Age-related hearing loss increases full-brain connectivity while reversing directed signaling within the dorsal–ventral pathway for speech

• Published in: Brain Structure and Function 2019-11, Vol.224 (8), p.2661-2676
• Main Authors: Bidelman, Gavin M., Mahmud, Md Sultan, Yeasin, Mohammed, Shen, Dawei, Arnott, Stephen R., Alain, Claude
• Format: Article
• Language: English
• Subjects: Acoustic Stimulation; Aged; Aging; Aging - physiology; Aging - psychology; Audiometry; Biomedical and Life Sciences; Biomedicine; Brain - physiopathology; Brain Mapping - methods; Cell Biology; Comprehension - physiology; Cortex (auditory); Cortex (frontal); Cortex (motor); EEG; Electroencephalography; Evoked Potentials, Auditory; Female; Frontal gyrus; Hearing loss; Hearing Loss - physiopathology; Hearing protection; Hemispheric laterality; Humans; Male; Middle Aged; Neural networks; Neural Pathways - physiopathology; Neurology; Neurosciences; Older people; Original Article; Signal transduction; Speech; Speech Perception - physiology
• ISSN: 1863-2653; 1863-2661; 0340-2061
• DOI: 10.1007/s00429-019-01922-9

Speech comprehension difficulties are ubiquitous to aging and hearing loss, particularly in noisy environments. Older adults’ poorer speech-in-noise (SIN) comprehension has been related to abnormal neural representations within various nodes (regions) of the speech network, but how senescent changes in hearing alter the transmission of brain signals remains unspecified. We measured electroencephalograms in older adults with and without mild hearing loss during a SIN identification task. Using functional connectivity and graph-theoretic analyses, we show that hearing-impaired (HI) listeners have more extended (less integrated) communication pathways and less efficient information exchange among widespread brain regions (larger network eccentricity) than their normal-hearing (NH) peers. Parameter optimized support vector machine classifiers applied to EEG connectivity data showed hearing status could be decoded (> 85% accuracy) solely using network-level descriptions of brain activity, but classification was particularly robust using left hemisphere connections. Notably, we found a reversal in directed neural signaling in left hemisphere dependent on hearing status among specific connections within the dorsal–ventral speech pathways. NH listeners showed an overall net “bottom-up” signaling directed from auditory cortex (A1) to inferior frontal gyrus (IFG; Broca’s area), whereas the HI group showed the reverse signal (i.e., “top-down” Broca’s → A1). A similar flow reversal was noted between left IFG and motor cortex. Our full-brain connectivity results demonstrate that even mild forms of hearing loss alter how the brain routes information within the auditory–linguistic–motor loop.