Nature of crossmodal plasticity in the blind brain and interplay with sight restoration

Thèse réalisée en cotutelle avec l'Université catholique de Louvain.Ce travail de thèse s’est intéressé à la plasticité cérébrale associée à la privation/restauration visuelle. A travers deux études transversales utilisant l’imagerie par résonance magnétique fonctionnelle auprès d’un groupe de participants présentant une cécité congénitale ou précoce (ainsi qu’auprès d’un groupe contrôle de participants voyants), nous avons tenté de caractériser la manière dont le cortex occipital - typiquement dédié au traitement de l’information visuelle - se réorganise afin de traiter différents stimuli auditifs. Nous démontrons qu’en cas de cécité précoce, différentes régions du cortex occipital présentent une préférence fonctionnelle pour certains types de stimuli non-visuels, avec une spécialisation fonctionnelle qui respecte celle de régions typiquement impliquées dans le traitement d’informations similaires en vision. Ces découvertes constituent une avancée conceptuelle concernant le rôle joué par les contraintes intrinsèques d’une part, et par l’expérience d’autre part, dans l’émergence de réponses sensorielles et fonctionnelles du cortex occipital. D’une part, l’observation de réponses occipitales à la stimulation auditive chez le non-voyant précoce (réorganisation transmodale) rend compte de la capacité du cortex occipital à réorienter sa modalité sensorielle préférentielle en fonction de l’expérience. D’autre part, l’existence de modules cognitifs spécialisés dans le cortex occipital du non-voyant précoce, semblables à ceux du cerveau voyant, démontre les contraintes intrinsèques imposées à une telle plasticité. Dans une étude de cas longitudinale, nous avons également exploré comment les changements plastiques associés à la cécité interagissent avec une récupération visuelle partielle à l’âge adulte. Nous avons réalisé des mesures pré et post-opératoires auprès d’un patient ayant récupéré la vision, en combinant les techniques comportementales ainsi que de neuroimagerie fonctionnelle et structurelle afin d’investiguer conjointement l’évolution de la réorganisation transmodale et de la récupération des fonctions visuelles à travers le temps. Nous démontrons que les changements structurels et fonctionnels caractérisant le cortex occipital du non-voyant sont partiellement réversibles suite à une récupération visuelle à l’âge adulte. De manière générale, ces recherches témoignent de l’importante adaptabilité du cortex occipital aux prises avec des changements drastiques dans l’expérience visuelle.The present Ph.D. work was dedicated to the study of experience-dependent brain plasticity associated with visual deprivation/restoration. In two cross-sectional studies involving the use of functional magnetic resonance imaging in a group of participants with congenital or early blindness (and in a control group of sighted participants), we attempted to characterize the way the occipital cortex - typically devoted to vision – reorganizes itself in order to process different auditory stimuli. We demonstrate that in case of early visual deprivation, distinct regions of the occipital cortex display a functional preference for specific non-visual attributes, maintaining a functional specialization similar to the one that characterizes the sighted brain. Such studies have shed new light on the role played by intrinsic constraints on the one side, and experience on the other, in shaping the modality- and functional tuning of the occipital cortex. On the one hand, the observation of occipital responses to auditory stimulation (crossmodal plasticity) highlights the ability of the occipital cortex to reorient its preferential tuning towards the preserved sensory modalities as a function of experience. On the other hand, the observation of specialized cognitive modules in the occipital cortex, similar to those observed in the sighted, highlights the intrinsic constraints imposed to such plasticity. In a longitudinal single-case study, we further explored how the neuroplastic changes associated with blindness may interact with the newly reacquired visual inputs following partial visual restoration in adulthood. We performed both pre- and post-surgery measurements in a sight-recovery patient combining behavioral, neurostructural and neurofunctional methods in order to jointly investigate the evolution of crossmodal reorganization and visual recovery across time. We demonstrate that functional and structural changes evidenced in the visually-deprived occipital cortex can only partially reverse following sight restoration in adulthood. Altogether, our findings demonstrate the striking adaptability of the occipital cortex facing drastic changes in visual experience

