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

Thèse réalisée en cotutelle avec l'Université catholique de Louvain.

Which factors are important for crossmodal attentional effect?

Some results in the literature suggest that crossmodal attention is very sensitive to the features of the experimental protocol. The current work examined the possible contribution of the asynchrony between the onset of the cue and the target (SOA) and the kind of task performed by the observer to the manifestation of crossmodal attentional effect. In a first experiment, a target (Gabor patch), whose spatial frequency had to be discriminated, was presented 133 or 159 ms after an auditory cue, in a close location on the same side or in a distant location on the opposite side. The crossmodal attentional effect was observed only for the 159 ms SOA. In a second experiment, the SOA was again 133 ms, but the location of the target had to be discriminated, instead of its spatial frequency. A crossmodal attentional effect was observed. The results of these two experiments indicate that crossmodal attentional effect depends on the SOA and the task. It takes longer to develop when the task requires the discrimination of the spatial frequency of the target than the discrimination of its location.

Emotional attention as a modulatory system of perception

Report for the scientific sojourn carried out at the University Medical Center, Swiss, from 2010 to 2012. Abundant evidence suggests that negative emotional stimuli are prioritized in the perceptual systems, eliciting enhanced neural responses in early sensory regions as compared with neutral information. This facilitated detection is generally paralleled by larger neural responses in early sensory areas, relative to the processing of neutral information. In this sense, the amygdala and other limbic regions, such as the orbitofrontal cortex, may play a critical role by sending modulatory projections onto the sensory cortices via direct or indirect feedback.The present project aimed at investigating two important issues regarding these mechanisms of emotional attention, by means of functional magnetic resonance imaging. In Study I, we examined the modulatory effects of visual emotion signals on the processing of task-irrelevant visual, auditory, and somatosensory input, that is, the intramodal and crossmodal effects of emotional attention. We observed that brain responses to auditory and tactile stimulation were enhanced during the processing of visual emotional stimuli, as compared to neutral, in bilateral primary auditory and somatosensory cortices, respectively. However, brain responses to visual task-irrelevant stimulation were diminished in left primary and secondary visual cortices in the same conditions. The results also suggested the existence of a multimodal network associated with emotional attention, presumably involving mediofrontal, temporal and orbitofrontal regions Finally, Study II examined the different brain responses along the low-level visual pathways and limbic regions, as a function of the number of retinal spikes during visual emotional processing. The experiment used stimuli resulting from an algorithm that simulates how the visual system perceives a visual input after a given number of retinal spikes. The results validated the visual model in human subjects and suggested differential emotional responses in the amygdala and visual regions as a function of spike-levels. A list of publications resulting from work in the host laboratory is included in the report.

Emotional attention as a modulatory system of perception

Report for the scientific sojourn carried out at the University Medical Center, Swiss, from 2010 to 2012. Abundant evidence suggests that negative emotional stimuli are prioritized in the perceptual systems, eliciting enhanced neural responses in early sensory regions as compared with neutral information. This facilitated detection is generally paralleled by larger neural responses in early sensory areas, relative to the processing of neutral information. In this sense, the amygdala and other limbic regions, such as the orbitofrontal cortex, may play a critical role by sending modulatory projections onto the sensory cortices via direct or indirect feedback.The present project aimed at investigating two important issues regarding these mechanisms of emotional attention, by means of functional magnetic resonance imaging. In Study I, we examined the modulatory effects of visual emotion signals on the processing of task-irrelevant visual, auditory, and somatosensory input, that is, the intramodal and crossmodal effects of emotional attention. We observed that brain responses to auditory and tactile stimulation were enhanced during the processing of visual emotional stimuli, as compared to neutral, in bilateral primary auditory and somatosensory cortices, respectively. However, brain responses to visual task-irrelevant stimulation were diminished in left primary and secondary visual cortices in the same conditions. The results also suggested the existence of a multimodal network associated with emotional attention, presumably involving mediofrontal, temporal and orbitofrontal regions Finally, Study II examined the different brain responses along the low-level visual pathways and limbic regions, as a function of the number of retinal spikes during visual emotional processing. The experiment used stimuli resulting from an algorithm that simulates how the visual system perceives a visual input after a given number of retinal spikes. The results validated the visual model in human subjects and suggested differential emotional responses in the amygdala and visual regions as a function of spike-levels. A list of publications resulting from work in the host laboratory is included in the report.

