The present study reports alterations of task-based functional brain connectivity in a group of 11 cosmonauts after a long-duration spaceflight, compared to a healthy control group not involved in the space program. To elicit the postural and locomotor sensorimotor mechanisms that are usually most significantly impaired when space travelers return to Earth, a plantar stimulation paradigm was used in a block design fMRI study. The motor control system activated by the plantar stimulation involved the pre-central and post-central gyri, SMA, SII/operculum, and, to a lesser degree, the insular cortex and cerebellum. While no post-flight alterations were observed in terms of activation, the network-based statistics approach revealed task-specific functional connectivity modifications within a broader set of regions involving the activation sites along with other parts of the sensorimotor neural network and the visual, proprioceptive, and vestibular systems. The most notable findings included a post-flight increase in the stimulation-specific connectivity of the right posterior supramarginal gyrus with the rest of the brain; a strengthening of connections between the left and right insulae; decreased connectivity of the vestibular nuclei, right inferior parietal cortex (BA40) and cerebellum with areas associated with motor, visual, vestibular, and proprioception functions; and decreased coupling of the cerebellum with the visual cortex and the right inferior parietal cortex. The severity of space motion sickness symptoms was found to correlate with a post- to pre-flight difference in connectivity between the right supramarginal gyrus and the left anterior insula. Due to the complex nature and rapid dynamics of adaptation to gravity alterations, the post-flight findings might be attributed to both the long-term microgravity exposure and to the readaptation to Earth’s gravity that took place between the landing and post-flight MRI session. Nevertheless, the results have implications for the multisensory reweighting and gravitational motor system theories, generating hypotheses to be tested in future research.

The information coming from the vestibular otolith organs is important for the brain when reflexively making appropriate visual and spinal corrections to maintain balance. Symptoms related to failed balance control and navigation are commonly observed in astronauts returning from space. To investigate the effect of microgravity exposure on the otoliths, we studied the otolith-mediated responses elicited by centrifugation in a group of 25 astronauts before and after 6 mo of spaceflight. Ocular counterrolling (OCR) is an otolith-driven reflex that is sensitive to head tilt with regard to gravity and tilts of the gravito-inertial acceleration vector during centrifugation. When comparing pre- and postflight OCR, we found a statistically significant decrease of the OCR response upon return. Nine days after return, the OCR was back at preflight level, indicating a full recovery. Our large study sample allows for more general physiological conclusions about the effect of prolonged microgravity on the otolith system. A deconditioned otolith system is thought to be the cause of several of the negative effects seen in returning astronauts, such as spatial disorientation and orthostatic intolerance. This knowledge should be taken into account for future long-term space missions.

Prolonged exposure to microgravity considerably affects all forms of visual tracking. Revealed disturbances in precision of visual tracking and adoption of the new tracking strategy substantially prolong (up to 2-3 times) the period required to acquire, recognize, and to fixate gaze on the target.

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