We demonstrated that fMRI signal change in Heschl's gyrus—the site of human primary auditory cortex—responded to unimodal somatosensory stimuli in congenitally deaf adults but not in hearing adults. Bimodal stimuli elicited a larger response than unimodal stimuli in Heschl's gyrus in both deaf and hearing adults but represented a more robust increase from the fixation baseline only in deaf adults. In deaf Heschl's gyrus, visual responses were weaker than somatosensory or bimodal stimulation. For unimodal vision, group differences were only significant in the contralateral posterior subregion of Heschl's gyrus, a likely homolog of primate area R (Da Costa et al., 2011
). In contrast to Heschl's gyrus, there was no difference between unimodal somatosensation and vision in the deaf superior-temporal region (auditory association and multisensory cortex). A key finding was that there were marked perceptual differences between deaf and hearing adults; deaf, but not hearing, adults were susceptible to an illusory percept of a double flash of light when a single flash was paired with a double touch to the face. The strength of the illusion was predicted by signal change in the contralateral rostral subregion of Heschl's gyrus (approximate Te1.2) (Morosan et al., 2001
) in the deaf adults.
A limitation of previous studies of cross-modal neuroplasticity of auditory cortex in deaf humans is the spatial resolution afforded by the techniques that were used. Individual Heschl's gyri vary in morphology and position (Morosan et al., 2001
; Da Costa et al., 2011
), and analyses that spatially average across individual brains can result in activity from the planum temporale or somatosensory regions of the parietal operculum being misattributed to Heschl's gyrus or true activity in Heschl's gyrus being missed due to low spatial concordance across participants. To our knowledge, no previous study of congenitally deaf humans has used an ROI approach to identify Heschl's gyrus or has subdivided these regions to test whether cross-modal neuroplasticity differs in subregions approximating human primary auditory cortical areas. In past fMRI studies of deaf adults, such as in Finney et al. (2001)
, standard practice was to use Talairach coordinates, an atlas based on a single elderly brain, to localize primary auditory cortex. As we illustrate (), Talairach coordinates for primary auditory cortex are more posterior on the right than recent probabilistic atlases (Eickhoff et al., 2007
). Even so, most studies of altered visual organization in deaf participants report cross-modal altered organization caudal to, rather than overlapping, the posterior aspect of Heschl's gyrus (Bavelier et al., 2006
Our results suggest that cross-modal neuroplasticity in deaf primary auditory cortex is greater for the somatosensory than the visual modality. This could be explained by stimulus intensity differences between visual and somatosensory stimuli, but this is unlikely in our experiment. Although somatosensory targets were more readily distinguished from somatosensory standards than visual targets from visual standards, the standard stimuli (80% of the trials) were easily detected for both modalities, and in the superior-temporal region there was no significant difference between visual and somatosensory signal amplitudes. Another possible explanation for the disparity between modalities in primary auditory cortex could be that a different stimulus type, such as peripheral visual motion, is more suited to elicit responses in deaf primary auditory cortex. Future studies with more diverse visual stimulation and parametric manipulation of stimulus strength with anatomical ROIs are needed to definitively address this issue.
Our results demonstrating robust responses in Heschl's gyrus for the somatosensory modality are consistent with the two previous reports of somatosensory responses in the auditory cortex of deaf humans. Auer et al. (2007)
reported somatosensory activation overlapping atlas-defined Heschl's gyrus in a deaf group relative to fixation, but ROI analysis was not performed making it difficult to determine whether responses were in primary auditory cortex. A magnetoencephalography (MEG) study using source modeling in a single elderly deaf person reported somatosensory responses were accounted for by a source in auditory cortex (Levänen et al., 1998
) although the spatial precision of MEG is lower than that of fMRI, making more precise localization problematic. However, in a different MEG and fMRI study of a 28-year-old congenitally deaf man, no visual or somatosensory responses were found in auditory cortex (Hickock et al., 1997
). In our sample of 13 congenitally deaf adults, there were individual differences in the cross-modal responses in deaf auditory cortex, and these differences were correlated with altered perception.
An interesting point to consider is whether group differences are influenced by qualitatively different experiences of background sounds in an MRI experiment. For example, the negative response of Heschl's gyrus in hearing participants could be elicited by overt attention to MRI scanner sounds during resting fixation. However, this interpretation is not supported by results in the superior-temporal region, which were positive or near zero for hearing participants. It seems unlikely that this auditory and multisensory region is less responsive with overt attention to the MRI scanner noise than primary auditory cortex. In addition, group differences in the resting fixation condition do not account for differential signal change between conditions. Unfortunately, MRI background sounds are inherent to the MRI technique and cannot be matched between deaf and hearing groups.