Affect-related synesthesias: A prospective view on their existence, expression and underlying mechanisms

The literature on developmental synaesthesia has seen numerous sensory combinations, with surprisingly few reports on synaesthesias involving affect. On the one hand, emotion, or more broadly affect, might be of minor importance to the synaesthetic experience (e.g. Sinke et al., 2012). On the other hand, predictions on how affect could be relevant to the synaesthetic experience remain to be formulated, in particular those that are driven by emotion theories. In this theoretical paper, we hypothesize that a priori studies on synaesthesia involving affect will observe the following. Firstly, the synaesthetic experience is not merely about discrete emotion processing or overall valence (positive, negative) but is determined by or even altered through cognitive appraisal processes. Secondly, the synaesthetic experience changes temporarily on a quantitative level according to i) the affective appraisal of the inducing stimulus or ii) the current affective state of the individual. These hypotheses are inferred from previous theoretical and empirical accounts on synaesthesia (including the few examples involving affect), different emotion theories, crossmodal processing accounts in synaesthetes and nonsynaesthetes, and the presumed stability of the synaesthetic experience. We hope that the current review will succeed in launching a new series of studies on "affective synaesthesias". We particularly hope that such studies will apply the same creativity in experimental paradigms as we have seen and still see when assessing and evaluating "traditional" synaesthesias.

Les habiletés spatio-cognitives des aveugles de naissance : résolution de labyrinthes tactiles

La navigation repose en majeure partie sur la vision puisque ce sens nous permet de rassembler des informations spatiales de façon simultanée et de mettre à jour notre position par rapport à notre environnement. Pour plusieurs aveugles qui se fient à l’audition, le toucher, la proprioception, l’odorat et l’écholocation pour naviguer, sortir à l’extérieur de chez soi peut représenter un défi considérable. Les recherches sur le circuit neuronal de la navigation chez cette population en particulier s’avèrent donc primordiales pour mieux adapter les ressources aux handicapés visuels et réussir à les sortir de leur isolement. Les aveugles de naissance constituent aussi une population d’intérêt pour l’étude de la neuroplasticité. Comme leur cerveau s’est construit en absence d’intrant visuel, la plupart des structures reliées au sens de la vue sont réduites en volume par rapport à ceux de sujets voyants. De plus, leur cortex occipital, une région normalement dédiée à la vision, possède une activité supramétabolique au repos, ce qui peut représenter un territoire vierge pouvant être recruté par les autres modalités pour exécuter diverses tâches sensorielles. Plusieurs chercheurs ont déjà démontré l’implication de cette région dans des tâches sensorielles comme la discrimination tactile et la localisation auditive. D’autres changements plastiques de nature intramodale ont aussi été observés dans le circuit neuronal de la navigation chez ces aveugles. Par exemple, la partie postérieure de l’hippocampe, impliquée dans l’utilisation de cartes mentales, est réduite en volume alors que la section antérieure est élargie chez ces sujets. Bien que ces changements plastiques anatomiques aient bel et bien été observés chez les aveugles de naissance, il reste toutefois à les relier avec leur aspect fonctionnel. Le but de la présente étude était d’investiguer les corrélats neuronaux de la navigation chez l’aveugle de naissance tout en les reliant avec leurs habiletés spatio-cognitives. La première étude comportementale a permis d’identifier chez les aveugles congénitaux une difficulté d’apprentissage de routes tactiles construites dans des labyrinthes de petite échelle. La seconde étude, employant la technique d’imagerie par résonance magnétique fonctionnelle, a relié ces faiblesses au recrutement de régions cérébrales impliquées dans le traitement d’une perspective égocentrique, comme le lobule pariétal supérieur droit. Alors que des sujets voyants aux yeux bandés excellaient dans la tâche des labyrinthes, ces derniers recrutaient des structures impliquées dans un traitement allocentrique, comme l’hippocampe et le parahippocampe. Par ailleurs, la deuxième étude a confirmé le recrutement du cortex occipital dans une tâche de navigation chez les aveugles seulement. Ceci confirme l’implication de la plasticité intermodale dans des tâches cognitives de plus haut niveau, comme la navigation.

Localisation sonore chez les aveugles : l'influence de l'âge de survenue de la cécité

Thèse numérisée par la Division de la gestion de documents et des archives de l'Université de Montréal

Le sens du goût chez l'aveugle congénital

Thèse réalisée en collaboration avec le Département de neurosciences et pharmacologie de l'Université de Copenhague, Danemark.

