Sep 28, 2014 - no data about the use of HA at all (Leporé et al., 2010; Penhune et al., 2003 ...... Allen, J.S., Emmore
Hearing Research 318 (2014) 1e10
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Research paper
Structural alterations of brain grey and white matter in early deaf adults a, b Manja Hribar a, Dusan Suput , Altiere Araujo Carvalho c, Saba Battelino d, Andrej Vovk a, * a
Center for Clinical Physiology, Faculty of Medicine, University of Ljubljana, Slovenia Institute of Pathophysiology, Faculty of Medicine, University of Ljubljana, Slovenia ~o Paulo, Brazil Faculdades Metropolitanas Unidas, FMU, Sa d Department of Otorhinolaryngology, Faculty of Medicine, University of Ljubljana, Slovenia b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 March 2014 Received in revised form 11 September 2014 Accepted 16 September 2014 Available online 28 September 2014
Functional and structural brain alterations in the absence of the auditory input have been described, but the observed structural brain changes in the deaf are not uniform. Some of the previous researchers focused only on the auditory areas, while others investigated the whole brain or other selected regions of interest. Majority of studies revealed decreased white matter (WM) volume or altered WM microstructure and preserved grey matter (GM) structure of the auditory areas in the deaf. However, preserved WM and increased or decreased GM volume of the auditory areas in the deaf have also been reported. Several structural alterations in the deaf were found also outside the auditory areas, but these regions differ between the studies. The observed differences between the studies could be due to the use of different single-analysis techniques, or the diverse population sample and its size, or possibly due to the usage of hearing aids by some participating deaf subjects. To overcome the aforementioned limitations four different image-processing techniques were used to investigate changes in the brain morphology of prelingually deaf adults who have never used hearing aids. GM and WM volume of the Heschl's gyrus (HG) were measured using manual volumetry, while whole brain GM volume, thickness and surface area were assessed by voxel-based morphometry (VBM) and surface-based analysis. The microstructural properties of the WM were evaluated by diffusion tensor imaging (DTI). The data were compared between 14 congenitally deaf adults and 14 sex- and age-matched normal hearing controls. Manual volumetry revealed preserved GM volume of the bilateral HG and significantly decreased WM volume of the left HG in the deaf. VBM showed increased cerebellar GM volume in the deaf, while no statistically significant differences were observed in the GM thickness or surface area between the groups. The results of the DTI analysis showed WM microstructural alterations between the groups in the bilateral auditory areas, including the superior temporal gyrus, the HG, the planum temporale and the planum polare, which were more extensive in the right hemisphere. Fractional anisotropy (FA) was significantly reduced in the right and axial diffusivity (AD) in the left auditory areas in the deaf. FA and AD were significantly reduced also in several other brain areas outside the auditory cortex in the deaf. The use of four different methods used in our study, although showing changes that are not directly related, provides additional information and supports the conclusion that in prelingually deaf subjects structural alterations are present both in the auditory areas and elsewhere. Our results support the findings of those studies showing that early deafness results in decreased WM volume and microstructural WM alterations in the auditory areas. As we observed WM microstructural alteration also in several other areas and increased GM volume in the cerebellum in the deaf, we can conclude that early deafness results in widespread structural brain changes. These probably reflect atrophy or degradation as well as compensatory cross-modal reorganisation in the absence of the auditory input and the use of the sign language. © 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-SA license (http://creativecommons.org/licenses/by-nc-sa/3.0/).
Abbreviations: AD, axial diffusivity; CC, corpus callosum; CMC, correction for multiple comparisons; DTI, diffusion tensor imaging; FA, fractional anisotropy; GM, grey matter; HA, hearing aid; HG, Heschl's gyrus; PP, planum polare; PT, planum temporale; RD, radial diffusivity; STG, superior temporal gyrus; SMG, supramarginal gyrus; SFG, superior frontal gyrus; VBM, voxel-based morphometry; WM, white matter * Corresponding author. Center for Clinical Physiology, Faculty of Medicine, University of Ljubljana, Vrazov trg 2, Slovenia. Tel.: þ386 15437821; fax: þ386 15437822. E-mail address:
[email protected] (A. Vovk). http://dx.doi.org/10.1016/j.heares.2014.09.008 0378-5955/© 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-SA license (http://creativecommons.org/licenses/by-nc-sa/3.0/).