EEG frequency-tagging demonstrates increased left hemispheric involvement and crossmodal plasticity for face processing in congenitally deaf signers

In humans, face-processing relies on a network of brain regions predominantly in the right occipito-temporal cortex. We tested congenitally deaf (CD) signers and matched hearing controls (HC) to investigate the experience dependence of the cortical organization of face processing. Specifically, we used EEG frequency-tagging to evaluate: (1) Face-Object Categorization, (2) Emotional Facial-Expression Discrimination and (3) Individual Face Discrimination. The EEG was recorded to visual stimuli presented at a rate of 6 Hz, with oddball stimuli at a rate of 1.2 Hz. In all three experiments and in both groups, significant face discriminative responses were found. Face-Object categorization was associated to a relative increased involvement of the left hemisphere in CD individuals compared to HC individuals. A similar trend was observed for Emotional Facial-Expression discrimination but not for Individual Face Discrimination. Source reconstruction suggested a greater activation of the auditory cortices in the CD group for Individual Face Discrimination. These findings suggest that the experience dependence of the relative contribution of the two hemispheres as well as crossmodal plasticity vary with different aspects of face processing

Functional selectivity in sensory-deprived cortices

In a recent study, Lomber, Meredith, and Kral (2010) investigated crossmodal reorganization in congenitally deaf cats. They demonstrated that specific regions of the auditory cortex are responsible for distinct supranormal visual performances following early auditory deprivation. These exciting results are considered in light of recently increasing research suggesting that crossmodal plasticity associated with early sensory deprivation follows organizational principles that maintain the functional specialization of the colonized brain regions. © 2011 the American Physiological Society

A common right fronto-parietal network for numerosity and duration processing : an fMRI study

Numerosity and duration processing have been modeled by a functional mechanism taking the form of an accumulator working under two different operative modes. Separate investigations of their cerebral substrates have revealed partly similar patterns of activation, mainly in parietal and frontal areas. However, the precise cerebral implementation of the accumulator model within these areas has not yet been directly assessed. In this study, we asked participants to categorize the numerosity of flashed dot sequences or the duration of single dot displays, and we used functional magnetic resonance imaging (fMRI) to examine the common neural correlates of these processes. The results reveal a large right-lateralized fronto-parietal network, including the intraparietal sulcus (IPS) and areas in the precentral, middle and superior frontal gyri, which is activated by both numerosity and duration processing. Complementary psychophysiological interaction (PPI) analyses show a functional connectivity between the right IPS and the frontal areas in both tasks, whereas the right IPS was functionally connected to the left IPS and the right precentral area in the numerosity categorization task only. We propose that the right IPS underlies a common magnitude processing system for both numerosity and duration, possibly corresponding to the encoding and accumulation stages of the accumulator model, whereas the frontal areas are involved in subsequent working-memory storage and decision-making processes. © 2011 Wiley Periodicals, Inc

Mode-dependent and mode-independent representations of numerosity in the right intraparietal sulcus

In humans, areas around the intraparietal sulcus (IPS) have been found to play a crucial role in coding nonsymbolic numerosities (i.e., number of elements in a collection). In the parietal cortex of monkeys, some populations of neurons were found to respond selectively to sequentially- or simultaneously-presented numerosities, whereas other populations showed similar activation in both modes of presentation. However, whether such mode-dependent and -independent representations of numerosity also exist in humans is still unknown. Here, we used fMRI to identify the areas involved in numerosity processing while participants classified linear arrays of dots (simultaneous stimuli) or flashed dot sequences (sequential stimuli). The processing of simultaneous numerosities induced activations bilaterally in several areas of the IPS, whereas activations during the processing of sequential numerosities were restricted to the right hemisphere. A conjunction analysis showed that only the right IPS and precentral gyrus showed overlapping activations during the judgement of sequential and simultaneous stimuli. Voxelwise correlations confirmed the highly similar pattern of activation found in these regions during both tasks. This pattern was weaker or absent in mode-dependent regions, like the right inferior frontal cortex and the lateral occipital complex. Finally, a close look at the right IPS revealed an anterior-to-posterior gradient of activation with selective activation for sequential and simultaneous stimuli in the anterior and posterior areas, respectively, and overlapping activations in-between. This study provides the first direct evidence that, in humans, the right IPS contains both mode-dependent and mode-independent representations of numerosity