Does tool use extend peripersonal space? A review and re-analysis

The fascinating idea that tools become extensions of our body appears in artistic, literary, philosophical, and scientific works alike. In the last fifteen years, this idea has been re-framed into several related hypotheses, one of which states that tool use extends the neural representation of the multisensory space immediately surrounding the hands (variously termed peripersonal space, peri-hand space, peri-cutaneous space, action space, or near space). This and related hypotheses have been tested extensively in the cognitive neurosciences, with evidence from molecular, neurophysiological, neuroimaging, neuropsychological, and behavioural fields. Here, I briefly review the evidence for and against the hypothesis that tool use extends a neural representation of the space surrounding the hand, concentrating on neurophysiological, neuropsychological, and behavioural evidence. I then provide a re-analysis of data from six published and one unpublished experiments using the crossmodal congruency task to test this hypothesis. While the re-analysis broadly confirms the previously-reported finding that tool use does not literally extend peripersonal space, the overall effect-sizes are small and statistical power is low. I conclude by questioning whether the crossmodal congruency task can indeed be used to test the hypothesis that tool use modifies peripersonal space.

Top down influence on visuo-tactile interaction modulates neural oscillatory responses

Multisensory integration involves bottom-up as well as top-down processes. We investigated the influences of top-down control on the neural responses to multisensory stimulation using EEG recording and time-frequency analyses. Participants were stimulated at the index or thumb of the left hand, using tactile vibrators mounted on a foam cube. Simultaneously they received a visual distractor from a light emitting diode adjacent to the active vibrator (spatially congruent trial) or adjacent to the inactive vibrator (spatially incongruent trial). The task was to respond to the elevation of the tactile stimulus (upper or lower), while ignoring the simultaneous visual distractor. To manipulate top-down control on this multisensory stimulation, the proportion of spatially congruent (vs. incongruent) trials was changed across blocks. Our results reveal that the behavioral cost of responding to incongruent than congruent trials (i.e., the crossmodal congruency effect) was modulated by the proportion of congruent trials. Most importantly, the EEG gamma band response and the gamma-theta coupling were also affected by this modulation of top-down control, whereas the late theta band response related to the congruency effect was not. These findings suggest that gamma band response is more than a marker of multisensory binding, being also sensitive to the correspondence between expected and actual multisensory stimulation. By contrast, theta band response was affected by congruency but appears to be largely immune to stimulation expectancy.

Atividade multimodal no córtex sensorial primário de ratos.

The currently accepted model of sensory processing states that different senses are processed in parallel, and that the activity of specific cortical regions define the sensorial modality perceived by the subject. In this work we used chronic multielectrode extracellular recordings to investigate to which extent neurons in the visual and tactile primary cortices (V1 and S1) of anesthetized rats would respond to sensory modalities not traditionaly associated with these cortices. Visual stimulation yielded 87% of responsive neurons in V1, while 82% of S1 neurons responded to tactile stimulation. In the same stimulation sessions, we found 23% of V1 neurons responding to tactile stimuli and 22% of S1 neurons responding to visual stimuli. Our data supports an increasing body of evidence that indicates the existence multimodal processing in primary sensory cortices. Our data challenge the unimodal sensory processing paradigm, and suggest the need of a reinterpretation of the currently accepted model of cortical hierarchy.

Residual visual processing following real or virtual lesions to primary visual pathways

Lesions to the primary geniculo-striate visual pathway cause blindness in the contralesional visual field. Nevertheless, previous studies have suggested that patients with visual field defects may still be able to implicitly process the affective valence of unseen emotional stimuli (affective blindsight) through alternative visual pathways bypassing the striate cortex. These alternative pathways may also allow exploitation of multisensory (audio-visual) integration mechanisms, such that auditory stimulation can enhance visual detection of stimuli which would otherwise be undetected when presented alone (crossmodal blindsight). The present dissertation investigated implicit emotional processing and multisensory integration when conscious visual processing is prevented by real or virtual lesions to the geniculo-striate pathway, in order to further clarify both the nature of these residual processes and the functional aspects of the underlying neural pathways. The present experimental evidence demonstrates that alternative subcortical visual pathways allow implicit processing of the emotional content of facial expressions in the absence of cortical processing. However, this residual ability is limited to fearful expressions. This finding suggests the existence of a subcortical system specialised in detecting danger signals based on coarse visual cues, therefore allowing the early recruitment of flight-or-fight behavioural responses even before conscious and detailed recognition of potential threats can take place. Moreover, the present dissertation extends the knowledge about crossmodal blindsight phenomena by showing that, unlike with visual detection, sound cannot crossmodally enhance visual orientation discrimination in the absence of functional striate cortex. This finding demonstrates, on the one hand, that the striate cortex plays a causative role in crossmodally enhancing visual orientation sensitivity and, on the other hand, that subcortical visual pathways bypassing the striate cortex, despite affording audio-visual integration processes leading to the improvement of simple visual abilities such as detection, cannot mediate multisensory enhancement of more complex visual functions, such as orientation discrimination.

