Gravity Influences Top-Down Signals in Visual Processing

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.