Emergent visual creativity in frontotemporal dementia is associated with dorsomedial visual cortex enhancement

IMPORTANCEThe neurological substrates of visual creativity are unknown. We demonstrate the role of dorsomedial visual cortex in emergence of visual artistic creativity (VAC) in the setting of dementia. Our findings illuminate neural substrates of human creativity and suggest that hyperactivation of specific brain areas may manifest as enhanced cognitive or behavioral capacities. OBJECTIVETo determine the anatomical and physiological underpinnings of VAC in dementia. DESIGN, SETTING, AND PARTICIPANTSAs part of a prospective, longitudinal cohort study focused on frontotemporal dementia (FTD), 734 patients met research criteria for an FTD spectrum disorder between 2002 and 2019. Of these, seventeen showed emergence of visual artistic creativity (VAC-FTD). Two control groups (n = 51 each) were matched to VAC-FTD based on demographic and clinical parameters: (1) Not Visually Artistic FTD (NVA-FTD) and (2) Healthy Controls (HC). MAIN OUTCOMES AND MEASURESClinical, neuropsychological, genetic and neuroimaging data were analyzed to characterize VAC-FTD and compare VAC-FTD to control groups. RESULTSEmergence of VAC occurred around the time of onset of symptoms, and was disproportionately seen in patients with temporal lobe predominant degeneration (n = 8/17). Atrophy network mapping identified a dorsomedial occipital region whose activity inversely correlated, in healthy brains, with activity in the patient-specific atrophy patterns in VAC-FTD (n = 17/17) and NVA-FTD (n = 45/51). Structural covariance analysis revealed that volume of this dorsal occipital region was strongly correlated, in VAC-FTD, but not in NVA-FTD or HC, with a volume in the primary motor cortex corresponding to the right hand representation. One patient, who underwent fluorodeoxyglucose positron emission tomography before and after VAC onset, showed increasing glucose metabolism in the dorsal occipital region over the interval when creativity emerged. CONCLUSIONS AND RELEVANCEFTD lesion-induced intensification of dorsal visual association cortex structure and function predisposes to emergence of VAC in certain environmental or genetic conditions. Paradoxical gains of function are early manifestations of neurodegenerative disease, and this study delineates a specific brain region associated with the emergence of VAC.