Introduction

Early profound deaf children and adolescents have been reported to suffer from cognitive decline ^1-3, attentional deficit ^4-5 and following academic difficulties, which suggest that auditory deprivation may lead to cognitive impairments, especially attentional deficits in profound deaf children and adolescents. Neural correlates of this attention deficits have been little documented. The brain network mechanism of this attention impairment in deaf children and adolescents is not clear yet.

Purpose

To investigate the difference of the resting state functional connectivity (RSFC) of the primary auditory cortex with the attention control networks, default mode network and other cognitive networks in inattentive children and adolescents with bilateral early profound deafness.

Materials and methods

Twenty-five inattentive children and adolescents with bilateral prelingual profound deafness and 30 age- and gender- matched normal controls were scanned at 3.0 T Siemens MAGNETOM Prisma scanner. High-resolution functional images were acquired using the simultaneous multi-slices echo planar imaging (SMS-EPI) sequence and the high-resolution 3D T1-weighted images were acquired using the magnetization-prepared rapid gradient echo (MPRAGE) sequence. Functional connectivity differences of the superior temporal gyrus and transverse temporal gyrus in primary auditory cortex on two groups were analyzed after data preprocess with AFNI⁶. Pearson correlation analyses were then used to explore the correlations of functional connectivity changes with the years of deafness, sign language usage, hearing aid usage.

Results

Compared with hearing controls, the deaf subjects showed significantly decreased functional connectivity between seeds and right anterior cingulate cortex and increased functional connectivity between the right superior temporal gyrus and media frontal gyrus, significantly decreased functional connectivity between seeds and middle temporal gyrus and significantly increased functional connectivity with right precentral gyrus. In addition, we also detected both significantly decreased and increased functional connectivity between seeds and left posterior cingulate cortex, bilateral superior frontal gyrus and inferior temporal gyrus as well as left cerebellar tonsil (Fig 1-4). Our results revealed alterations, mainly decrease in resting-state functional connectivity between the primary auditory cortex and the attention control networks, language comprehension networks, default-mode networks and sensorimotor networks in these deaf subjects. The usage of hearing aid was also found to normalize the connectivity between primary auditory cortex and attention network in these deaf subjects (Fig 5).

Discussion

We found both significantly decreased and increased RSFC between the primary auditory cortex and the nodes of the attention control networks. Our findings are partially consistent with one of the previous rs-fMRI studies by Ding and colleagues⁷. Their study found increased functional connectivity between bilateral STG and attention network in deaf adults. Different from their study, in addition to increased RSFC, we mainly found significantly decreased RSFC between primary auditory cortex and the nodes (ACC and MeFG) of the attentional network. The reason for this difference may be due to difference in the research populations. This study focused on deaf children and adolescents while Ding et al. studied early deaf adults. Both impairment and compensation likely happen during the early years of hearing deprivation. The enhanced functional connectivity between the deprived auditory cortex and the attentional network reported in early deaf adults mainly reflected adaptation and compensatory remodeling following the long-term auditory deprivation. The decreased RSFC between primary auditory and attention control networks may contribute to the fundamental reasons of classroom mis-behavior, impaired speech and language acquisition and other cognitive issues in children and adolescents with profound deafness.
We also found significantly decreased RSFC between the middle temporal gyrus (MTG) and bilateral STG and TTG due to deafness. The MTG is one of the key nodes in the language comprehension and self-perceptual network⁸. In daily life, deaf individuals rely on visual information for communication, such as sign language and lip reading, since auditory based language comprehension is impaired. This impairment would severely derail the language development in children and adolescents with prelingual and profound deafness.
Interestingly, in this study, the right precentral gyrus (PreCG) showed increased RSFC with both the right and left STGs. This result is consistent with previous studies^7,9. Hand and figure movements are critical to the sign language processing. The increased RSFC between the auditory cortex and the right precentral gyrus could be related to the sign language usage in deaf individuals.
Finally, we found significant negative correlation between the duration of the hearing usage and the RSFC between the right TTG and the left MFG. Left MFG is a node of the attention network. This suggests that the compensatory involvement of attention network was reduced over time with the usage of hearing aid. In other words, the hearing function becomes more normal after the usage of hearing aid. This implies that the hearing aid should be used as early as possible as an intervention tool.

Conclusion

Our findings indicated a direct impact of early auditory deprivation on high cognitive related networks. The usage of hearing aid was also found to normalize the connectivity between primary auditory cortex and attention network.

Acknowledgements

This study was supported by National Natural Science Foundation of China (grant number: 81501449). We thank all subjects for their time and effort. We thank Lihua Tai, Xiaocui Wang and Xingxing Fu for their assistance in subject recruitment and hearing testing. We thank Ms. Chunfang Yan and Dr. Xiaoxia Qu in MRI scanning support.