Neuroanatomical Profiles of Deafness in the Context of Native Language Experience

Discussion

The present study investigated how lack of auditory experience affects brain anatomy by contrasting GMV and WMV in deaf and hearing adults using whole-brain voxel-based morphometry. By analogy with reports on visual system differences in studies of the blind, one might expect less brain volume in early auditory regions. However, studies of deafness are complicated by the fact that deaf individuals are raised with varying language experiences and acoustic stimuli and language are both processed in auditory regions within the superior temporal gyrus. Therefore, our study involved deaf and hearing participants with and without native sign experience to determine whether the effects of deafness manifest differently on brain matter in deaf individuals with distinct language backgrounds.

Our first study of deaf native signers was intended to provide consistency with prior investigations that have focused primarily on this population. Hearing native signers served as the comparison group because differences between deaf signers and hearing nonsigners as reported by most (but see Allen et al., 2008, 2013) make it impossible to make attributions to sensory versus language experience. Unlike prior work, in the present study, we investigated the whole brain. Prior work in the deaf (using hand tracing, VBM, and other methods) has often examined a priori regions of interest to focus specifically on auditory areas (Emmorey et al., 2003; Penhune et al., 2003; Smith et al., 2011), visual areas (Fine et al., 2005; Allen et al., 2013), insula (Allen et al., 2008), motor cortex and inferior frontal gyrus (Allen et al., 2013), and corpus callosum (Kara et al., 2006; Leporé et al., 2010). Those who examined differences at the whole-brain level have in some cases reported differences in auditory regions (Shibata, 2007; Kim et al., 2009; Leporé et al., 2010; Pénicaud et al., 2012) and elsewhere, including parietal, frontal, and temporal lobes; motor regions; and cerebellum (Penhune et al., 2003; Shibata, 2007; Kim et al., 2009; Leporé et al., 2010). When comparing deaf with hearing native users of ASL across the whole brain, we found less GMV and WMV in superior temporal regions bilaterally, including primary auditory cortex. Less WMV in auditory brain regions has been reported in comparisons of adult deaf signers and hearing nonsigners (Emmorey et al., 2003; Shibata, 2007; Leporé et al., 2010; Pénicaud et al., 2012), and deaf and hearing prelingual infants (Smith et al., 2011). Our replication of less WMV in superior temporal regions bilaterally, achieved here with a hearing native signing control group, is consistent with work conducted without hearing signers; it also converges with our novel finding of less GMV in bilateral transverse temporal gyri. An interesting outcome of this analysis is the finding of more GMV in the deaf native signers in right superior frontal cortex.

Our second and main analysis served to address the concern that prior studies have largely involved deaf native users of ASL, who represent a small section of the deaf population and whose native experience with a spatial language might play a mitigating role in the results to date (Cardin et al., 2013). Although both the hearing and deaf participants in the first study were matched on their ASL experience, the experience of a signed language might add another layer of experience-induced plasticity that could in part be responsible for the anatomical differences attributed to deafness. Sign language use makes unique motor, visuospatial, and temporal demands on the brain (Campbell et al., 2008; MacSweeney et al., 2008). Indeed, our results from the ANOVA revealed a main effect of language experience in numerous brain areas, notably in the right hemisphere, where native users of ASL (deaf and hearing together) had more GMV than native users of English (deaf and hearing), whereas there were no areas that showed less GMV for native signers. These observations, especially the most robust finding in right middle frontal (BA9) gyrus, fit with the idea that spatial demands of ASL affect right hemisphere brain anatomy, here found in regions known to subserve planning of motor movements.

