Regular articleThe morphometry of auditory cortex in the congenitally deaf measured using MRI
Introduction
The study of congenitally deaf individuals provides a unique opportunity to understand the organization and potential for reorganization of human auditory cortex. Studies in congenitally deaf individuals stimulated with cochlear implants indicate preserved potential for auditory cortical function Hari et al., 1988, Okazawa et al., 1996, but suggest that this potential diminishes with age and with duration of deafness (Ponton et al., 1999). Neuroimaging studies show auditory cortical activity in deaf subjects processing sign language and other complex visual stimuli Finney et al., 2001, Newman et al., 2002, Petitto et al., 2000. But, despite intense current interest in neural plasticity and in the development of cochlear implants, there have been no experiments examining the possible structural changes in human auditory cortex that might underlie the observed functional changes. A single postmortem study of seven individuals with adult-onset deafness showed changes in auditory brainstem nuclei, but did not examine the cortex (Moore et al., 1997). Here, we used volumetric MRI to examine the region of primary auditory cortex, Heschl's gyrus (HG), and a secondary cortical region, the planum temporale (PT), in congenitally deaf individuals. Possible changes in these and other anatomical regions were also assessed using a whole-brain voxel-based technique.
The first question we asked is what global changes might occur in auditory cortex as a result of long-term sensory deprivation? Anatomical and physiological studies have shown reduction in the number and activity of neurons and changes in their response properties in the auditory brainstem of congenitally deaf, or experimentally deafened animals (for review, see Shepherd et al., 1997), but studies of auditory cortex have been inconclusive, because of the use of unilaterally deafened animals McMullen and Glaser, 1988, Reale et al., 1987. More recent studies in congenitally deaf cats have demonstrated microstructural changes in the dendrites in primary auditory cortex (Wurth et al., 1999), as well as changes in electrophysiological function Klinke et al., 1999, Kral et al., 2000. Finally, human neuroimaging studies with cochlear implant users show variable responsiveness in auditory cortex Hirano et al., 2000, Naito et al., 1997, Okazawa et al., 1996. However, none of these studies have examined possible structural changes in auditory cortex that might underlie these functional changes.
The second question we asked is whether there might be specific changes in auditory cortex of the congenitally deaf related to auditory language function. Human auditory cortex is characterized by interhemispheric asymmetries in gross morphology and cytoarchitectonic organization. Gross anatomical asymmetries between the hemispheres have been noted since the beginning of the century in both HG Heschl, 1878, von Economo and Horn, 1930 and PT Geschwind and Levitsky, 1968, Pfeifer, 1936, von Economo and Horn, 1930. Previous work in our laboratory using structural MRI has documented a L > R asymmetry in the volume of HG (Penhune et al., 1996), and has replicated earlier findings (Galaburda et al., 1978a; Loftus et al., 1993) of an asymmetry in the angulation of the PT (Westbury et al., 1999). The findings of gross anatomical asymmetries have been complemented by cytoarchitectonic studies (Anderson et al., 1999; Galaburda et al., 1978b, Galuske et al., 2000, Morosan et al., 2001, Seldon, 1982 showing left-right differences in cellular organization of these regions. These asymmetries have been hypothesized to be related to auditory language processing Foundas et al., 1994, Galaburda et al., 1978a, Galaburda et al., 1978b; Geschwind and Levitsky, 1968, Zatorre et al., 2002, but whether they are genetically determined or develop with exposure to auditory language has not been established. This question can be elucidated by determining whether these asymmetries are present in congenitally deaf individuals with no auditory language experience.
Finally, this experiment is also relevant to the question of plasticity or reorganization in auditory cortex. Animal experiments where retinal output is surgically redirected to auditory cortex have shown that auditory cortex can be reorganized to resemble visual cortex in its response patterns and topography Gao and Pallas, 1999, Sharma et al., 2000, and that these animals can perform visual tasks Frost et al., 2000, von Melchner et al., 2000. Recent neuroimaging studies in the deaf have found activity in the auditory cortex during processing of sign language and other visual stimuli Finney et al., 2001, Newman et al., 2002, Petitto et al., 2000, indicative of cortical reorganization. Understanding the structural changes that occur in these individuals can tell us about the time course and limits of such reorganization.
Section snippets
Subjects
Subjects were 12 right-handed, deaf adults (7 male, 5 female; average age = 29 years) and 10 right-handed hearing adults (5 male, 5 female; average age = 32 years) who had previously participated in a PET activation study of sign language processing (Petitto et al., 2000). All deaf subjects were profoundly congenitally deaf in both ears [average dB loss right ear = 95 (range = 90–110); average dB loss left ear = 94 (range = 88–110)], with no residual hearing and no known neurological deficits.
Procedure
HG and PT were identified in each scan using landmarks (see Fig. 1) and criteria defined in previous studies Penhune et al., 1996, Westbury et al., 1999. Based on careful review of the anatomical and physiological literature, HG was defined as only the most anterior transverse gyrus on the superior temporal plane (for review of the relevant literature, see Penhune et al., 1996). Although there is no one-to-one correspondence between this gross anatomical definition and the cytoarchitectonic
Volume measurements
Measurements of HG (see Fig. 2 and Table 1 ) showed preserved cortical grey and white matter volumes for the deaf compared to the hearing group [F(1,20) = 0.13, P > 0.05]. Further, the distributions of HG volumes of the deaf and hearing groups in this sample were overlapping with those obtained in a previous sample (Penhune et al., 1996) of 20 hearing subjects [F(2,38) = 0.7, P > 0.05]. When the deaf subjects were compared to a combined sample of the current matched controls plus the previous
Discussion
The results of this study are striking in showing preservation of cortical volume in HG and PT of deaf subjects deprived of auditory input since birth. Measurements of grey and white matter, as well as the location and extent of these regions in the deaf, showed complete overlap both with matched controls and with two previous samples of hearing subjects. Most importantly, expected L > R differences in the volume of HG and in the angulation of the PT that are hypothesized to be related to
Acknowledgements
This work was supported by operating grants from the Canadian Institutes of Health Research and postdoctoral fellowship from l'Institut de réadaptation en déficience physique du Québec. We thank the faculty and staff of the McConnell Brain Imaging Centre at the Montreal Neurological Institute for their assistance in acquiring and analyzing the data. In particular, we thank Alex Zijdenbos and Jason Lurch for their assistance in the automatic segmentation and voxel-based analyses.
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Review article: Structural brain alterations in prelingually deaf
2020, NeuroImageCitation Excerpt :Apart from a few reports of altered GM in the auditory areas among the deaf, the majority of studies confirmed the presence of structural alterations in the auditory WM among the deaf. Using manual volumetry, VBM or TBM, some studies reported preserved WM volume (J. Li et al., 2012; Meyer et al., 2007; Penhune et al., 2003), while others observed a statistically significant or insignificant decrease in the WM volume (Emmorey et al., 2003; Hribar et al., 2014; Leporé et al., 2010a; Olulade et al., 2014; Pénicaud et al., 2013; Shibata, 2007; Smith et al., 2011) among deaf subjects. Leporé et al. (2010a) observed a statistically insignificant decrease in the WM volume of the HG and STG and increased WM volume around the primary auditory areas in the deaf, compared to normal–hearing subjects.