Brain Morphological Modifications in Congenital and Acquired Auditory Deprivation: A Systematic Review and Coordinate-Based Meta-Analysis

Abstract

Neuroplasticity following deafness has been widely demonstrated in both humans and animals, but the anatomical substrate of these changes is not yet clear in human brain. However, it is of high importance since hearing loss is a growing problem due to aging population. Moreover, knowing these brain changes could help to understand some disappointing results with cochlear implant, and therefore could improve hearing rehabilitation. A systematic review and a coordinate-based meta-analysis were realized about the morphological brain changes highlighted by MRI in severe to profound hearing loss, congenital and acquired before or after language onset. 25 papers were included in our review, concerning more than 400 deaf subjects, most of them presenting prelingual deafness. The most consistent finding is a volumetric decrease in gray matter around bilateral auditory cortex. This change was confirmed by the coordinate-based meta-analysis which shows three converging clusters in this region. The visual areas of deaf children is also significantly impacted, with a decrease of the volume of both gray and white matters. Finally, deafness is responsible of a gray matter increase within the cerebellum, especially at the right side. These results are largely discussed and compared with those from deaf animal models and blind humans, which demonstrate for example a much more consistent gray matter decrease along their respective primary sensory pathway. In human deafness, a lot of other factors than deafness could interact on the brain plasticity. One of the most important is the use of sign language and its age of acquisition, which induce among others changes within the hand motor region and the visual cortex. But other confounding factors exist which have been too little considered in the current literature, such as the etiology of the hearing impairment, the speech-reading ability, the hearing aid use, the frequent associated vestibular dysfunction or neurocognitive impairment. Another important weakness highlighted by this review concern the lack of papers about postlingual deafness, whereas it represents most of the deaf population. Further studies are needed to better understand these issues, and finally try to improve deafness rehabilitation.

Keywords: MRI; brain morphology; cochlear implant; deafness/hearing loss; neuroplasticity; sign language (SL); systematic review and meta-analysis.

FIGURE 1

Cochlear implant with its two main components. The external part, which is placed behind the ear, is composed of a microphone, an audio processor, a battery and a coil, kept in place in front of the internal part by a magnet. The internal part is placed during a surgical procedure under general anesthesia. The implant transmits the electrical stimulation to the fibers of the cochlear nerve through electrodes placed in the cochlea (from MED-EL© 2021).

FIGURE 2

Primary auditory pathway and main white matter tracts involved in auditory processing and language. (A) The relays of the auditory pathway are the cochlear nuclei, the superior olivary complex, the nuclei of the lateral lemniscus for some neurons, the inferior colliculus and the medial geniculate nucleus of the thalamus. The 8th cranial nerve finally reaches the auditory cortex in the superior temporal gyrus. The major part of the fibers from the cochlea cross the medial line at different levels of the neuraxis and arrive in contralateral auditory cortex. (B) The main intrahemispheric white matter bundles involved in auditory processing and language are the superior longitudinal fasciculus (SLF), the inferior fronto-occipital fasciculus (IFOF), and the uncinate fasciculus (UF), schematically represented here (Maffei et al., 2015).

FIGURE 3

Modifications in the auditory cortex in early- and late-deaf cats. Cytoarchitectonic study showing that A1 is reduced in both early- and late-deaf cats (#) compared to hearing cats. Additionally, in early-deaf cats, A2 and VAF are larger (*), whereas fAES is smaller compared to normal hearing cats (°). Data adapted from Wong et al. (2014) with permission of the author and publisher.

FIGURE 4

Study flowchart according to PRISMA 2020.

FIGURE 5

Morphometric changes in the human deaf brain. Increases in GM or WM volume in the deaf compared to hearing controls are shown in red, decreases in blue. (A) GM and WM volume in deaf children; (B) cortical thickness in deaf children; (C) GM and WM volume in deaf adults; (D) cortical thickness in deaf adults. The image shows the peak (or center) of the areas with modifications in volume or cortical thickness; cluster volumes are not indicated. Some spheres appear smaller because they are shown on slices which are not positioned at the center of the spheres. Right hemisphere is shown on the right of the images. The numbers on top of the slices show the y-coordinates of the coronal slices in MNI space. The numbers inside the slices correspond to the studies from which the coordinates are taken. 1: Li J. et al. (2012); 2: Feng et al. (2018); 3: Smith et al. (2011); 4: Li et al. (2013); 5: Qi et al. (2019); 6: Kim et al. (2009); 7: Olulade et al. (2014); 8: Kumar and Mishra (2018); 9: Leporé et al. (2010a); 10: Hribar et al. (2014).

FIGURE 6

Cerebellar anatomy. (A) Sagittal section of the human brain and cerebellum. The arrows show the way the cerebellum is unfolded. (B) Flatmap representation of the unfolded cerebellum, using both the classification of Larsell (1952) and the classical nomenclature of the human cerebellum (Malacarne, 1791; Reil, 1808; Burdach, 1829).

FIGURE 7

ALE meta-analysis of changes in GM and WM density in the deaf brain. Right hemisphere is shown on the right in the images. The numbers on top of the slices show the y-coordinates of the coronal slices in MNI space. Three clusters of decreased volume in deaf were found significant, and none of increased volume (p < 0.01, cluster-level family-wise error p < 0,05). They are situated in both STG and adjacent middle temporal gyrus and insula, and involve mainly WM. The numbers correspond to those indicated in Table 1.