Auditory cortex encodes lipreading information through spatially distributed activity

Abstract

Watching a speakers face improves speech perception accuracy. These benefits are owed, in part, to implicit lipreading abilities present in the general population. While it is established that lipreading can alter the perception of a heard word, it is unknown how information that is extracted from lipread words is transformed into a neural code that the auditory system can use. One influential, but untested, hypothesis is that visual speech modulates the population coded representations of phonetic and phonemic features in the auditory system. This model is largely supported by data showing that silent lipreading evokes activity in auditory cortex, but these activations could alternatively reflect general effects of arousal or attention, or the encoding of non-linguistic features such as visual timing information. This gap limits our understanding of how vision supports speech perception processes. To test the hypothesis that the auditory system encodes visual speech information, we acquired fMRI data from healthy adults and intracranial recordings from electrodes implanted in patients with epilepsy during auditory and visual speech perception tasks. Across both methods, linear classifiers successfully decoded the identity of silently lipread words using the spatial pattern of auditory cortex responses. Examining the time-course of classification using intracranial recordings, lipread words were classified at significantly earlier time-points relative to heard words, suggesting a predictive mechanism for facilitating speech. These results support a model in which the auditory system combines the joint neural distributions evoked by heard and lipread words to generate a more precise estimate of what was said. Significance StatementWhen we listen to someone speak in a noisy environment, watching their face can help us understand them better, largely due to automatic lipreading abilities. However, it unknown how lipreading information is transformed into a neural code that the auditory system can use. We used fMRI and intracranial recordings in patients to study how the brain processes silently lipread words and found that the auditory system encodes the identity of lipread words through spatially distributed activity. These results suggest that the auditory system combines information from both lipreading and hearing to generate more precise estimates of what is said, potentially by both activating the corresponding representation of the heard word and suppressing incorrect phonemic representations.