Through the looking-glass: neural basis of self representation during speech perception

International audienceIntroduction: Our ability to recognize one's own face in a mirror, or know that a voice is one's own is key for our self-awareness and for our ability to communicate effectively with others. Based on a constructivist approach, several recent theories and studies suggest that self-awareness and self-recognition during action observation may partly result from a functional coupling between action and perception systems and a better integration of sensory inputs with our own sensory-motor knowledge. The present fMRI study aimed at further investigate the neural basis of self representation during auditory, visual and audio-visual speech perception. Specifically, our working hypothesis was that hearing and/or viewing oneself talk might activate sensory-motor plans to a greater degree than does observing others. Methods: • Participants were twelve healthy adults (???±??? years; ??? men). • For each participant, multiple occurrences of auditory (A), visual (V), audio-visual (AV) and incongruent audiovisual (AVi, a visual /ka/ dubbed with an acoustic /pa/) of /pa/, /ta/ and /ka/ syllables were recorded and embedded or not with continuous white noise (&#8722;6 dB SNR). A total of 1152 stimuli were created (12 participants x 4 modalities x 3 syllables x 4 occurrences x 2 noise levels) • During the scanning session, participants were asked to passively listening and/or viewing A, V, AV and AVi stimuli. Half of the stimuli were related to themselves, the other half to an unknown speaker, and they were either presented with or without noise. In addition, a resting face of the participant or of the unknown speaker, presented with and without acoustic noise, served as baseline. • Functional MRI images were acquired on a Philips Achieva TX 3T with a sparse-sampling acquisition used to minimize scanner noise (EPI: 53 axial slices, 3 mm3; TR = 8 sec, delay in TR = 5 sec). All stimuli were presented while the MRI gradients were turned off. In addition, a structural T1-weighted whole-brain structural image was also acquired (256 x 224 x 176mm3 with a 1 mm isotropic resolution). • For each participant, the functional series were first realigned by estimating the six movement parameters of a rigid-body transformation. After segmentation of the T1 structural image and coregistration to the mean functional image, all functional images were spatially normalized into the standard stereotaxic space of the Montreal Neurological Institute using segmentation parameters of the T1 structural image. All functional images were then smoothed using a 9 mm full-width at half maximum Gaussian kernel. • BOLD responses were analyzed using a general linear model, including 16 regressors of interest (4 modalities x 2 speakers x 2 noise levels x 18 trials) and the 4 corresponding baselines (2 speakers x 2 noise levels x 18 trials). The six realignment parameters were also included as covariates of no interest. The BOLD response for each event was modeled using a single-bin finite impulse response basis function spanning the time of acquisition (3s). Individual statistical maps were calculated for each regressors of interest compared to its corresponding baseline (e.g., self-related stimuli compared to self-related baseline and noisy stimuli compared to noisy baseline) and subsequently used for group statistics. In order to draw population-based inferences, a second-level random effect group analysis was carried-out, with the modality (4 levels: A, V, AV, AVi), the speaker (2 levels: self, other), and the noise level (2 levels: with, without noise) as within-subject factors and the subjects treated as a random factor. All reported effects and interactions were calculated with a significance level set at p < .001 uncorrected at the voxel level with a cluster extent superior to 10 voxels. Results: • In line with previous brain-imaging studies on multimodal speech perception, the main effect of modality revealed stronger activity in the superior temporal auditory regions during A, AV and AVi compared to V, in the middle temporal visual motion area MT/V5 during V, AV, and AVi compared to A, as well as in the premotor cortices during V, AV and AVi compared to A. Likely due to additional processing during the noisy baseline, the main effect of noise and the modality by noise interaction also showed stronger activity in the primary and secondary auditory cortices for the stimuli presented without noise during A, AV and AVi compared to V, while lower or no activity occurred for the stimuli presented with white noise. • Of more interest, the main effect of the speaker showed stronger activity of the left posterior inferior frontal gyrus as well as of the left cerebellum (lobules I-IV) during the observation of self-related stimuli compared to those related to an unknown speaker. In addition, the self by noise interaction revealed stronger activity in the ventral superior parietal lobules and the dorsal extrastriate cortices during the observation of other-related compared to self-related stimuli presented without noise, while the opposite pattern of activity was observed for noisy stimuli. Finally, the self by modality interaction showed stronger activity for self-related compared to other-related stimuli during A in the right auditory cortex, as well as stronger activity for other-related compared to self-related stimuli for V, AV and AVi in the left posterior temporal sulcus. Conclusions: Irrespective of the speaker, our results first appeared fully consistent with previous brain imaging studies on multimodal speech perception with clear activity changes observed in visual, temporal and premotor brain areas during speech listening and viewing. Crucially, listening and/or viewing oneself talk was found to activate to a greater extent the left posterior inferior frontal gyrus and cerebellum, two regions thought to be responsible for predicting sensory outcomes of action generation constraining perceptual recognition. In addition, activity in auditory and visual associative brain areas was also found to be modulated by the speaker identity depending on the modality of presentation and the acoustic noise. Altogether these results suggest that processing of afferent and efferent signals in sensory-motor areas give rise to the self during speech perception