Visual–vestibular interactive responses in the macaque ventral intraparietal area (VIP)

Abstract

Self-motion detection requires the interaction of a number of sensory systems for correct perceptual interpretation of a given movement and an eventual motor response. Parietal cortical areas are thought to play an important role in this function, and we have thus studied the encoding of multimodal signals and their spatiotemporal interactions in the ventral intraparietal area of macaque monkeys. Thereby, we have identified for the first time the presence of vestibular sensory input to this area and described its interaction with somatosensory and visual signals, via extracellular single-cell recordings in awake head-fixed animals. Visual responses were driven by large field stimuli that simulated either backward or forward self-motion (contraction or expansion stimuli, respectively), or movement in the frontoparallel plane (visual increments moving simultaneously in the same direction). While the dominant sensory modality in most neurons was visual, about one third of all recorded neurons responded to horizontal rotation. These vestibular responses were typically in phase with head velocity, but in some cases they could signal acceleration or even showed integration to position. The associated visual responses were always codirectional with the vestibular on-direction, i.e. noncomplementary. Somatosensory responses were in register with the visual preferred direction, either in the same or in the opposite direction, thus signalling translation or rotation in the horizontal plane. These results, taken together with data on responses to optic flow stimuli obtained in a parallel study, strongly suggest an involvement of area VIP in the analysis and the encoding of self-motion.

Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey

“…VIP has been shown to be a site of multisensory convergence (Colby et al, 1993;Duhamel et al, 1998;Bremmer et al, 2002;Schlack et al, 2002Schlack et al, , 2005Schroeder and Foxe, 2002). We show that the majority of VIP neurons integrate multisensory stimuli.…”

“…Such a convergence has been described in parietal area 7b (Hyvärinen, 1981;Graziano and Gross, 1995), in the ventral intraparietal area (VIP) (Colby et al, 1993;Duhamel et al, 1998;Bremmer et al, 2002;Schlack et al, 2002Schlack et al, , 2005, in the ventral premotor area (Rizzolatti et al, 1981;Graziano and Gross, 1995;Graziano et al, 1999;Graziano and Gandhi, 2000), in the superior temporal sulcus (Benevento et al, 1977;Leinonen et al, 1980;Bruce et al, 1981;Hikosaka et al, 1988), in the putamen (Graziano and Gross, 1995), and in the superior colliculus (SC) (Meredith and Stein, 1986a;Stein and Meredith, 1993;Wallace et al, 1996;Bell et al, 2001Bell et al, , 2003.…”

Multisensory anatomical pathways

“…This is particularly the case for the areas buried in the intraparietal sulcus (LIP, VIP) which present anatomical links with cortical areas of different sensory modalities (Lewis and Van Essen, 2000). For instance, in the monkey, the parietal area VIP receives inputs from visual, auditory, somatosensory, vestibular, motor and polysensory areas (Duhamel et al, 1998) that confer typical multimodal responses to the VIP neurons (Bremmer et al, 2002;Schlack et al, 2005;Avillac et al, 2007). Similarly, the connectivity pattern of the LIP Blatt et al, 1990;Lewis and Van Essen, 2000) is consistent with the multisensory properties reported for LIP neurons (Cohen et al, 2005;Russ et al, 2006;Gottlieb, 2007).…”

Vestibular Signals in Primate Thalamus: Properties and Origins

“…Other portions of parietal and temporal cortex showing vestibular activity include the anterior tip of the intraparietal sulcus (area 2v) (Büttner and Buettner 1978;Fredrickson et al, 1966;Schwarz and Fredrickson 1971a,b), the medial superior temporal area (Page and Duffy, 2003;Gu et al, 2006Gu et al, , 2007, and the ventral intraparietal area (Bremmer et al, 2002;Klam and Graf, 2003;Chen et al, 2007). Whether the pulvinar units we recorded could supply these parietal and temporal areas is presently unknown.…”