Our central question was how such effects of ASL experience would compound with deafness. The interaction analysis between language and sensory experience confirmed our prediction that some anatomical differences attributed to deafness are unique to native users of ASL. These included less GMV in right precentral gyrus (BA6) and insula (BA13) and more in right medial frontal gyrus (BA9) and left caudate in deaf native signers. The frontal locations imply a role for movement sequencing or decisions about actions in the absence of audition in signers. Notably, there was less WMV in the deaf native signers in left superior (BA21) and inferior frontal gyri (BA45), suggesting an impact on language areas in the absence of audition in signers. Together, these observations illustrate that some anatomical differences attributed to deafness are unique to native users of ASL. Native users of English in turn exhibit differential effects in other brain regions.

So, what are the most salient differences between deaf and hearing people independent of their language experience? The main effect of sensory experience revealed less GMV, most notably in fusiform gyrus (BA20). This focus, along with a similar finding in left lingual gyrus (BA18), suggests that visual areas within and outside of striate cortex contain less GMV in the deaf independent of their language experience. We also found more GMV in the deaf in right superior frontal gyrus (BA10), consistent with a report of “hypertrophy” in deaf signers in nearby prefrontal lobe structures (Leporé et al., 2010). This suggests the possibility of altered, perhaps enhanced executive function in all deaf in the absence of auditory information.

Our prediction was that brain matter within and surrounding auditory regions would be affected by deafness. Although we did not find overall less GMV in auditory cortex of the deaf, WMV was less in left superior temporal gyrus (BA41) in the deaf (native users of english and ASL combined) compared with hearing groups. This is consistent with prior studies of the deaf (Emmorey et al., 2003; Shibata, 2007; Kim et al., 2009; Leporé et al., 2010; Smith et al., 2011; Pénicaud et al., 2012) and our own between-group comparison presented in the first analysis. White matter reduction in auditory regions has been attributed to reduced myelination or increased pruning of auditory fibers, and thus fewer connections between auditory cortex and other brain regions (Emmorey et al., 2003), or as a result of functional reorganization (Finney et al., 2001; Bavelier and Neville, 2002; Fine et al., 2005). Indeed, there are reports of reduced white matter microstructural integrity measured with diffusion tensor imaging in superior temporal areas in adults with congenital hearing loss (Kim et al., 2009; Li et al., 2012). The interpretation of GMV differences is not straightforward. Much of the cortex undergoes thinning over development perhaps due to neuronal pruning (Giedd and Rapoport, 2010), but perisylvian language areas thicken (Sowell et al., 2004). Therefore, observation of more GMV could reflect normal maturation, but also failure to mature, depending on the location. In sum, the mechanisms underlying microstructural changes and their interpretation require further study and will benefit from other measures, such as gyrification patterns (Im et al., 2010).

Whether classical language areas in the left superior temporal lobe, also closely located to auditory cortex, are used differently in the deaf has been a topic of debate, especially in the context of sign language processing. Some have shown that sign language elicits activity in auditory regions (Nishimura et al., 1999; Lambertz et al., 2005; MacSweeney et al., 2008), whereas others have found activity in visual (but not auditory) cortex (Leonard et al., 2012). A recent report attributed activity in the left superior temporal sulcus in deaf signers to the linguistic (not visual sensory) aspects of sign language (Cardin et al., 2013). Our findings provide important new context for these observations, demonstrating that all deaf people in our study, independent of their native language background, have less white matter within left hemisphere auditory regions (BA41). However, the interaction analysis revealed critical new information: white matter in areas associated with language—the left STG (BA21) and inferior frontal gyrus (BA45)—is reduced only in deaf native users of sign (not in native users of English). Together, these findings provide new insights, inferring fewer white matter connections in early auditory regions in the deaf population in general, with extension of these WMV differences into areas known to process phonological information only in the deaf subjects who did not grow up with English as a native language. This may reflect a distinction that exists for phonology in ASL versus phonology in English.

Together, these results demonstrate that language background plays an important role in determining how deafness affects brain anatomy. Some anatomical differences attributed to deafness are unique to native users of ASL and are not generalizable to the larger deaf population. Further, the differential effects on brain areas subserving audition versus those subserving language can be disambiguated by studying deaf groups with distinct native language experiences, in this case English and ASL.