Virtual reality-based sensorimotor adaptation shapes subsequent spontaneous and naturalistic stimulus-driven brain activity

Abstract

Our everyday life summons numerous novel sensorimotor experiences, to which our brain needs to adapt in order to function properly. However, tracking plasticity of naturalistic behaviour and associated brain modulations is challenging. Here we tackled this question implementing a prism adaptation training in virtual reality (VRPA) in combination with functional neuroimaging. Three groups of healthy participants (N=45) underwent VRPA (with a spatial shift either to the left/right side, or with no shift), and performed fMRI sessions before and after training. To capture modulations in free-flowing, task-free brain activity, the fMRI sessions included resting state and free viewing of naturalistic videos. We found significant decreases in spontaneous functional connectivity between large-scale cortical networks – namely attentional and default mode/fronto-parietal networks - only for adaptation groups. Additionally, VRPA was found to bias visual representations of naturalistic videos, as following rightward adaptation, we found upregulation of visual response in an area in the parieto-occipital sulcus (POS) in the right hemisphere. Notably, the extent of POS upregulation correlated with the size of the VRPA induced after-effect measured in behavioural tests. This study demonstrates that a brief VRPA exposure is able to change large-scale cortical connectivity and correspondingly bias the representation of naturalistic sensory inputs. Significance statement In the current work, we tested how a brief sensorimotor experience changes subsequent brain activity and connectivity. Using virtual reality (VR) as a tool for sensorimotor training opens a window for creating otherwise impossible sensory experiences and sensorimotor interactions. Specifically, we studied how VR adaptation training in ecological conditions modulates spontaneous functional connectivity and brain representation of naturalistic real-life-like stimuli. Previous adaptation studies used artificial, lab-designed setups both during adaptation and while measuring subsequent aftereffects. Testing brain response while observing naturalistic stimuli and in resting state allowed us to stay as close as possible to naturalistic real-life-like conditions, not confounded by performance during a task. The current work demonstrates how rapid changes in free-flowing brain activity and connectivity occur following short-term VR visuomotor adaptation training in healthy individuals. Moreover, we found a link between sensory responses to naturalistic stimuli and adaptation-induced behavioural aftereffect, thus demonstrating a common source of training-induced spatial recalibration, which affects both behaviour and brain representations of naturalistic stimuli. These findings might have meaningful implications both for understanding the mechanisms underlying visuomotor plasticity in healthy individuals and for using VR adaptation training as a tool for rehabilitating brain-damaged patients suffering from deficits in spatial representation.