Robust vestibular self-motion signals in macaque posterior cingulate region.

Bingyu Liu,Qingyang Tian,Yong Gu

doi:10.7554/elife.64569

Abstract

Self-motion signals, distributed ubiquitously across parietal-temporal lobes, propagate to limbic hippocampal system for vector-based navigation via hubs including posterior cingulate cortex (PCC) and retrosplenial cortex (RSC). Although numerous studies have indicated posterior cingulate areas are involved in spatial tasks, it is unclear how their neurons represent self-motion signals. Providing translation and rotation stimuli to macaques on a 6-degree-of-freedom motion platform, we discovered robust vestibular responses in PCC. A combined three-dimensional spatiotemporal model captured data well and revealed multiple temporal components including velocity, acceleration, jerk, and position. Compared to PCC, RSC contained moderate vestibular temporal modulations and lacked significant spatial tuning. Visual self-motion signals were much weaker in both regions compared to the vestibular signals. We conclude that macaque posterior cingulate region carries vestibular-dominant self-motion signals with plentiful temporal components that could be useful for path integration.

Highlights

By recording spiking activities from these areas in macaques during passive physical motions, we provided solid evidence showing that majority of posterior cingulate cortex (PCC) neurons (~2/3), and a modest proportion (~1/3) of retrosplenial cortex (RSC) neurons carry robust vestibular linear translation and rotation signals originated from otolith organs and semicircular canals, respectively
A combined 3D spatiotemporal model captured PCC data well and revealed multiple temporal components that could be useful for estimation of instantaneous heading direction or head direction
These properties are consistent with the view that posterior cingulate region may serve as an important hub mediating self-motion related signals propagated from parietal-temporal lobes to hippocampal system for path integration during vector-based spatial navigation (Rushworth et al, 2006; Vincent et al, 2010; Kravitz et al, 2011)

Summary

Introduction

Posterior cingulate region may be one important hub mediating the propagation of self-motion signals from parietal-temporal cortices to the hippocampal-entorhinal system. Supporting this notion, numerous studies have provided evidence showing that posterior cingulate region is involved in spatial navigation. We recorded single unit activities in both subregions in the posterior region of the cingulate cortex under linear translation and angular rotation conditions

Results

Discussion

Materials and methods