Visuospatial Properties of Ventral Premotor Cortex

Abstract

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.

Peripersonal space boundaries around the lower limbs

“…Critically, these reaction times within the approximated PPS are significantly faster than reaction times to unimodal tactile stimulation (i.e., when no visual stimulus is presented in conjunction with the tactile stimulus). Notably, when the stimulus instead recedes from the body, this sigmoidal relationship (usually) disappears (Canzoneri et al 2012;Teneggi et al 2013;Noel et al 2015;Serino et al 2015).This aligns with the aforementioned neurophysiological studies that have shown that neurons in the PPS network preferentially respond to stimuli approaching (in contrast to receding from) the body (Colby et al 1993;Graziano and Gross 1995;Fogassi et al 1996;Graziano et al 1997;Duhamel et al 1998).…”

“…For instance, one might swat an approaching (buzzing) fly away from his face, or retract the foot from an oncoming wave on the beach shore. Intriguingly, early neurophysiological studies in non-human primates have shown that there are special fronto-parietal neurons that respond not only to an object touching a body part but also the presence of an object near that same body part (Graziano et al 1994(Graziano et al , 1997Fogassi et al 1996;Graziano and Cooke 2006). These neurons are bi-and tri-modal in nature; their tactile receptive fields overlap with visual and/or auditory receptive fields that extend into space around the body.…”

“…Noteworthily, this system is particularly sensitive to dynamic, compared to static, stimuli (Fogassi et al 1996). And specifically, it is more responsive to stimuli approaching the body than to stimuli receding away from the body (Colby et al 1993;Graziano and Gross 1995;Fogassi et al 1996;Graziano et al 1997;Duhamel et al 1998). This space ultimately serves as a defense network Graziano 2003, 2004;Graziano and Cooke 2006) and sensorimotor interaction area for the body (Rizzolatti et al 1997;Makin et al 2008;Brozzoli et al 2010).…”

“…In monkeys, PPS extends (usually) to approximately 30 cm for the upper (head, hands, arms, upper torso) body, but can range between 5 and 100 cm (Colby et al 1993;Graziano et al 1994Graziano et al , 1999Graziano and Gross 1995). In other words, once an approaching object arrives within 30 cm of the body, the discharge rate of these bimodal neurons is enhanced (Graziano et al 1997). In turn, the size of the PPS representation for a body part can be defined by the activity of these neurons.…”

“…The stepping action is directly guided by the lower limbs, and perhaps it is modulated by their (or the whole body's) PPS representation. But while Graziano et al (1997) suggested that 'foot-centered' PPS neurons likely exist, PPS boundaries around the lower limbs were never (neurophysiologically) investigated. One possibility (as alluded to) is that the lower limb PPS representation aligns with the trunk's PPS representation, as both the trunk and the feet are intimately linked to full body actions (such as walking or balance).…”