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Functional specificity is a core principle of human brain organization, as revealed by highly anatomically atypical brains

Poster B29 in Poster Session B, Friday, October 25, 10:00 - 11:30 am, Great Hall 4

Hope* Kean1, Agata* Wolna1, Niharika Jhingan1, Sara Swords1, Alan Shewmon2, Mark Richardson3,4, Evelina Fedorenko1; 1MIT, 2UCLA Medical School, 3Department of Neurological Surgery, University of Pittsburgh, 4Massachusetts General Hospital

The human brain contains many areas and networks of areas that show a high degree of selectivity for particular inputs (Kanwisher 2010). However, it is unclear to what extent functional specialization is a core principle of human brain organization, or whether other brain architectures could also support typical-like cognition. We investigate this question by studying individuals who were born or grew up with atypical brains but have intact, typical-like cognition. Unlike cases of adult-onset brain damage, usually associated with cognitive difficulties, many cases of early tissue damage (due to presumed prenatal or perinatal stroke) or tissue displacement (due to cysts and hydrocephalus) are characterized by intact cognition (e.g., Tuckute et al., 2022; Newport et al. 2017). Given that functional specialization is a spatial luxury, we ask whether different perceptual and cognitive functions remain segregated in the presence of severe spatial constraints. We tested a group of individuals (n=21) with brain cysts ranging in size from 5g (a teaspoon) to 258g (a large grapefruit), with an average size of 63g (a lemon) resulting in significant brain tissue reduction (up to 7%; with cysts taking up to 21% of the whole brain volume (mean = 6,17%)), along with a set of age-matched neurotypical controls (n=30). Each participant completed a wide range of ‘localizer’ tasks while undergoing fMRI, along with a comprehensive set of cognitive behavioral assessments. We focused on parts of the brain where different specialized areas are located in close proximity, which should make it most likely that some spatial overlap would be observed in cases of insufficient space. In particular, we examined functional specificity in the i) ventral visual pathway, focusing on face-, body-, and scene-selective areas (Pitcher et et al., 2011); ii) superior temporal sulcus and adjacent cortex, focusing on areas selective for dynamic faces, interacting bodies, and theory of mind (Pitcher et al., 2011; Deen et al., 2015; Isik, Koldewyn et al., 2017; Saxe & Kanwisher, 2003); iii) lateral frontal cortex, focusing on areas selective for language vs. domain-general areas of the Multiple Demand network (Fedorenko et al., 2010; Fedorenko et al., 2013; Braga et al., 2020); iv) medial frontal cortex, focusing on areas selective for theory-of-mind and domain-general areas of the Multiple Demand network (Saxe & Kanwisher, 2003; Saxe et al., 2006; Fedorenko et al., 2013); and v) lateral temporo-parietal cortex, focusing on areas selective for language and theory-of-mind (Fedorenko et al., 2010; Saxe & Kanwisher, 2003; Shain et al., 2022). Our results show that despite substantial reduction in brain tissue, these participants show the same degree of functional specificity as controls, as evidenced in both i) the magnitudes of response to the preferred vs. non-preferred stimuli, and ii) the degree of spatial overlap between the relevant areas. In other words, even when space is scarce, different perceptual and functional systems remain robustly segregated. Thus, functional specialization appears to be a hard constraint on brain organization, presumably for reasons of computational and metabolic efficiency as has been much discussed over the years (e.g., Chlovski & Koulakov, 2004).

Topic Areas: Disorders: Developmental, Language Development/Acquisition

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