Plasticity of the Dorsal “Spatial” Stream in Visually Deprived Individuals

Studies on visually deprived individuals provide one of the most striking demonstrations that the brain is highly plastic and is able to rewire as a function of the sensory input it receives from the environment. In the current paper, we focus on spatial abilities that are typically related to the dorsal visual pathway (i.e., spatial/motion processing). Bringing together evidence from cataract-reversal individuals, early- and late-blind individuals and sight-recovery cases of long-standing blindness, we suggest that the dorsal “spatial” pathway is mostly plastic early in life and is then more resistant to subsequent experience once it is set, highlighting some limits of neuroplasticity

Attentional shifts due to irrelevant numerical cues: Behavioral investigation of a lateralized target discrimination paradigm

Behavioural evidence indicates the existence of a link between numerical representations and visuo-spatial processes. A striking demonstration of this link was provided by Fischer and colleagues (2003), who reported that participants detect a target more rapidly in the left hemifield, if it is preceded by a small number (e.g. 2 or 3) and more rapidly in the right hemifield if preceded by a large number (e.g. 8 or 9). This is strong evidence that numbers orient visuo-spatial attention to different visual hemifields (e.g., left and right) depending on their magnitude (e.g., small and large, respectively). Here, we sought to replicate number-related attentional shifts using a discrimination task. The participants (n=16) were presented 1 digit (1,2 vs. 8,9) at the centre of the screen for 400ms. After 500ms, 1000ms or 2000ms, a target was briefly flashed in either the right or left hemifield and participants had to report its colour (red or green). They were told that the central digit was irrelevant to the task. We hypothesized that the attentional shift induced by the centrally presented numbers should induce congruency effects for the target discrimination task, so that small (or large) numbers would facilitate the processing of left (or right) targets. Our results confirmed this prediction, but only for the shortest digit-target interval (500ms). This is supported by a significant interaction between number magnitude (small/large) and target hemifield (left/right). The link between numerical and spatial representations further predicts a positive relation between number magnitude and the difference in RT between left and right targets. Regression slopes were computed individually and a positive slope was obtained for short number-target interval. These findings indicate that the attentional shifts induced by irrelevant numerical material are independent of the exact nature of target processing (discrimination vs. detection)

Extensive visual training in adulthood significantly reduces the face inversion effect

The poorer recognition performance for inverted as compared to upright faces is one of the most well-known and robust behavioral effects observed in the field of face perception. Here we investigated whether extensive training at individualizing a large set of inverted faces in adulthood could significantly reduce this inversion effect for novel faces. This issue is important because inverted faces are as complex as upright faces but they are not visually experienced during development. Moreover, inverted faces violate the biological constraints, present at birth, for preferential looking (i.e., a larger number of elements in the top part than the bottom part of the stimulus). Eight adult observers were trained for 2 weeks (16 hr) to individualize 30 inverted face identities presented under different depth-rotated views. Following training, all participants showed a significant reduction of their inversion effect for novel face identities presented in a challenging four-alternatives delayed matching task. This reduction of the face inversion effect was observed in comparison to the magnitude of the same observers’ effect before training, and to the magnitude of the face inversion effect of a group of untrained participants. These observations indicate that extensive training in adulthood can lead to a significant reduction of the inversion effect that generalizes to novel faces, suggesting a larger degree of flexibility of the adult face processing system than previously thought