Search bioRxivSearch

Biology subjects

Collignon, O.

Publications and source records attributed to Collignon, O..

10 recordsLinked to original sources

Different neural networks for conceptual retrieval in sighted and blind reveal the experiential bases of knowledge.

We investigated the experiential bases of knowledge by asking whether people that perceive the world in a different way also show a different neurobiology of concepts. We characterized the brain activity of early-blind and sighted individuals during a conceptual retrieval task in which participants rated the perceptual similarity between color and action concepts evoked by spoken words. Adaptation analysis showed that word-pairs referring to perceptually similar colors (e.g., red-orange) or actions (e.g., run-jump) led to repetition-suppression in occipital visual regions in the sighted, regions that are known to encode visual features of objects and events, independently of their category. Early blind showed instead adaptation for similar concepts in language-related regions, but not in occipital cortices. Further analysis contrasting the two categories (color and action), independently of item similarity, activated category-sensitive regions in the pMTG (for actions) and the precuneus (for color) in both sighted and blind. These two regions, however, showed a different connectivity profile as a function of visual deprivation, increasing task-dependent connectivity with reorganized occipital regions in the early blind. Overall, our results show that visual deprivation changes the neural bases of conceptual retrieval, which is partially grounded in sensorimotor experience.\n\nSignificance StatementDo people with different sensory experience conceive the world differently? We tested whether conceptual knowledge builds on sensory experience by looking at the neurobiology of concepts in early blind individuals. Participants in fMRI heard pairs of words referring to colors (e.g., green-blue) or actions (e.g., jump-run) and rated their perceptual similarity. Perceptual similarity of colors and actions was represented in occipital visual regions in the sighted, but in language-related regions in the blind. Occipital regions in the blind, albeit not encoding perceptual similarity, were however recruited during conceptual retrieval, working in concert with classic semantic hubs such as the Precuneus and the lpMTG. Overall, visual deprivation changes the neural bases of conceptual processing, which is partially grounded in sensorimotor experience.

neuroscience

White matter connectivity between occipital and temporal regions involved in face and voice processing in hearing and early deaf individuals.

Neuroplasticity following sensory deprivation has long inspired neuroscience research in the quest of understanding how sensory experience and genetics interact in developing the brain functional and structural architecture. Many studies have shown that sensory deprivation can lead to cross-modal functional recruitment of sensory deprived cortices. Little is known however about how structural reorganization may support these functional changes. In this study, we examined early deaf, hearing signer and hearing non-signer individuals using diffusion MRI to evaluate the potential structural connectivity linked to the functional recruitment of the temporal voice area by face stimuli in deaf individuals. More specifically, we characterized the structural connectivity between occipital, fusiform and temporal regions typically supporting voice- and face-selective processing. Despite the extensive functional reorganization for face processing in the temporal cortex of the deaf, macroscopic properties of these connections did not differ across groups. However, both occipito- and fusiform-temporal connections showed significant microstructural changes between groups (fractional anisotropy reduction, radial diffusivity increase). We propose that the reorganization of temporal regions after early auditory deprivation builds on intrinsic and mainly preserved anatomical connectivity between functionally specific temporal and occipital regions.\n\nHighlightsO_LIMacrostructural connectivity of the face-voice system is preserved in early deafness\nC_LIO_LIEarly deafness impacts on the microstructural connectivity of the face-voice system\nC_LIO_LIBoth genetics and experience shape structural connections in the face-voice system\nC_LIO_LIInnate anatomical networks might constrain the expression of cross-modal plasticity\nC_LI\n\nAbbreviations

neuroscience

Recruitment of occipital cortex by arithmetic processing follows computational bias in early blind

Arithmetic reasoning activates the occipital cortex of early blind people (EB). This activation of visual areas may reflect functional flexibility or the intrinsic computational role of specific occipital regions. We contrasted these competing hypotheses by characterizing the brain activity of EB and sighted participants while performing subtraction, multiplication and a control verbal task. In both groups, subtraction selectively activated a bilateral dorsal network commonly activated during spatial processing. Multiplication triggered more activity in temporal regions thought to participate in memory retrieval. No between-group difference was observed for the multiplication task whereas subtraction induced enhanced activity in the right dorsal occipital cortex of the blind individuals only. As this area overlaps and exhibits increased functional connectivity with regions showing selective tuning to auditory spatial processing, our results suggest that the recruitment of occipital regions during high-level cognition in the blind actually relates to the intrinsic computational role of the reorganized regions.

neuroscience

Representation of auditory motion directions and sound source locations in the human planum temporale

