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The Journal of Neuroscience, October 28, 2009, 29(43):13445-13453; doi:10.1523/JNEUROSCI.3194-09.2009

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Behavioral/Systems/Cognitive
Dual Neural Routing of Visual Facilitation in Speech Processing

Luc H. Arnal,¹ Benjamin Morillon,¹ Christian A. Kell,^1,2 and Anne-Lise Giraud^1,3

¹Inserm U960, Laboratoire de Neurosciences Cognitives, Département d'Etudes Cognitives, Ecole Normale Supérieure, F-75005 Paris, France, ²Brain Imaging Center, Department of Neurology, Goethe-University, D-60590 Frankfurt am Main, Germany, and ³Centre de Neuroimagerie de Recherche, Hôpital de la Pitié-Salpêtrière, F-75013 Paris, France

Correspondence should be addressed to Luc H. Arnal, Laboratoire de Neurosciences Cognitives, Département d'Etudes Cognitives, Ecole Normale Supérieure, 29 rue d'Ulm, F-75005 Paris, France. Email: luc.arnal{at}ens.fr

Viewing our interlocutor facilitates speech perception, unlike for instance when we telephone. Several neural routes and mechanisms could account for this phenomenon. Using magnetoencephalography, we show that when seeing the interlocutor, latencies of auditory responses (M100) are the shorter the more predictable speech is from visual input, whether the auditory signal was congruent or not. Incongruence of auditory and visual input affected auditory responses 20 ms after latency shortening was detected, indicating that initial content-dependent auditory facilitation by vision is followed by a feedback signal that reflects the error between expected and received auditory input (prediction error). We then used functional magnetic resonance imaging and confirmed that distinct routes of visual information to auditory processing underlie these two functional mechanisms. Functional connectivity between visual motion and auditory areas depended on the degree of visual predictability, whereas connectivity between the superior temporal sulcus and both auditory and visual motion areas was driven by audiovisual (AV) incongruence. These results establish two distinct mechanisms by which the brain uses potentially predictive visual information to improve auditory perception. A fast direct corticocortical pathway conveys visual motion parameters to auditory cortex, and a slower and indirect feedback pathway signals the error between visual prediction and auditory input.

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Received July 3, 2009; revised Sept. 8, 2009; accepted Sept. 21, 2009.

Correspondence should be addressed to Luc H. Arnal, Laboratoire de Neurosciences Cognitives, Département d'Etudes Cognitives, Ecole Normale Supérieure, 29 rue d'Ulm, F-75005 Paris, France. Email: luc.arnal{at}ens.fr

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