The gradient in gray matter thickness across auditory cortex and differential cortical thickness changes following perinatal deafness

Abstract

In the absence of hearing during development, the brain adapts and repurposes what was destined to become auditory cortex. As cortical thickness is commonly used as a proxy to identify cortical regions that have undergone plastic changes, the purpose of this investigation was to compare cortical thickness patterns between hearing and deaf cats. In this study, normal hearing (n = 29) and deaf (n = 26) cats were scanned to examine cortical thickness in hearing controls, as well as differential changes in thickness as a consequence of deafness. In hearing cats, a gradient in cortical thickness was identified across auditory cortex in which it is thinner in more dorsal regions and thicker in more ventral regions. Compared with hearing controls, differential thickening and thinning was observed in specific regions of deaf auditory cortex. More dorsal regions were found to be bilaterally thicker in the deaf group, while more ventral regions in the left hemisphere were thinner. The location and nature of these changes creates a gradient along the dorsoventral axis, wherein dorsal auditory cortical fields are thicker, whereas more ventral fields are thinner in deaf animals compared with hearing controls.

Keywords: MRI; cat; cortical thickness; gray matter; plasticity.

Fig. 1

Scatterplots of mean thickness before a) and after b) linear age regression. Each point represents one subject, with hearing cats indicated in blue and deaf cats in red.

Fig. 2

Mean cortical thickness values for each auditory region. Regions sorted based on dorsoventral position in the brain, with more dorsal regions being on the left. Blue downward pointing arrows () indicate significant decreased thicknesses in the deaf group and red upward pointing arrows () indicate increased thickness. Data presented as mean + SEM. ^P < 0.05, ^^P < 0.01 between the hearing and deaf conditions.

Fig. 3

Visual representation of mean thicknesses and thickness differences between the two groups. ROIs in the hearing left a) and right b) hemispheres and deaf left c) and right d) hemispheres are shown with mean thicknesses in mm. Thickness differences between the two groups in the left e) and right f) hemispheres shown as deaf mean minus hearing mean for each ROI in mm, with solid colors denoting significant changes (Table 1). The dorsal zone (DZ), dorsal and posterior divisions of posterior ectosylvian auditory cortex (dPE, pPE), primary auditory cortex (A1), and secondary auditory cortex (A2) were all significantly thicker in the deaf group bilaterally. Temporal auditory cortex (T) and the VPAF were found to be significantly thinner in the left hemisphere only.

Fig. 4

Thickness change versus vertical position of auditory ROIs in the brain. Thickness change was calculated as mean thickness of each ROI in the hearing group minus mean thickness in the deaf group. A linear line of best fit with properties R² = 0.7579, P = 1.726 × 10⁻⁹ shows that the more dorsal in the brain a region is the more likely that it is thicker in the deaf group and vice versa. Image in top right is a lateral view of the left hemisphere of the cat brain with auditory regions labeled. For all full ROI names, refer to the list of abbreviations provided. L or R at the end of each abbreviation indicates left or right hemisphere, respectively.