Abstract

Visual perception is not only based on incoming visual signals but also on information about a multimodal reference frame that incorporates vestibulo-proprioceptive input and motor signals. In addition, top-down modulation of visual processing has previously been demonstrated during cognitive operations including selective attention and working memory tasks. In the absence of a stable gravitational reference, the updating of salient stimuli becomes crucial for successful visuo-spatial behavior by humans in weightlessness. Here we found that visually-evoked potentials triggered by the image of a tunnel just prior to an impending 3D movement in a virtual navigation task were altered in weightlessness aboard the International Space Station, while those evoked by a classical 2D-checkerboard were not. Specifically, the analysis of event-related spectral perturbations and inter-trial phase coherency of these EEG signals recorded in the frontal and occipital areas showed that phase-locking of theta-alpha oscillations was suppressed in weightlessness, but only for the 3D tunnel image. Moreover, analysis of the phase of the coherency demonstrated the existence on Earth of a directional flux in the EEG signals from the frontal to the occipital areas mediating a top-down modulation during the presentation of the image of the 3D tunnel. In weightlessness, this fronto-occipital, top-down control was transformed into a diverging flux from the central areas toward the frontal and occipital areas. These results demonstrate that gravity-related sensory inputs modulate primary visual areas depending on the affordances of the visual scene.

Highlights

  • Gravity plays a crucial role in building a neural representation of physical space [1,2,3]

  • Basic visual evoked potentials (VEPs) responses induced by a checkerboardreversal pattern and the related theta-alpha phase locking were preserved in weightlessness

  • VEPs triggered by the presentation of a virtual 3D tunnel, and sustained by a thetaalpha phase locking and a fronto-occipital directional flux on Earth, were, dramatically perturbed in weightlessness

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Summary

Introduction

Gravity plays a crucial role in building a neural representation of physical space [1,2,3]. This region participates in a network that is activated by visual motion and by vestibular stimulation This ‘‘vestibular network’’ is composed of the temporo-parietal junction, the cingulate cortex, the ventral premotor area, the supplementary motor area, the middle and post-central gyrus, the posterior thalamus and the putamen [1,6,7]. It has been demonstrated [2] that this network is involved in processing visual motion when it is coherent with natural gravity, supporting the hypothesis that the fundamental physical constraint of Earth’s gravity is internalized by the human brain [8]

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