Cortical Mechanisms of Multisensory Linear Self-motion Perception

Abstract

Accurate self-motion perception, which is critical for organisms to survive, is a process involving multiple sensory cues. The two most powerful cues are visual (optic flow) and vestibular (inertial motion). Psychophysical studies have indicated that humans and nonhuman primates integrate the two cues to improve the estimation of self-motion direction, often in a statistically Bayesian-optimal way. In the last decade, single-unit recordings in awake, behaving animals have provided valuable neurophysiological data with a high spatial and temporal resolution, giving insight into possible neural mechanisms underlying multisensory self-motion perception. Here, we review these findings, along with new evidence from the most recent studies focusing on the temporal dynamics of signals in different modalities. We show that, in light of new data, conventional thoughts about the cortical mechanisms underlying visuo-vestibular integration for linear self-motion are challenged. We propose that different temporal component signals may mediate different functions, a possibility that requires future studies.

Visuo-vestibular heading perception: a model system to study multi-sensory decision making

“…The behavioural data were well fitted by the above-mentioned extended DDM with temporally changing reliabilities, suggesting that humans are able to accumulate evidence optimally across time as well as modalities. In addition, this study also implies that any temporal misalignment of the two pieces of sensory evidence may result in apparently non-optimal integration [70].…”

“…This may be addressed by simultaneously targeting each sensory area and the decision-related areas to figure out how different heading signals are propagated through the circuit, by using analysis such as spike-field correlation [133]. Third, based on the neural-activity causal manipulation and the temporal-offset manipulation experiment results, we speculate that the vestibular velocity signals in MSTd may contribute to some other self-motion variables such as velocity or distance perception [70]. Future studies need to be conducted to test these hypotheses to further identify the exact functions of MSTd.…”

Vestibular-derived internal models in active self-motion estimation

“…One explanation of these findings is that participants built an internal model of the steering dynamics, which transforms the steering motor commands into predicted vestibular feedback, that they continued to update throughout the experiment based on the vestibular feedback (Brooks et al ., 2015; van Helvert et al ., 2022). Another explanation is that participants simply relied on path integration mechanisms (Loomis et al ., 1993; Lappe et al ., 2007; Zhou & Gu, 2023), estimating their location relative to the target by integrating the vestibular information over time without building an internal model of the steering dynamics. In the present study we aim to distinguish between these two explanations (internal model versus path integration), taking inspiration from studies on the adaptation of reaching movements.…”

Temporal and spatial properties of vestibular signals for perception of self-motion

“…We have previously summarized the findings in a series of reviews. For example, some earlier reviews focus on vestibular coding of self-motion signals [For reviews, see Cheng and Gu ( 11 ), which presents vestibular signals in the perception of translation, curve motion and distance in details; ( 12 ), which primarily introduces tuning properties in self-motion areas; ( 34 ), which focuses on multisensory integration]. Compared to the previous reviews, here we summarize the current understanding of the tuning properties of vestibular signals in these areas during self-motion and discusses the outstanding questions regarding how the brain integrates vestibular and visual cues to perceive heading direction.…”

“…Result from the temporal offset manipulation experiment could also fit into the causal inference model ( 34 ). In particular, the brain still integrates the vestibular and visual signals when the two stimuli inputs are offset within a small amount (e.g., <500 ms), as reflected by the reduced psychophysical threshold compared to the condition when no offset is introduced.…”