We found that the deaf participants perceived a somatosensory-induced double-flash illusion while hearing participants did not. The absence of any illusion in hearing participants is surprising in light of previous reports that have shown that this double-flash illusion may be observed for either auditory or somatosensory stimulation in hearing adults (Violentyev et al., 2005
; Lange et al., 2011
). This may be due to stimulus differences; our somatosensory stimuli were air puffs to the face and were spatially coregistered with the lights in the far visual periphery while previous studies used vibrotactile stimulation to the fingertips. We positioned the lights in the far periphery because previous studies have shown that visual enhancements in the deaf are strongest in the visual periphery (Neville and Lawson, 1987
; Bavelier et al., 2000
) and this factor, combined with increased deaf tactile sensitivity (Levänen and Hamdorf, 2001
), may be what led to a robust illusory percept only in the deaf participants. Across deaf individuals, there was variability in the susceptibility to the illusion, and the response in rostrolateral Heschl's gyrus predicted the strength of the illusion in the deaf participants. This finding is consistent with our hypothesis that cross-modal neuroplasticity in primary auditory cortex contributes to altered perceptions in deaf people.
Notably, although somatosensory responses were robust in each subregion of Heschl's gyrus, it was the rostrolateral region (Te1.2) that predicted the strength of the somatosensory-induced double-flash illusion and had the largest overall signal change. The functional specialization of different regions of human primary auditory cortex is not currently known, but our results suggest that altered cross-modal organization of primary auditory cortex in deaf people is not uniform. In addition, while visual responses in deaf Heschl's gyrus were weak compared to somatosensory and bimodal responses, they were equal to somatosensory responses in the superior-temporal region. These findings are interesting in light of evidence from animal studies of visual-somatosensory cross-modal plasticity in auditory cortex. In cats, there are dissociations between auditory cortical regions; a core auditory area, the anterior auditory field (AAF), in cats responds to somatosensory stimulation (Meredith and Lomber, 2011
) and shows different cross-modal responses than the auditory field of the anterior ectosylvian sulcus (fAES) (Meredith et al., 2011
). In addition, multisensory visual-somatosensory neurons are prevalent in the primary auditory cortex of congenitally deaf mice (Hunt et al., 2006
). Research addressing which human auditory areas are likely homologs of regions in animal models would allow for more direct comparisons across models.
An important question is how altered organization of the auditory cortex arises. One possibility is the developmental stabilization of cross-modal connections that occur even in typically developing individuals. Primate studies indicate that multisensory interactions between hearing and touch occur in the auditory cortex of hearing individuals (Kayser et al., 2005
), with some very early somatosensory responses to median nerve electrical stimulation in primary auditory cortex (Lakatos et al., 2007
). In addition, visual stimuli influence auditory cortex (Bizley et al., 2007
; Kayser et al., 2007
), and multisensory interactions occur in low-level auditory cortex (Musacchia and Schroeder, 2009
). In our study, even the hearing participants had increased signal in Heschl's gyrus and superior-temporal cortex for bimodal stimuli relative to unimodal stimuli. If cross-modal connections are typical in the auditory cortex of hearing individuals, it is reasonable to speculate that these connections increase in number and strength when acoustic input is reduced. The receptive fields for these cross-modal inputs into deaf auditory cortex may be large and extend bilaterally (Meredith and Lomber, 2011
; Meredith et al., 2011
Future research using methods sensitive to the timing of multisensory responses in auditory cortex, such as EEG and MEG, may elucidate whether these signals occur early in the sensory processing hierarchy or are due to later feedback from other cortical areas (e.g., subcortical connectivity, corticocortical feedback, or feedforward pathways between primary cortices). Future studies using event-related designs or block designs with alternating rest (Kayser et al., 2005
) could address whether time-series differ between regions and conditions. Another important question for future research is whether altered organization and altered perception have a sensitive period leading to different plasticity for individuals who become deaf later in childhood or adulthood and how it is affected by later reintroduction of auditory nerve input through cochlear implantation; for example, deafness in adulthood induces somatosensory conversion of ferret auditory cortex (Allman et al., 2009
). It is important to understand how the age of onset of deafness, sign language learning, and degree of deafness influence cross-modal neuroplasticity of auditory cortex and perceptual changes such as the somatosensory-induced double-flash illusion. Together, our results highlight the central role of experiential factors in driving brain development and function, even at the level of primary sensory cortices, and have practical implications for educational and rehabilitative programs for both typically and nontypically developing individuals.