The ability to compute the location and direction of sounds is a crucial perceptual skill to efficiently interact with dynamic environments. How the human brain implements spatial hearing is however poorly understood. In our study, we used fMRI to characterize the brain activity of male and female humans listening to left, right, up and down moving as well as static sounds. Whole brain univariate results contrasting moving and static sounds varying in their location revealed a robust functional preference for auditory motion in bilateral human Planum Temporale (hPT). Using independently localized hPT, we show that this region contains information about auditory motion directions and, to a lesser extent, sound source locations. Moreover, hPT showed an axis of motion organization reminiscent of the functional organization of the middle-temporal cortex (hMT+/V5) for vision. Importantly, whereas motion direction and location rely on partially shared pattern geometries in hPT, as demonstrated by successful cross-condition decoding, the responses elicited by static and moving sounds were however significantly distinct. Altogether our results demonstrate that the hPT codes for auditory motion and location but that the underlying neural computation linked to motion processing is more reliable and partially distinct from the one supporting sound source location.\n\nSIGNIFICANCE STATEMENTIn comparison to what we know about visual motion, little is known about how the brain implements spatial hearing. Our study reveals that motion directions and sound source locations can be reliably decoded in the human Planum Temporale (hPT) and that they rely on partially shared pattern geometries. Our study therefore sheds important new lights on how computing the location or direction of sounds are implemented in the human auditory cortex by showing that those two computations rely on partially shared neural codes. Furthermore, our results show that the neural representation of moving sounds in hPT follows a \"preferred axis of motion\" organization, reminiscent of the coding mechanisms typically observed in the occipital hMT+/V5 region for computing visual motion.

neuroscience

Visual cortical entrainment to unheard acoustic speech reflects intelligibility of lip movements and is mediated by dorsal stream regions

Successful lip reading requires a mapping from visual to phonological information [1]. Recently, visual and motor cortices have been implicated in tracking lip movements (e.g. [2]). It remains unclear, however, whether visuo-phonological mapping occurs already at the level of the visual cortex, that is, whether this structure tracks the acoustic signal in a functionally relevant manner. In order to elucidate this, we investigated how the cortex tracks (i.e. entrains) absent acoustic speech signals carried by silent lip movements. Crucially, we contrasted the entrainment to unheard forward (intelligible) and backward (unintelligible) acoustic speech. We observed that the visual cortex exhibited stronger entrainment to the unheard forward acoustic speech envelope compared to the unheard backward acoustic speech envelope. Supporting the notion of a visuo-phonological mapping process, this forward-backward difference of occipital entrainment was not present for actually observed lip movements. Importantly, the respective occipital region received more top-down input especially from left premotor, primary motor, somatosensory regions and, to a lesser extent, also from posterior temporal cortex. Strikingly, across participants, the extent of top-down modulation of visual cortex stemming from these regions partially correlates with the strength of entrainment to absent acoustic forward speech envelope but not to present forward lip movements. Our findings demonstrate that a distributed cortical network, including key dorsal stream auditory regions [3-5], influence how the visual cortex shows sensitivity to the intelligibility of speech while tracking silent lip movements.\n\nHighlightsO_LIVisual cortex tracks better forward than backward unheard acoustic speech envelope\nC_LIO_LIEffects not \"trivially\" caused by correlation of visual with acoustic signal\nC_LIO_LIStronger top-down control of visual cortex during forward display of lip movements\nC_LIO_LITop-down influence correlates with visual cortical entrainment effect\nC_LIO_LIResults seem to reflect visuo-phonological mapping processes\nC_LI

neuroscience

Neuronal populations in the occipital cortex of the blind synchronize to the temporal dynamics of speech

The occipital cortex of early blind individuals (EB) activates during speech processing, challenging the notion of a hard-wired neurobiology of language. But, at what stage of speech processing do occipital regions participate in EB?Here we demonstrate that parieto-occipital regions in EB enhance their synchronization to acoustic fluctuations in human speech in the theta-range (corresponding to syllabic rate), irrespective of speech intelligibility. Crucially, enhanced synchronization to the intelligibility of speech was selectively observed in primary visual cortex in EB, suggesting that this region is at the interface between speech perception and comprehension. Moreover, EB showed overall enhanced functional connectivity between temporal and occipital cortices sensitive to speech intelligibility and altered directionality when compared to the sighted group. These findings suggest that the occipital cortex of the blind adopts an architecture allowing the tracking of speech material, and therefore does not fully abstract from the reorganized sensory inputs it receives.

neuroscience

A (blue) light in the dark: Blue light modulates oscillatory alpha activity in the occipital cortex of totally visually blind individuals with intact non-visual photoreception

