Contrary neuronal recalibration in different multisensory cortical areas

Abstract

AbstractThe adult brain demonstrates remarkable multisensory plasticity by dynamically recalibrating information from multiple sensory sources. When a systematic visual-vestibular heading offset is experienced, the unisensory perceptual estimates recalibrate toward each other (in opposite directions) to reduce the conflict. The neural substrate of this recalibration is unknown. Here, we recorded single-neuron activity from the dorsal medial superior temporal (MSTd), parieto-insular vestibular cortex (PIVC), and ventral intraparietal (VIP) areas in three male rhesus macaques during visual-vestibular recalibration. Both visual and vestibular tuning in MSTd recalibrated-each according to their respective cues’ perceptual shifts. Vestibular tuning in PIVC also recalibrated together with corresponding perceptual shifts (cells were not visually tuned). By contrast, VIP neurons demonstrated a unique phenomenon: both vestibular and visual tuning recalibrated according to vestibular perceptual shifts. Such that, visual tuning shifted, surprisingly, contrary to visual perceptual shifts. Therefore, while unsupervised recalibration (to reduce cue conflict) occurs in early multisensory cortices, higher-level VIP reflects only a global shift, in vestibular space.In Brief:The neural bases of multisensory plasticity are currently unknown. Here, Zeng et al. studied neuronal recalibration to a systematic visual-vestibular cue conflict. In multisensory cortical areas MSTd and PIVC, single-unit responses to visual and vestibular stimuli recalibrated to reduce the cue conflict, along with their respective unisensory perceptual shifts. By contrast, in higher-level VIP, both visual and vestibular neuronal responses recalibrated with vestibular perceptual shifts. This led to a surprising recalibration of visual responses opposite in direction to visual perceptual shifts. This exposes differential aspects of multisensory plasticity across multisensory cortical areas, and reveals a novel hybrid of visual responses within a vestibular reference frame in parietal neurons.HighlightsIn the presence of a systematic heading conflict, visual and vestibular cues recalibrate towards one another to reduce the conflict.In MSTd, neuronal responses to vestibular and visual cues recalibrated, each according to their respective cues’ perceptual shifts.In PIVC, vestibular responses recalibrated according to vestibular perceptual shifts (cells were not visually tuned).In VIP, neuronal responses to both vestibular and visual cues recalibrated together with vestibular perceptual shifts (opposite in direction to visual perceptual shifts).Profound differences in neuronal recalibration expose different functions across multisensory cortical areas.