Elsevier

NeuroImage

Volume 19, Issue 3, July 2003, Pages 777-783
NeuroImage

Regular article
Developmental hemispheric asymmetry of interregional metabolic correlation of the auditory cortex in deaf subjects

https://doi.org/10.1016/S1053-8119(03)00118-6Get rights and content

Abstract

The functional connectivity of the auditory cortex might be altered in deaf subjects due to the loss of auditory input. We studied the developmental changes of functional connectivity of the primary auditory cortex (A1) in deaf children, deaf adults, and normal hearing adults by examining interregional metabolic correlation with 18F-FDG PET. The mean activity of FDG uptake in the cytoarchitectonically defined A1 region served as a covariate in the interregional and interhemispheric correlation analysis. A1 metabolic rate was correlated with that of the ipsilateral superior temporal lobe in both normal and deaf subjects. This correlated area was larger in deaf children than in deaf or normal hearing adults. Concerning the functional connectivity of A1, a hemispheric asymmetry was found in that the extent of interregional correlation was clearly larger in the right than in the left hemisphere. This asymmetry was particularly pronounced in the younger deaf children. Both extent and asymmetry of the functional connectivity of A1 subsided with age. Contrary to this, a correlation between the left and the right primary auditory cortices was absent in younger deaf children but became apparent as they grew older.

Introduction

Early perception of auditory information is critical for the normal development of the auditory cortex and its connections with other brain regions (Truy, 1999). The auditory cortex develops in association with related cortical areas. Interregional and cross-callosal correlations develop or subside with age, and regional organization and functional connectivity are achieved in adults. Synaptic revision and intermodal or top-down modulation both play roles throughout early development, during which A1 and related brain regions become engaged in auditory processing and language functions. Unlike normal hearing children, deaf children might show unusual interregional correlations due to the differential growth of the diverse sensory modalities.

While auditory cortical glucose metabolism decreases in postlingual deaf adults (Ito et al., 1990), in deaf children it can vary widely depending on individual characteristics Lee et al 2001, Catalan-Ahumada et al 1993, Hirano et al 2000. This individual variation was correlated with the degree to which hearing and speech capabilities were recovered following cochlear implantation (Lee et al., 2001). Before implantation, metabolism in auditory cortex was decreased initially but recovered later, which might indicate cortical plasticity either of the same (cross-modal), lower (bottom-up), or higher level (top-down) reorganization. Auditory cortical hypermetabolism could indicate greater synaptic density due to either a delayed or an absent synaptic pruning by auditory deprivation during early developmental age (Hirano et al., 2000). Greater synaptic density is, in turn, associated with greater glucose metabolism Chugani et al 1987, Chugani 1998.

The synaptic density within the primary auditory cortex in either hemisphere as well as the connectivity between A1 and other brain regions might differ between deaf and normal hearing subjects. That is, the way in which A1 is functionally connected to other brain regions in deaf subjects may or may not be different from normal hearing individuals. Examination of the interregional relationship of the auditory cortex (A1) with other brain areas in deaf subjects would provide an opportunity to study the developmental changes in the functional connectivity of A1 both within and between hemispheres (Schreckenberger et al., 1998).

Precise anatomical delineation of the auditory cortex, however, is a prerequisite for an interregional correlation analysis. Fortunately, a stereotactic probabilistic map of cytoarchitectonic area Te1 was recently published Morosan et al 2001, Rademacher et al 2001. This map is based on an observer-independent definition of cytoarchitectonical borders in a sample of 10 human postmortem brains Morosan et al 2001, Rademacher et al 2001. In this study, using this probability map as a spatial template (covariate), interregional metabolic correlation of A1 was examined in an objective manner.

In order to understand how the deprivation of auditory input in deaf subjects influences interregional or cross-callosal functional connectivity during development, we examined four groups: two deaf children groups (younger deaf children who are 6 years old or younger and older deaf children from 7 to 16 years old), a postlingual deaf adult group, and a normal hearing adult group.

Section snippets

Materials and methods

18F-FDG positron emission tomography (PET) scan was performed for the deaf patient as a clinical presurgical evaluation in the Seoul National University hospital since the PET results served as an inclusion criterion for cochlear implantation surgery (Lee et al., 2001). Sufficient and detailed explanations for the procedure, risk, and purpose/benefit of FDG-PET study as an evaluation method for prediction of postsurgical outcome were given to the adult patients or the parents of child patients

Results

Adult deaf subjects showed a significantly lower metabolism within the A1 (54.2 ± 0.49 in left; 54.0 ± 0.66 in right) than normal hearing adults (55.9 ± 0.28 in left; 55.6 ± 0.33 in right) (P < 0.05, Fig. 1). The average glucose metabolism of either deaf children group was not significantly lower than normal hearing adults.

In all subjects, the ipsilateral superior temporal lobe showed a significant positive correlation with A1, which is probably due to interregional autocorrelation (P < 0.05,

Discussion

Our findings based on the deaf children data suggest that the functional connectivity of the primary auditory cortex with adjacent regions was more extensive in right hemisphere than in left and it decreases with advancing age. The extensive connectivity found in deaf children was greater in younger than in older children. No evidence indicating functional connectivity between the left and the right A1 was found in younger deaf children. The cross-hemispheric connectivity was observed only with

Acknowledgements

This study was supported by the BK21 (D.L.) project of the Korean Ministry of Education and the Brain Science Project (E.K.) of the Ministry of Science and Technology.

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