Visual and Vestibular Selectivity for Self-Motion in Macaque Posterior Parietal Area 7a

Abstract

We examined the responses of neurons in posterior parietal area 7a to passive rotational and translational self-motion stimuli, while systematically varying the speed of visually simulated (optic flow cues) or actual (vestibular cues) self-motion. Contrary to a general belief that responses in area 7a are predominantly visual, we found evidence for a vestibular dominance in self-motion processing. Only a small fraction of neurons showed multisensory convergence of visual/vestibular and linear/angular self-motion cues. These findings suggest possibly independent neuronal population codes for visual versus vestibular and linear versus angular self-motion. Neural responses scaled with self-motion magnitude (i.e., speed) but temporal dynamics were diverse across the population. Analyses of laminar recordings showed a strong distance-dependent decrease for correlations in stimulus-induced (signal correlation) and stimulus-independent (noise correlation) components of spike-count variability, supporting the notion that neurons are spatially clustered with respect to their sensory representation of motion. Single-unit and multiunit response patterns were also correlated, but no other systematic dependencies on cortical layers or columns were observed. These findings describe a likely independent multimodal neural code for linear and angular self-motion in a posterior parietal area of the macaque brain that is connected to the hippocampal formation.

Spatial coordinate transforms linking the allocentric hippocampal and egocentric parietal primate brain systems for memory, action in space, and navigation

“…Indeed, something like this is exactly what is proposed to account for the fact that hippocampal spatial view neurons update the allocentric location in space “out there” to which they respond when eye movements, head direction changes, or even locomotion are made in the dark (Robertson et al, ). The idiothetic update could be performed in the dorsal visual system based on the vestibular, proprioceptive, and corollary discharge related signal that reach the dorsal stream visual areas and update spatial representations in it, with examples including the update of representations made for example by eye movements described here, and by vestibular signals (Avila, Lakshminarasimhan, DeAngelis, & Angelaki, ; Chen et al, ). Furthermore, in virtual reality, some macaque hippocampal neurons can respond to a view location toward which eye movements are made even before the view has actually appeared on the screen (Wirth et al, ).…”

Robust vestibular self-motion signals in macaque posterior cingulate region

“…To date, robust vestibular and visual signals related with self-motion have been discovered in numerous cortical areas including the dorsal part of medial superior temporal sulcus (MSTd) ( Duffy and Wurtz, 1997 ; Page and Duffy, 2003 ; Gu et al, 2006 ), the ventral intraparietal area (VIP) ( Bremmer et al, 1999 ; Bremmer et al, 2002 ; Zhang and Britten, 2004 ; Chen et al, 2011a ; Chen et al, 2011b ), the visual posterior sylvian area (VPS) ( Chen et al, 2011c ), parietal insular vestibular cortex (PIVC) ( Grüsser et al, 1990a , Grüsser et al, 1990b ; Chen et al, 2010 ; Chen et al, 2011b ), the smooth eye movement of the frontal eye field (FEFsem) ( Gu et al, 2016 ), and 7a ( Avila et al, 2019 ), composing a network ( Guldin and Grüsser, 1998 ; Britten, 2008 ; Cheng and Gu, 2018 ; Gu, 2018 ). However, most of these areas (except for 7a) have not shown direct connections with the hippocampal navigation system.…”

Sensory Input Modulates Microsaccades during Heading Perception

“…Since then, many studies have investigated, both on animal and human models, the cortical and subcortical mechanisms responsible for heading perception. In macaques, several studies have shown precise neuronal selectivity to optic flow stimuli [ 4 , 5 , 6 , 7 , 8 , 9 ], to the interaction between optic flow and ocular position [ 10 , 11 , 12 , 13 ], and to the interaction between optic flow and other sensory signals [ 14 , 15 , 16 ]. In humans, several studies have shown that specific optic flow stimuli are important for guiding locomotion [ 17 , 18 , 19 , 20 ] and for the postural control [ 21 , 22 , 23 , 24 , 25 ].…”