Tinnitus and hyperacusis involve hyperactivity and enhanced connectivity in auditory-limbic-arousal-cerebellar network

Author:

Chen Yu-Chen1,Li Xiaowei2,Liu Lijie2,Wang Jian23,Lu Chun-Qiang1,Yang Ming1,Jiao Yun1,Zang Feng-Chao1,Radziwon Kelly4,Chen Guang-Di4,Sun Wei4,Krishnan Muthaiah Vijaya Prakash4,Salvi Richard4,Teng Gao-Jun1

Affiliation:

1. Jiangsu Key Laboratory of Molecular Imaging and Functional Imaging, Department of Radiology, Zhongda Hospital, Medical School, Southeast University, Nanjing, China

2. Department of Physiology, Southeast University, Nanjing, China

3. School of Human Communication Disorders, Dalhousie University, Halifax, Canada

4. Center for Hearing and Deafness, University at Buffalo, The State University of New York, Buffalo, United States

Abstract

Hearing loss often triggers an inescapable buzz (tinnitus) and causes everyday sounds to become intolerably loud (hyperacusis), but exactly where and how this occurs in the brain is unknown. To identify the neural substrate for these debilitating disorders, we induced both tinnitus and hyperacusis with an ototoxic drug (salicylate) and used behavioral, electrophysiological, and functional magnetic resonance imaging (fMRI) techniques to identify the tinnitus–hyperacusis network. Salicylate depressed the neural output of the cochlea, but vigorously amplified sound-evoked neural responses in the amygdala, medial geniculate, and auditory cortex. Resting-state fMRI revealed hyperactivity in an auditory network composed of inferior colliculus, medial geniculate, and auditory cortex with side branches to cerebellum, amygdala, and reticular formation. Functional connectivity revealed enhanced coupling within the auditory network and segments of the auditory network and cerebellum, reticular formation, amygdala, and hippocampus. A testable model accounting for distress, arousal, and gating of tinnitus and hyperacusis is proposed.

Funder

Ministry of Science and Technology of the People's Republic of China

National Natural Science Foundation of China

Natural Science Foundation of Jiangsu Province

Fundamental Research Funds for the Central Universities and Jiangsu Graduate Student Innovation Grant

National Institutes of Health (NIH)

China Scholarship Council

Ministry of Education of the People's Republic of China

Office of Naval Research

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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