Functional magnetic resonance imaging of enhanced central auditory gain and electrophysiological correlates in a behavioral model of hyperacusis

• Published in: Hearing research Vol. 389; p. 107908
• Main Authors: Wong, Eddie, Radziwon, Kelly, Chen, Guang-Di, Liu, Xiaopeng, Manno, Francis AM, Manno, Sinai HC, Auerbach, Benjamin, Wu, Ed X., Salvi, Richard, Lau, Condon
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.04.2020
• Subjects: Acoustic Stimulation; Animals; Auditory Pathways - diagnostic imaging; Auditory Pathways - physiopathology; Behavior, Animal; Brain - diagnostic imaging; Brain - physiopathology; Brain Mapping; Central auditory gain; Disease Models, Animal; Electroencephalography; Evoked Potentials, Auditory; fMRI; Functional magnetic resonance imaging; Hyperacusis; Hyperacusis - diagnostic imaging; Hyperacusis - physiopathology; Hyperacusis - psychology; Loudness Perception; Magnetic Resonance Imaging; Male; Predictive Value of Tests; Rat; Rats, Sprague-Dawley; Reaction Time; Time Factors; Hyperacusis; Functional magnetic resonance imaging; fMRI; Central auditory gain; Rat
• ISSN: 0378-5955; 1878-5891
• DOI: 10.1016/j.heares.2020.107908

Hyperacusis is a debilitating hearing condition in which normal everyday sounds are perceived as exceedingly loud, annoying, aversive or even painful. The prevalence of hyperacusis approaches 10%, making it an important, but understudied medical condition. To noninvasively identify the neural correlates of hyperacusis in an animal model, we used sound-evoked functional magnetic resonance imaging (fMRI) to locate regions of abnormal activity in the central nervous system of rats with behavioral evidence of hyperacusis induced with an ototoxic drug (sodium salicylate, 250 mg/kg, i.p.). Reaction time-intensity measures of loudness-growth revealed behavioral evidence of salicylate-induced hyperacusis at high intensities. fMRI revealed significantly enhanced sound-evoked responses in the auditory cortex (AC) to 80 dB SPL tone bursts presented at 8 and 16 kHz. Sound-evoked responses in the inferior colliculus (IC) were also enhanced, but to a lesser extent. To confirm the main results, electrophysiological recordings of spike discharges from multi-unit clusters were obtained from the central auditory pathway. Salicylate significantly enhanced tone-evoked spike-discharges from multi-unit clusters in the AC from 4 to 30 kHz at intensities ≥60 dB SPL; less enhancement occurred in the medial geniculate body (MGB), and even less in the IC. Our results demonstrate for the first time that non-invasive sound-evoked fMRI can be used to identify regions of neural hyperactivity throughout the brain in an animal model of hyperacusis. •In hyperacusis, sounds are perceived as exceedingly loud, frightening, or painful.•Prevalence of hyperacusis approaches 10%.•Sound-evoked fMRI developed to locate abnormal brain activity in hyperacusis rats.•Enhanced central auditory gain observed and confirmed electrophysiologically.•Animal fMRI advances basic research and connects human fMRI data with animal data.