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Naturalistic stimulation in sensory-deprived individuals reveals overlapping large-scale brain organization with differential cross-modal mechanisms

Setti, Francesca (2020) Naturalistic stimulation in sensory-deprived individuals reveals overlapping large-scale brain organization with differential cross-modal mechanisms. Advisor: Ricciardi, Prof. Emiliano. Coadvisor: Handjaras, Dr. Giacomo . pp. 188. [IMT PhD Thesis]

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Animal and human sensory-deprived models offer the possibility to study the causal mechanisms implicated in perceptual processing and knowledge organization and investigate how the brain copes with the absence of modality dependent information. Congenital blindness and deafness represent unique tools to comprehend to what extent (the lack of) a specific sensory input is a necessary condition for the morpho-functional development of both early sensory and higher-level brain regions. Accumulated evidence from animal studies and comparative works in humans with congenital/early sensory loss has reliably described major general tenets: preservation of modality-independent large-scale organization with topological/regional task selectivity, and crossmodal, modality-dependent plasticity phenomena. Indeed, whilst on one hand the large-scale architecture of the brain conserves task specificity, at the local level, early sensory areas deprived since birth consistently show cross-modal engagement for the information coming from spared senses (e.g. auditory and tactile stimulation for the visual cortex in congenital/early blind individuals), whereas higher level cortical regions in both the auditory and visual hierarchy are still able to represent stimulus characteristics regardless from the sensory modality conveying the information to the brain. Although robust and replicable, these findings leave open questions about the functional mechanisms underlying the observed brain reorganizations. Recently, a growing number of studies have used naturalistic stimulation in fMRI to convey complex, real-life-like perceptual and semantic information thus fulfilling the need of ecological validity and generalizability of results to daily-life perception and cognition. Indeed, contrary to traditional paradigms, that make use of simplified, artificial stimuli (static images, visual geometrical patterns or isolated sounds), the setup of naturalistic experiments consists in the usage of prolonged, complex stimulation with the aim to reflect more faithfully the dynamic structure of natural environments humans experience on a daily basis. To this regard, movies and books audiodescriptions have been widely used to convey a continuous and rich stream of information whose processing requires the concerted deployment and combination of different brain mechanisms, going from the online integration of the incoming multisensory perceptual input to more complex cognitive operations that impinge on attention, information retrieval/update and semantic knowledge. Thus, the richness of such paradigms offers the unique possibility to study brain functioning in complex settings that closely mimic everyday life experiences.My PhD research meant to provide new insights on the role of experience-dependent plasticity in shaping brain functioning in everyday life. The project was carried out through a 3T functional Magnetic Resonance Imaging (fMRI) study with the aim to evaluate and compare patterns of brain response to a prolonged naturalistic stimulus (@ 50 minutes long movie) in the early sensory areas of two models of sensory-deprivation, congenital blindness and deafness. The film One Hundred and One Dalmatians (Walt Disney, 1996) was shortened and edited (with the addition of subtitles and audio descriptions) in order to create three different versions: two unimodal conditions (i.e. auditorymovie with audiodescriptions or visual-movie complemented by subtitles) and one multimodal setting (audio-visual). Specifically, we measured brain responses in five experimental groups of participants: congenitally blind (n=9; 44±14 years), congenitally deaf (n=9, 24±4 years), and three control groups that attended the auditory (n=10, 39±17 years), visual (n=10, 37±15 years), or audiovisual (n=10, 35±13 years) variants of the movie.After standard preprocessing, we took advantage of an Inter- Subject Correlation (ISC) analysis to measure to what extent sensory deprivation affected whole-brain participants synchronization in each group separately. We then compared congenitally deaf and blind with their control groups, demonstrating wide and overlapping modality-independent responses across groups, accompanied by a less lateralized recruitment (e.g., higher ISC in the right hemisphere) in both blind and deaf individuals. Afterwards, we focused our analysis on sensory areas, showing how V1 and A1 and late regions were differently affected in the congenitally deaf and blind groups. Finally, through computational modeling, we further described in each brain region to what extent the ISC was dependent to specific stimulus characteristics, in terms of both low- (i.e., visual or auditory) and high-level (i.e., semantic) features. Results clearly indicated that V1 functional activity in blind individuals was driven by acoustic features (i.e., sound envelope), whereas the role of A1 in deaf individuals was not related to any of the low-level nor high-level stimulus descriptions explored. In this thesis, I presented the methodology and the result of the study and discussed the implications of the findings as compared to the current evidence in the literature.

Item Type: IMT PhD Thesis
Subjects: R Medicine > RC Internal medicine > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry
PhD Course: Cognitive, Computational and Social Neurosciences
Identification Number: 10.6092/imtlucca/e-theses/324
Date Deposited: 21 Dec 2020 09:13
URI: http://e-theses.imtlucca.it/id/eprint/324

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