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M. Hribar et al. / Hearing Research 318 (2014) 1e10
1. Introduction Sensory inputs such as hearing, vision and touch play important roles in human brain development. It is not yet fully understood what happens with the structure and function of the auditory cortex and other brain regions in the absence of the auditory input. Functional neuroimaging studies have shown that in individuals who lack one sensory modality another such modality can 'take over' the latter's cortical area. For example, in deaf subjects the auditory cortex can be activated by sign language comprehension and production (Neville et al., 1998; Nishimura et al., 1999; Sadato -Robertson et al., 2004), non-linguistic et al., 2004; San Jose motionless as well as moving visual stimuli (Finney et al., 2001; Karns et al., 2012; Vachon et al., 2013), vibrotactile stimuli (Lev€ anen et al., 1998) and somatosensory stimuli (Karns et al., 2012). Furthermore, the enhancement of other senses, such as €nen and Hamdorf, 2001), better increased tactile sensitivity (Leva peripheral vision skills (Bavelier et al., 2006) and better visual motion detection (Hauthal et al., 2013; Shiell et al., 2014) in deaf subjects and animals (Lomber et al., 2010) were also reported. These functional and behavioural changes are probably accompanied by underlying structural changes, waiting to be discovered. Recently, a post-mortem anatomical study revealed the presence of cytoarchitectonic alterations in the auditory cortex of deaf cats, related to the onset age of deafness (Wong et al., 2013). Postmortem studies on animals can give us a unique insight into the fine structural brain changes. On the other hand evaluation of structural brain changes in humans depends almost exclusively on non-invasive imaging methods. Most of the previous volumetry based studies revealed preserved grey matter (GM) volume of the auditory cortex in deaf (Emmorey et al., 2003; Kim et al., 2009; et al., 2010; Li et al., 2012a; Penhune et al., 2003; Lepore nicaud et al., 2012; Shibata, 2007), but increased GM volume in Pe the deaf infants (Smith et al., 2011) and decreased GM volume in the deaf adults (Olulade et al., 2014) has also been reported. Findings about the WM volume in the auditory areas are also not uniform. Some researchers reported decreased WM volume in the Heschl's gyrus (HG) (Emmorey et al., 2003) or in the STG (Shibata, 2007) in deaf, while others found no alterations between the deaf and normal hearing subjects (Penhune et al., 2003). Volumetric changes in various areas outside the auditory cortex have also been et al., 2010; Li et al., reported in the WM (Kim et al., 2009; Lepore 2012a) as well as in the GM (Allen et al., 2013; Olulade et al., 2014) in the deaf. Given that most changes were found in the WM, it is reasonable to explore these alterations further. Diffusion tensor imaging (DTI) allows better estimation of the microstructure and architectural organization of different tissues using the diffusion properties of water molecules (Basser et al., 1994). In anisotropic media, such as brain WM, the diffusivity of water molecules is limited by the tissue boundaries. In WM these boundaries are myelin and membranes, which cause increased diffusion in the direction of the fibres relative to the diffusion perpendicular to the direction of fibres (Le Bihan et al., 2001). The properties of WM, such as axon diameter and myelination, can be expressed by means of fractional anisotropy (FA), axial diffusivity (AD), and radial diffusivity (RD) (Song et al., 2002). Up to now three studies have used DTI to explore alterations of the cortical WM in the absence of auditory input (Kim et al., 2009; Li et al., 2012b; Miao et al., 2013). All three studies showed decreased FA values in the right or in the bilateral auditory cortex in the deaf subjects. Altered FA was described also outside the auditory areas, but in different regions in every study. The observed discrepancies between the results of the previous studies investigating structural brain plasticity in the absence of the
auditory input may be related to the use of the hearing aids (HA) in participating hearing-impaired subjects. In one study all the deaf participants wore HA for different periods of time (Miao et al., 2013), whereas in others there are only data about not wearing HA during the brain developing period in the first few years of life (Emmorey et al., 2003; Kim et al., 2009; Li et al., 2012b), or there is et al., 2010; Penhune no data about the use of HA at all (Lepore et al., 2003; Shibata, 2007). Functional and anatomical brain changes due to the use of the HA and cochlear implants have been reported in the deaf children as well as in the deaf adults (Connor et al., 2006; Fallon et al., 2008; Kral and Sharma, 2012; Li et al., 2013a; Philibert et al., 2002; Ponton et al., 2001; Syka, 2002). So the possible structural changes and neuronal plasticity due to the absence of auditory input can be best assessed in the early deaf individuals who have never used HA. As most previously mentioned studies employed different single analysis approaches, like voxel-based morphometry (VBM), tensor-based morphometry (TBM) and DTI, which cover only one aspect of the brain structural property at a time, interpretation of the results is therefore limited and may be difficult to compare (Li et al., 2012a; Penhune et al., 2003; Shibata, 2007). Our aim was to assess structural alterations in a well-defined group of prelingually deaf adults who had never used HA. To overcome the limitations of individual analytical approaches, four different image-processing techniques were employed, including manual volumetry of the primary auditory cortex e HG, automatic volumetry (VBM) of the whole-brain GM, surface-based analysis (including thickness, surface area and volume) of the whole-brain GM and the whole brain DTI. So far the combination of these four techniques has not yet been used to investigate structural brain changes in deaf adults.
2. Materials and methods 2.1. Subjects Fourteen deaf adults (8 females, 6 males; age range 23e50 years, mean age 35.4 ± 6) and 14 normal hearing control subjects (8 females, 6 males; age range 23e50 years, mean age 30.5 ± 5.2 years) participated in the study. All the deaf individuals exhibited a profound hearing loss (
