Brain functional and effective connectivity in response to optic and tactile flow perception in sighted and congenitally blind individuals

During the research program of my Doctorate Course, we investigated whether the visual hMT+ complex may plays a role in the supramodal representation of sensory flow, not mediated by visual mental imagery. We used functional magnetic resonance imaging to measure neural activity in sighted and congenitally blind individuals during passive perception of optic and tactile flows to determine the role of visual experience in the development of the functional organization of the hMT complex. Visual motion-responsive cortex, including hMT+, was identified in the lateral occipital and inferior temporal cortices of the sighted subjects by response to optic flow. Tactile flow perception in sighted subjects activated the more anterior part of these cortical regions but deactivated the more posterior part. By contrast, perception of tactile flow in blind subjects activated the full extent, including the more posterior part. These results demonstrate that activation of hMT+ and surrounding cortex by tactile flow is not mediated by visual mental imagery and that the functional organization of hMT+ can develop to subserve tactile flow perception in the absence of any visual experience. Moreover, visual experience leads to a segregation of the motion-responsive occipito-temporal cortex into an anterior "supramodal" subregion involved in the representation of both optic and tactile flows and a posterior "visual" subregion that processes optic flow only. To further support our hypothesis, we assessed brain regions functionally and effectively connected with the hMT+ cortex, and found a set of regions, including bilateral ventral premotor, inferior frontal and insular cortex, sensorimotor region, intraparietal and inferior parietal cortex, ventral and lateral occipital cortex, cuneus and middle and superior temporal cortex, that positively correlated with the bilateral hMT complex both in sighted and congenitally blind subjects, both for tactile and optic flow perception. These regions form a common functional connectivity network for motion processing, that is independent from the sensory modality through which the information is acquired. Interestingly, we found that in sighted subjects during tactile flow perception, the functional connectivity network obtained using the anterior "supramodal" part of the bilateral hMT complex as seed ROI is different from the network obtained using the posterior "visual" part of this area. In fact, ventral premotor, sensorimotor and posterior parietal cortex are functionally correlated with the anterior "supramodal" part of hMT+ only, but not with the posterior "visual" one. Furthermore, in blind subjects the brain network obtained with either the anterior or posterior part of the bilateral hMT complex is similar to the network identified in sighted subjects using the anterior "supramodal" part of the same area. These findings confirm that visual experience may lead to a segregation of the motion-responsive occipito-temporal cortex into an anterior subregion involved in the representation of both optic and tactile flows, and a posterior subregion that processes optic flow only. The observation of similar functional connectivity networks obtained using the bilateral hMT complex as seed ROI in both congenitally blind and sighted subjects during either optic or tactile flow perception supports the hypothesis that these visual processing areas involved in the perception of motion can manage acquired information independently from the sensory modality that carries such information to the brain (supramodality), and therefore that a previous visual experience is not necessary for the development of the hMT complex functional organization. We additionally explored the functional connectivity between the primary sensorimotor cortex and the ipsi- or contro-lateral hMT complex. Our results demonstrated that, independently from the side of tactile stimulation and from the brain hemisphere, the primary sensorimotor cortex seed showed a stronger functional connection with the ipsilateral rather than with the controlateral hMT complex. This effect is significantly greater in sighted than in blind participants. These findings demonstrated the existence of a bilateral functional connection between the primary sensorimotor cortex and the hMT complex and also proved that the motion information processing in the human brain, mainly in sighted subjects, is basically ipsilateral. As a last step, we also performed an effective connectivity analyses in order to identify a possible connection network among the several circuitries involved in the supramodal motion processing, and to evaluate the effect of the two formats (visual and tactile) of stimulation on the strengths of the connections between the regions involved in motion processing. A preliminary analysis of the effective connectivity results in both sighted and congenitally blind individuals suggests that most of the tactile information is "transferred" to the extrastriate regions for motion processing mainly through a thalamic pathway, and in part through a posterior parietal stream, that appears particularly more manifest in blind subjects. Moreover, this tactile motion processing network correlates also with primary visual regions in both groups. In sighted subjects, a reciprocal connections between the anterior and the posterior part of the hMT complex (aMT, pMT) is significantly found for both for tactile and visual stimulation, and is stronger in the left than in the right brain hemisphere. As future developments, further functional and effective connectivity analyses are needed to better comprehend and identify the possible connection networks involved in the supramodal motion processing, independent from the sensory modality through which the information is acquired and to better understand the role of the thalamus in the processing of moving stimuli