A brief exposure to rightward prismatic adaptation changes resting-state network characteristics of the ventral attentional system

Gudmundsson, Louis; Vohryzek, Jakub; Fornari, Eleonora; Clarke, Stéphanie; Hagmann, Patric; Crottaz-Herbette, Sonia

doi:10.1371/journal.pone.0234382

Cited by 5 publications

(9 citation statements)

References 84 publications

(141 reference statements)

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“…To that end, we generated similar connectivity matrices from our previously published data, in which resting state fMRI was collected before and after a brief exposure to rightward-shifting PA goggles (see Wilf et al. 2019 ; Gudmundsson et al. 2020 for details).…”

Section: Resultsmentioning

confidence: 99%

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

Wilf

Dupuis²,

Nardo

et al. 2022

Cerebral Cortex

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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 behavior and associated brain modulations is challenging. Here, we tackled this question implementing a prism adaptation-like training in virtual reality (VRPA) in combination with functional neuroimaging. Three groups of healthy participants (N = 45) underwent VRPA (with a shift either to the left/right side, or with no shift), and performed functional magnetic resonance imaging (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 attentional and default mode (DMN)/fronto-parietal networks, only for the adaptation groups, more pronouncedly in the hemisphere contralateral to the induced shift. In addition, VRPA was found to bias visual responses to naturalistic videos: Following rightward adaptation, we found upregulation of visual response in an area in the parieto-occipital sulcus (POS) only in the right hemisphere. Notably, the extent of POS upregulation correlated with the size of the VRPA-induced after-effect measured in behavioral tests. This study demonstrates that a brief VRPA exposure can change large-scale cortical connectivity and correspondingly bias visual responses to naturalistic sensory inputs.

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Section: Resultsmentioning

confidence: 99%

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

Wilf

Dupuis²,

Nardo

et al. 2022

Cerebral Cortex

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“…Our finding of an enhanced decoupling between DMN/FPN regions and dorsal and ventral attentional networks after VRPA (see Figure 3b ), more pronounced in the hemisphere contralateral to the shift, is consistent with recent studies that measured standard PA aftereffects in resting state connectivity (Schintu et al ., 2019; Tsujimoto et al ., 2019; Wilf et al ., 2019; Gudmundsson et al ., 2020). We suggest that the bottom-up learning process during adaptation eventually propagates forward in the processing pathway to affect high-level, heteromodal, cortical networks.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies show that the aftereffects of PA manifest also in brain activity as changes in activation of the inferior-parietal lobule (IPL; Crottaz-Herbette et al ., 2014; Crottaz-Herbette et al ., 2017b), a key area at the intersection between the attentional networks and the DMN. In addition to its effect on task-induced activation, PA has been recently found to modulate task-free resting-state connectivity, inducing enhanced decoupling between the attentional networks and the DMN (Wilf et al ., 2019) or a modulation of the right/left fronto-parietal networks (Schintu et al ., 2019; Tsujimoto et al ., 2019; Gudmundsson et al ., 2020; see Panico et al ., 2020 for review).…”

Section: Introductionmentioning

confidence: 99%

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

Wilf

Dupuis²,

Nardo

et al. 2021

Preprint

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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.

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“…In a first study, global connectivity analysis revealed significant decreases in functional connectivity of nodes within left IPL and left insula as well as bilaterally within the medial prefrontal cortex, revealing a reduction of the connectivity between the Default Mode Network and the attentional network ( Wilf et al, 2019 ). In a second study, whole brain analysis using the graph theory approach revealed a decrease in connectivity strength and in local efficiency in VAN, but not DAN ( Gudmundsson et al, 2020 ). A third study carried out seed-based correlation analysis within the attentional network before and after a brief exposure to R-PA, without a control group ( Tsujimoto et al, 2019 ).…”

Section: Prism-induced Topographical Mismatch Reshuffles Spatial Repr...mentioning

confidence: 95%

Choosing Sides: Impact of Prismatic Adaptation on the Lateralization of the Attentional System

Clarke

Farron²,

Crottaz-Herbette³

2022

Front. Psychol.

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Seminal studies revealed differences between the effect of adaptation to left- vs. right-deviating prisms (L-PA, R-PA) in normal subjects. Whereas L-PA leads to neglect-like shift in attention, demonstrated in numerous visuo-spatial and cognitive tasks, R-PA has only minor effects in specific aspects of a few tasks. The paucity of R-PA effects in normal subjects contrasts with the striking alleviation of neglect symptoms in patients with right hemispheric lesions. Current evidence from activation studies in normal subjects highlights the contribution of regions involved in visuo-motor control during prism exposure and a reorganization of spatial representations within the ventral attentional network (VAN) after the adaptation. The latter depends on the orientation of prisms used. R-PA leads to enhancement of the ipsilateral visual and auditory space within the left inferior parietal lobule (IPL), switching thus the dominance of VAN from the right to the left hemisphere. L-PA leads to enhancement of the ipsilateral space in right IPL, emphasizing thus the right hemispheric dominance of VAN. Similar reshaping has been demonstrated in patients. We propose here a model, which offers a parsimonious explanation of the effect of L-PA and R-PA both in normal subjects and in patients with hemispheric lesions. The model posits that prismatic adaptation induces instability in the synaptic organization of the visuo-motor system, which spreads to the VAN. The effect is lateralized, depending on the side of prism deviation. Successful pointing with prisms implies reaching into the space contralateral, and not ipsilateral, to the direction of prism deviation. Thus, in the hemisphere contralateral to prism deviation, reach-related neural activity decreases, leading to instability of the synaptic organization, which induces a reshuffling of spatial representations in IPL. Although reshuffled spatial representations in IPL may be functionally relevant, they are most likely less efficient than regular representations and may thus cause partial dysfunction. The former explains, e.g., the alleviation of neglect symptoms after R-PA in patients with right hemispheric lesions, the latter the occurrence of neglect-like symptoms in normal subjects after L-PA. Thus, opting for R- vs. L-PA means choosing the side of major IPL reshuffling, which leads to its partial dysfunction in normal subjects and to recruitment of alternative or enhanced spatial representations in patients with hemispheric lesions.

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A brief exposure to rightward prismatic adaptation changes resting-state network characteristics of the ventral attentional system

Cited by 5 publications

References 84 publications

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

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

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

Choosing Sides: Impact of Prismatic Adaptation on the Lateralization of the Attentional System

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