How Visual Is the Visual Cortex? Comparing Connectional and Functional Fingerprints between Congenitally Blind and Sighted Individuals

Abstract

Classical animal visual deprivation studies and human neuroimaging studies have shown that visual experience plays a critical role in shaping the functionality and connectivity of the visual cortex. Interestingly, recent studies have additionally reported circumscribed regions in the visual cortex in which functional selectivity was remarkably similar in individuals with and without visual experience. Here, by directly comparing resting-state and task-based fMRI data in congenitally blind and sighted human subjects, we obtained large-scale continuous maps of the degree to which connectional and functional "fingerprints" of ventral visual cortex depend on visual experience. We found a close agreement between connectional and functional maps, pointing to a strong interdependence of connectivity and function. Visual experience (or the absence thereof) had a pronounced effect on the resting-state connectivity and functional response profile of occipital cortex and the posterior lateral fusiform gyrus. By contrast, connectional and functional fingerprints in the anterior medial and posterior lateral parts of the ventral visual cortex were statistically indistinguishable between blind and sighted individuals. These results provide a large-scale mapping of the influence of visual experience on the development of both functional and connectivity properties of visual cortex, which serves as a basis for the formulation of new hypotheses regarding the functionality and plasticity of specific subregions.

Domain Selectivity in the Parahippocampal Gyrus Is Predicted by the Same Structural Connectivity Patterns in Blind and Sighted Individuals

“…reported that when blind subjects and sighted subjects listened to the names of large objects such as "couch" or "refrigerator" in contrast to small tools and animals, the PHG was significantly more strongly activated, and this activation overlapped well with the parahippocampal place area (Epstein and Kanwisher, 1998;Epstein, 2008). These findings were replicated in the study by Wang et al (2015) and are consistent with the findings in the study by Wolbers et al (2011), who reported that in both blind and sighted subjects, haptic exploration of Lego scenes elicited stronger activation in the PHG than did the exploration of Lego objects. We thus used the selectivity for large objects in PHG as a test case for the effect of visual experience in the mapping between white matter connectivity and regional functional preferences.…”

“…For example, the same subjects may produce different functional response profiles in a particular brain region when performing different tasks. In the current context, Wang et al (2015) showed that sighted subjects had different category response profiles in posterior lateral fusiform and inferior occipital gyrus when viewing pictures and when listening to names, indicating that different tasks can recruit different sets of connections within an identical white matter background.…”

“…Several previous studies that examined the effect of visual deprivation on white matter structures did not observe a significant alteration of WM connectivity in PHG. When the fractional anisotropy of the white matter was compared between sighted and blind adults across the whole brain, a significant decrease in fractional anisotropy associated with blindness was only observed for the geniculocalcarine tract (Shu et al, 2009a;Wang et al, 2013). Shu et al (2009b) compared multiple white matter network properties between early blind and sighted control subjects and observed plastic changes only in the primary systems, with reduced connectivity strength and communication efficiency in the primary visual cortex and increased connectivity strength and efficiency in the primary motor and somatosensory areas.…”

Sensorimotor-independent development of hands and tools selectivity in the visual cortex

“…These include the anterior intraparietal area [involved, among other tasks, in producing accurate grip (41)(42)(43)] and the ventral premotor cortex (44)(45)(46). Furthermore, the fact that similar tool-selective and body-selective responses have been found in the same part of the occipito-temporal cortex in individuals deprived of visual experience from birth (32,33,47,48), invites the inference that, because vision is not necessary for developing theses preferences, the burden for shaping this region's functional specialization is carried by motor experience. Our finding, however, calls for a reexamination of this experience-based account.…”

“…Still, to account for the topographic arrangement of the hand and tool specialization, we would need to assume that the region in question is preferentially disposed to encode information about those object categories independently of a specific type of sensory input. This would, in turn, suggest that the nature of representations in this region would need to be of a form that is accessible through different modalities, including written words (48), haptic stimulation (49,50), or sensory-substitution-based audition (51), and that they be independent from low-level effectorbound motor properties and experience, such that they develop normally in individuals with atypical bodies, as in the dysplasics.…”