The discovery of intrinsically photosensitive retinal ganglion cells (ipRGCs) marked a major shift in our understanding of how light is processed by the mammalian brain. These ipRGCs influence multiple functions not directly related to vision such as the synchronization of circadian rhythmicity, pupil constriction, the regulation of alertness and sleep, as well as the modulation of cognition. More recently, it was demonstrated that ipRGCs may also contribute to basic visual functions. The impact of ipRGCs on visual functions, independently of image forming photoreceptors, remains however difficult to isolate, particularly in humans. We previously showed that exposure to intense monochromatic blue light (465nm) induced awareness of light in a forced choice task in three rare totally visually blind individuals without detectable rod and cone function, but who retained non-visual responses to light, very likely via ipRGCs. The neural foundation of such light awareness in the absence of conscious vision is unknown, however. In this study, we characterized the brain activity of these three rare participants using electroencephalography (EEG), and demonstrate that unconsciously perceived light triggers an early and reliable transient desynchronization (i.e. decreased power) of the alpha EEG rhythm (8-14 Hz) over the occipital cortex. These results provide compelling insight into how ipRGC may contribute to transient changes in ongoing brain activity. They suggest that occipital alpha rhythm synchrony, which is typically linked to the visual system, is modulated by ipRGCs photoreception; a process that may contribute to the awareness of light in those blind individuals.

neuroscience

Functional selectivity for face processing in the temporal voice area of early deaf individuals

Brain systems supporting face and voice processing both contribute to the extraction of important information for social interaction (e.g., person identity). How does the brain reorganize when one of these channels is absent? Here we explore this question by combining behavioral and multimodal neuroimaging measures (magneto-encephalography and functional imaging) in a group of early deaf humans. We show enhanced selective neural response for faces and for individual face coding in a specific region of the auditory cortex that is typically specialized for voice perception in hearing individuals. In this region, selectivity to face signals emerges early in the visual processing hierarchy, shortly following typical face-selective responses in the ventral visual pathway. Functional and effective connectivity analyses suggest reorganization in long-range connections from early visual areas to the face-selective temporal area in individuals with early and profound deafness. Altogether, these observations demonstrate that regions that typically specialize for voice processing in the hearing brain preferentially reorganize for face processing in born deaf people. Our results support the idea that cross-modal plasticity in case of early sensory deprivation relates to the original functional specialization of the reorganized brain regions.

neuroscience

Visual experience shapes the neural networks remapping touch into external space

Localizing touch relies on the activation of skin-based and externally defined spatial frames of references. Psychophysical studies have demonstrated that early visual deprivation prevents the automatic remapping of touch into external space. We used fMRI to characterize how visual experience impacts on the brain circuits dedicated to the spatial processing of touch. Sighted and congenitally blind humans (male and female) performed a tactile temporal order judgment (TOJ) task, either with the hands uncrossed or crossed over the body midline. Behavioral data confirmed that crossing the hands has a detrimental effect on TOJ judgments in sighted but not in blind. Crucially, the crossed hand posture elicited more activity in a fronto-parietal network in the sighted group only. Psychophysiological interaction analysis revealed that the congenitally blind showed enhanced functional connectivity between parietal and frontal regions in the crossed versus uncrossed hand postures. Our results demonstrate that visual experience scaffolds the neural implementation of touch perception.\n\nSignificance statementAlthough we seamlessly localize tactile events in our daily life, it is not a trivial operation because the hands move constantly within the peripersonal space. To process touch correctly, the brain has therefore to take the current position of the limbs into account and remap them to their location in the external world. In sighted, parietal and premotor areas support this process. However, while visual experience has been suggested to support the implementation of the automatic external remapping of touch, no studies so far have investigated how early visual deprivation alters the brain network supporting touch localization. Examining this question is therefore crucial to conclusively determine the intrinsic role vision plays in scaffolding the neural implementation of touch perception.

neuroscience

Functional Preference For Object Sounds But Not For Voices In The Occipito-Temporal Cortex Of Early Blind Individuals

Sounds activate occipital regions in early blind individuals. How different sound categories map onto specific regions of the occipital cortex remains however debated. We used fMRI to characterize brain responses of early blind and sighted individuals to familiar object sounds, human voices and their respective low-level control sounds. Sighted participants were additionally tested when viewing pictures of faces, objects and phase-scrambled control pictures. In both early blind and sighted, a double dissociation was evidenced in bilateral auditory cortices between responses to voices and object sounds: voices elicited categorical responses in bilateral superior temporal sulci while object sounds elicited categorical responses along the lateral fissure bilaterally, including the primary auditory cortex and planum temporale. Outside of the auditory regions, object sounds additionally elicited categorical responses in left lateral and ventral occipito-temporal regions in both groups. These regions also showed response preference for images of objects in the sighted, thus suggesting a functional specialization in these regions that is independent of sensory input and visual experience. Between-group comparisons revealed that only in the blind group, categorical responses to object sounds extended more posteriorly into the occipital cortex. Functional connectivity analyses evidenced a selective increase in the functional coupling between these reorganized regions and regions of the ventral occipito-temporal cortex in the early blind. In contrast, vocal sounds did not elicit preferential responses in the occipital cortex in either group. Nevertheless, enhanced voice-selective connectivity between the left temporal voice area and the right fusiform gyrus were found in the blind. Altogether, these findings suggest that separate auditory categories are not equipotent in driving selective auditory recruitment of occipito-temporal regions in the absence of developmental vision, highlighting domain-region constraints on the expression of crossmodal plasticity.

neuroscience