Distributed Representation of Curvilinear Self-Motion in the Macaque Parietal Cortex

Abstract

Information about translations and rotations of the body is critical for complex self-motion perception during spatial navigation. However, little is known about the nature and function of their convergence in the cortex. We measured neural activity in multiple areas in the macaque parietal cortex in response to three different types of body motion applied through a motion platform: translation, rotation, and combined stimuli, i.e., curvilinear motion. We found a continuous representation of motion types in each area. In contrast to single-modality cells preferring either translation-only or rotation-only stimuli, convergent cells tend to be optimally tuned to curvilinear motion. A weighted summation model captured the data well, suggesting that translation and rotation signals are integrated subadditively in the cortex. Interestingly, variation in the activity of convergent cells parallels behavioral outputs reported in human psychophysical experiments. We conclude that representation of curvilinear self-motion perception is widely distributed in the primate sensory cortex.

Visual–vestibular estimation of the body's curvilinear motion through the world: A computational model

“…There is also some existing psychophysical evidence pointing to changes in curvilinear path estimation when a brief pure forward-translation vestibular signal occurs (Bertin & Berthoz, 2004), and electrophysiological evidence that curvilinear-sensitive neurons in the primate brain respond differently when forward motion occurs concurrently with the rotation (Z. Cheng & Gu, 2016). I have tested the model with and without this additional heading constraint and found that it does not have a large effect on the performance characteristics for the simulations I have reported in this article.…”

“…Many animals, including humans and nonhuman primates, have a vestibular system made up of the otoliths and semicircular canals to convey information about rotation and acceleration of the head relative to gravity (Angelaki & Cullen, 2008;Goldberg et al, 2012;Howard, 1982;Imai, Moore, Raphan, & Cohen, 2001). While there are countless studies on the vestibular system in general, unfortunately there is a relative paucity of research on human or nonhuman primate vestibular responses during curvilinear selfmotion, because the experiments require mobile robots (Bertin & Berthoz, 2004;Bertin & Israel, 2005;Ivanenko, Grasso, Israel, & Berthoz, 1997) or large (and expensive) moving-base simulators to measure sensitivity correctly (Chen, DeAngelis, & Angelaki, 2011;Z. Cheng & Gu, 2016;Crane, 2014;Gu et al, 2006;MacNeilage, Turner, & Angelaki, 2010;Nooij, Nesti, Bulthoff, & Pretto, 2016;Takahashi et al, 2007).…”

“…We have previously suggested a scheme in which parts of the heading template maps (see Figure 2b) are inhibited depending on extraretinal signals (Perrone & Stone, 1994), but the details of how this might occur were never specified. Since that time, many more experiments have been carried out examining the neural signals in the primate visual system during combined visual-vestibular movement throughout a number of visual areas (Chen et al, 2011;Z. Cheng & Gu, 2016;Gu et al, 2006;Takahashi et al, 2007).…”

Sensorimotor basis of motor vehicle control

“…A recent study has found that certain neurons in the primate (i.e. monkeys) cortex have the largest response for curvilinear motion with both translation and rotation (Cheng and Gu 2016). In Study 4, where a real vehicle and a large test ground were used, the results clearly indicate that participants significantly changed their steering behaviour ---that they conducted a largely accurate lane change manoeuvre.…”

“…does it have to be directional signal above a certain threshold, or would jerks during steering suffice? A recent study done by Cheng and Gu (2016) may shed light on this topic. They found that it is the curvilinear motion (translation with rotation) that significantly activates the vestibular system, compared with translation or rotation only.…”