In order to understand the evolution of human language, it is necessary to explore the neural systems that support language processing in its many forms. In particular, it is informative to separate those mechanisms that may have evolved for sensory processing (hearing) from those that have evolved to represent events and actions symbolically (language). To what extent are the brain systems that support language processing shaped by auditory experience and to what extent by exposure to language, which may not necessarily be acoustically structured? In this first neuroimaging study of the perception of British Sign Language (BSL), we explored these questions by measuring brain activation using functional MRI in nine hearing and nine congenitally deaf native users of BSL while they performed a BSL sentence-acceptability task. Eight hearing, non-signing subjects performed an analogous task that involved audio-visual English sentences. The data support the argument that there are both modality-independent and modality-dependent language localization patterns in native users. In relation to modality-independent patterns, regions activated by both BSL in deaf signers and by spoken English in hearing non-signers included inferior prefrontal regions bilaterally (including Broca's area) and superior temporal regions bilaterally (including Wernicke's area). Lateralization patterns were similar for the two languages. There was no evidence of enhanced right-hemisphere recruitment for BSL processing in comparison with audio-visual English. In relation to modality-specific patterns, audio-visual speech in hearing subjects generated greater activation in the primary and secondary auditory cortices than BSL in deaf signers, whereas BSL generated enhanced activation in the posterior occipito-temporal regions (V5), reflecting the greater movement component of BSL. The influence of hearing status on the recruitment of sign language processing systems was explored by comparing deaf and hearing adults who had BSL as their first language (native signers). Deaf native signers demonstrated greater activation in the left superior temporal gyrus in response to BSL than hearing native signers. This important finding suggests that left- temporal auditory regions may be privileged for processing heard speech even in hearing native signers. However, in the absence of auditory input this region can be recruited for visual processing.

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Just as words can rhyme, the signs of a signed language can share structural properties, such as location. Linguistic description at this level is termed phonology. We report that a left-lateralised fronto-parietal network is engaged during phonological similarity judgements made in both English (rhyme) and British Sign Language (BSL; location). Since these languages operate in different modalities, these data suggest that the neural network supporting phonological processing is, to some extent, supramodal. Activation within this network was however modulated by language (BSL/English), hearing status (deaf/hearing), and age of BSL acquisition (native/non-native). The influence of language and hearing status suggests an important role for the posterior portion of the left inferior frontal gyrus in speech-based phonological processing in deaf people. This, we suggest, is due to increased reliance on the articulatory component of speech when the auditory component is absent. With regard to age of first language acquisition, non-native signers activated the left inferior frontal gyrus more than native signers during the BSL task, and also during the task performed in English, which both groups acquired late. This is the first neuroimaging demonstration that age of first language acquisition has implications not only for the neural systems supporting the first language, but also for networks supporting languages learned subsequently.