Abstract
It remains poorly understood how brain causal connectivity networks change following hearing loss and their effects on cognition. In the current study, we investigated this issue. Twelve patients with long-term bilateral sensorineural hearing loss [mean age, 55.7 ± 2.0; range, 39–63 years; threshold of hearing level (HL): left ear, 49.0 ± 4.1 dB HL, range, 31.25–76.25 dB HL; right ear, 55.1 ± 7.1 dB HL, range, 35–115 dB HL; the duration of hearing loss, 16.67 ± 4.5, range, 3–55 years] and 12 matched normally hearing controls (mean age, 52.3 ± 1.8; range, 42–63 years; threshold of hearing level: left ear, 17.6 ± 1.3 dB HL, range, 11.25–26.25 dB HL; right ear, 19.7 ± 1.3 dB HL, range, 8.75–26.25 dB HL) participated in this experiment. We constructed and analyzed the causal connectivity networks based on functional magnetic resonance imaging data of these participants. Two-sample t-tests revealed significant changes of causal connections and nodal degrees in the right secondary visual cortex, associative visual cortex, right dorsolateral prefrontal cortex, left subgenual cortex, and the left cingulate cortex, as well as the shortest causal connectivity paths from the right secondary visual cortex to Broca’s area in hearing loss patients. Neuropsychological tests indicated that hearing loss patients presented significant cognitive decline. Pearson’s correlation analysis indicated that changes of nodal degrees and the shortest causal connectivity paths were significantly related with poor cognitive performances. We also found a cross-modal reorganization between associative visual cortex and auditory cortex in patients with hearing loss. Additionally, we noted that visual and auditory signals had different effects on neural activities of Broca’s area, respectively. These results suggest that changes in brain causal connectivity network are an important neuroimaging mark of cognitive decline. Our findings provide some implications for rehabilitation of hearing loss patients.
Highlights
IntroductionBehavioral studies have reported that individuals with early or congenitally hearing loss are highly reliant on their remaining intact sensory modalities to interact with their surrounding environment (Merabet and Pascual-Leone, 2010) and displayed superior visual behavioral performing skills compared with normal-hearing controls, such as enhanced peripheral attention to moving stimuli (Neville and Lawson, 1987; Bavelier et al, 2000; Proksch and Bavelier, 2002; Dye et al, 2009) and increased performance abilities in visual motion detection (Hauthal et al, 2013; Shiell et al, 2014, 2016)
Our study focused on the shortest causal connectivity paths between the visual cortex, auditory cortex, and those brain areas associated with speech processing
The present study investigated adult-onset hearing loss and its effects on the connectivity in the brain using restingstate functional magnetic resonance imaging
Summary
Behavioral studies have reported that individuals with early or congenitally hearing loss are highly reliant on their remaining intact sensory modalities to interact with their surrounding environment (Merabet and Pascual-Leone, 2010) and displayed superior visual behavioral performing skills compared with normal-hearing controls, such as enhanced peripheral attention to moving stimuli (Neville and Lawson, 1987; Bavelier et al, 2000; Proksch and Bavelier, 2002; Dye et al, 2009) and increased performance abilities in visual motion detection (Hauthal et al, 2013; Shiell et al, 2014, 2016). An animal study indicated that those improvements in visual performances were caused by cross-modal functional reorganization of auditory cortex in individuals with early or congenitally hearing loss, and several experimental approaches had been used to localize individual visual functions in discrete portions of reorganized auditory cortex (Lomber et al, 2010). The structural connectivity changes between visual and auditory cortices contribute to reduced restingstate alpha band activity in the posterior auditory field (Yusuf et al, 2017) and reduced stimulus-related effective connectivity from higher-order auditory cortical areas involved in the crossmodal reorganization to primary areas (Yusuf et al, 2021) in congenitally hearing loss cats
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