one of seven different disparity values ranging from 3° uncrossed- (far) to 3° crossed- (near) disparity in 1° steps. Stimuli moved at constant speed in all simulated depth planes. Different disparity values were presented across trials in pseudo-randomized order. Sixty-one percent of the motion sensitive cells had a statistically significant selectivity for the horizontal disparity of the stimulus (p < 0.05, distribution free ANOVA). Seventy-five percent of them preferred crossed-disparity values, i.e., moving stimuli in near space, with the highest mean activity for the nearest stimulus. At the population level, preferred direction of visual stimulus motion was not affected by horizontal disparity. Thus, our findings are in agreement with the behavioral role of area VIP in the representation of movement in near extrapersonal space.

Vestibular modulation of peripersonal space boundaries

“…Indeed, the core brain regions of PPS—area VIP and ventral premotor cortex (Graziano et al ., ; di Pellegrino et al ., )—receive prominent vestibular, somatosensory, auditory, and visual inputs (Bremmer et al ., ; Schlack et al ., ; Chen et al ., ). Furthermore, direction‐dependent tuning of multimodal neurons has been demonstrated in VIP neurons (Bremmer et al ., , ; Schlack et al ., ), as dynamic visual and somatosensory stimuli at or close to the head induced the strongest neuronal response when monkeys are rotated in the same direction as the stimulus motion (Bremmer et al ., ). We suggest that the neurophysiological substrate for our reported behavioral effects are rooted within homologues areas of such PPS network in humans, and in particular the VIP region (Guipponi et al ., ).…”

“…The third experiment quantified the effects of vestibular stimulation on audio‐tactile interaction in peri‐head space. Based on previous evidence for direction‐specific PPS expansion during limb movements (e.g., Brozzoli et al ., ) and whole‐body walking (e.g., Noel et al ., ), as well as direction‐dependent encoding of visual, auditory, and somatosensory motion stimuli in monkey VIP neurons (Bremmer et al ., , ; Schlack et al ., ; Chen et al ., ), we hypothesized that vestibular stimulation would induce remapping of peri‐head space boundaries that depended on the directions of the presented motion stimuli. We tested this prediction in Experiment 3 by combining whole‐body Leftward or Rightward Rotation with Leftward or Rightward looming Sound stimulation, collapsed into Congruent trials (i.e., Leftward Rotation and Leftward Sound, Rightward Rotation and Rightward Sound) and Incongruent trials (i.e., Leftward Rotation and Rightward Sound, Rightward Rotation and Leftward Sound, Fig.…”

Looming sensitive cortical regions without V1 input: evidence from a patient with bilateral cortical blindness

“…Even more significant for our purpose, neurons in monkeys' area VIP have been found to be sensitive to the position of the movement relative to the observer, and to respond differentially according to whether the apparent location of the movement is situated in near or far extrapersonal space. Neuronal responses were found to be strongest for close, head-centered, approaching stimuli, in comparison to the responses to stimulation in the more distant extrapersonal space (Colby et al, 1993 ; Bremmer et al, 2013 ). The fact that approaching visual stimuli in the near, head-centered, personal space trigger neuronal responses, highlights the role of this area in guiding head movements in space, as well as in assessing the salience of moving stimuli and in preparing for avoidance reactions (Colby et al, 1993 ; Bremmer et al, 2013 ).…”

“…Neuronal responses were found to be strongest for close, head-centered, approaching stimuli, in comparison to the responses to stimulation in the more distant extrapersonal space (Colby et al, 1993 ; Bremmer et al, 2013 ). The fact that approaching visual stimuli in the near, head-centered, personal space trigger neuronal responses, highlights the role of this area in guiding head movements in space, as well as in assessing the salience of moving stimuli and in preparing for avoidance reactions (Colby et al, 1993 ; Bremmer et al, 2013 ). This interpretation is supported by evidence showing that monkeys display defensive behaviors such as protecting the face with their arms following VIP electrical stimulation (Cooke and Graziano, 2004 ; Graziano and Cooke, 2006 ).…”

Distributed Visual–Vestibular Processing in the Cerebral Cortex of Man and Macaque

“…The macaque ventral intraparietal area, VIP (Colby et al, 1993), is a polysensory area in the fundus of the intraparietal sulcus that encodes visual, vestibular, auditory and somatosensory stimuli. It is particularly sensitive to visual stimuli located near the observer in depth (Bremmer et al, 2013;Colby et al, 1993;Yang et al, 2011) and to air puffs on the face (Avillac et al, 2005), suggesting that it may be specialised for encoding nearby objects such as reach targets and/or obstacles during locomotion. There is evidence not only for visual-vestibular integration (discussed below), but also for visualauditory (Schlack et al, 2005) and visual-somatosensory (Avillac et al, 2007) integration.…”