Differential patterns of multisensory interactions in core and belt areas of human auditory cortex

The auditory cortex is anatomically segregated into a central core and a peripheral belt region, which exhibit differences in preference to bandpassed noise and in temporal patterns of response to acoustic stimuli. While it has been shown that visual stimuli can modify response magnitude in auditory cortex, little is known about differential patterns of multisensory interactions in core and belt. Here, we used functional magnetic resonance imaging and examined the influence of a short visual stimulus presented prior to acoustic stimulation on the spatial pattern of blood oxygen level-dependent signal response in auditory cortex. Consistent with crossmodal inhibition, the light produced a suppression of signal response in a cortical region corresponding to the core. In the surrounding areas corresponding to the belt regions, however, we found an inverse modulation with an increasing signal in centrifugal direction. Our data suggest that crossmodal effects are differentially modulated according to the hierarchical core-belt organization of auditory cortex.

Brain responses to auditory and visual stimulus offset: Shared representations of temporal edges

Edges are crucial for the formation of coherent objects from sequential sensory inputs within a single modality. Moreover, temporally coincident boundaries of perceptual objects across different sensory modalities facilitate crossmodal integration. Here, we used functional magnetic resonance imaging in order to examine the neural basis of temporal edge detection across modalities. Onsets of sensory inputs are not only related to the detection of an edge but also to the processing of novel sensory inputs. Thus, we used transitions from input to rest (offsets) as convenient stimuli for studying the neural underpinnings of visual and acoustic edge detection per se. We found, besides modality-specific patterns, shared visual and auditory offset-related activity in the superior temporal sulcus and insula of the right hemisphere. Our data suggest that right hemispheric regions known to be involved in multisensory processing are crucial for detection of edges in the temporal domain across both visual and auditory modalities. This operation is likely to facilitate cross-modal object feature binding based on temporal coincidence. Hum Brain Mapp, 2008. (c) 2008 Wiley-Liss, Inc.

Developing Synaesthesia

Synaesthesia is a condition in which a stimulus elicits an additional subjective experience. For example, the letter E printed in black (the inducer) may trigger an additional colour experience as a concurrent (e.g., blue). Synaesthesia tends to run in families and thus, a genetic component is likely. However, given that the stimuli that typically induce synaesthesia are cultural artefacts, a learning component must also be involved. Moreover, there is evidence that synaesthetic experiences not only activate brain areas typically involved in processing sensory input of the concurrent modality; synaesthesia seems to cause a structural reorganisation of the brain. Attempts to train non-synaesthetes with synaesthetic associations have been successful in mimicking certain behavioural aspects and posthypnotic induction of synaesthetic experiences in non-synaesthetes has even led to the according phenomenological reports. These latter findings suggest that structural brain reorganization may not be a critical precondition, but rather a consequence of the sustained coupling of inducers and concurrents. Interestingly, synaesthetes seem to be able to easily transfer synaesthetic experiences to novel stimuli. Beyond this, certain drugs (e.g., LSD) can lead to synaesthesia-like experiences and may provide additional insights into the neurobiological basis of the condition. Furthermore, brain damage can both lead to a sudden presence of synaesthetic experiences in previously non-synaesthetic individuals and a sudden absence of synaesthesia in previously synaesthetic individuals. Moreover, enduring sensory substitution has been effective in inducing a kind of acquired synaesthesia. Besides informing us about the cognitive mechanisms of synaesthesia, synaesthesia research is relevant for more general questions, for example about consciousness such as the binding problem, about crossmodal correspondences and about how individual differences in perceiving and experiencing the world develop. Hence the aim of the current Research Topic is to provide novel insights into the development of synaesthesia both in its genuine and acquired form. We welcome novel experimental work and theoretical contributions (e.g., review and opinion articles) focussing on factors such as brain maturation, learning, training, hypnosis, drugs, sensory substitution and brain damage and their relation to the development of any form of synaesthesia.