Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model

Abstract

BackgroundHearing loss was proposed as a factor affecting development of cognitive impairment in elderly. Deficits cannot be explained primarily by dysfunctional neuronal networks within the central auditory system. We here tested the impact of hearing loss in adult rats on motor, social, and cognitive function. Furthermore, potential changes in the neuronal activity in the medial prefrontal cortex (mPFC) and the inferior colliculus (IC) were evaluated.Materials and methodsIn adult male Sprague Dawley rats hearing loss was induced under general anesthesia with intracochlear injection of neomycin. Sham-operated and naive rats served as controls. Postsurgical acoustically evoked auditory brainstem response (ABR)-measurements verified hearing loss after intracochlear neomycin-injection, respectively, intact hearing in sham-operated and naive controls. In intervals of 8 weeks and up to 12 months after surgery rats were tested for locomotor activity (open field) and coordination (Rotarod), for social interaction and preference, and for learning and memory (4-arms baited 8-arms radial maze test). In a final setting, electrophysiological recordings were performed in the mPFC and the IC.ResultsLocomotor activity did not differ between deaf and control rats, whereas motor coordination on the Rotarod was disturbed in deaf rats (P < 0.05). Learning the concept of the radial maze test was initially disturbed in deaf rats (P < 0.05), whereas retesting every 8 weeks did not show long-term memory deficits. Social interaction and preference was also not affected by hearing loss. Final electrophysiological recordings in anesthetized rats revealed reduced firing rates, enhanced irregular firing, and reduced oscillatory theta band activity (4–8 Hz) in the mPFC of deaf rats as compared to controls (P < 0.05). In the IC, reduced oscillatory theta (4–8 Hz) and gamma (30–100 Hz) band activity was found in deaf rats (P < 0.05).ConclusionMinor and transient behavioral deficits do not confirm direct impact of long-term hearing loss on cognitive function in rats. However, the altered neuronal activities in the mPFC and IC after hearing loss indicate effects on neuronal networks in and outside the central auditory system with potential consequences on cognitive function.

Hearing loss in juvenile rats leads to excessive play fighting and hyperactivity, mild cognitive deficits and altered neuronal activity in the prefrontal cortex

“…An alternative explanation could be that these behaviors reflect an adaptive strategy to access information from the environment that is not available through hearing. Interestingly, hearing loss induced in adult rats had no effect on motor activity except for a transient increase in the distance walked in the open field one month after deafening (Johne et al, 2022). On the other hand, adult deafened rats were impaired on the Rotarod, a test traditionally used to assess balance deficits in rodents (Brooks et al, 2012;Hamm et al, 1994), while juvenile deafened rats did not differ from sham-and naïve controls.…”

“…Signals were additionally filtered (300-3000 Hz). ABRs were determined manually by appearance of ABR components 2 -3 ms after stimulus onset (Johne et al, 2022;Schopf et al, 2014;Tillein et al, 2012).…”

“…Electrophysiological recordings were performed with a similar setup as previously used in adult deafened rats (Johne et al, 2022). For extracellular measurements of SU neuronal activity and recording of LFPs, rats were anesthetized with urethane (1.4 g/kg in 0.9% NaCl, i.p.…”

“…A rodent model provides the opportunity to investigate the causality between hearing loss and cognitive function in juvenile rats and their development in a controlled environment, without the influence of language. Longitudinal studies of adult rat behavior after hearing loss showed only a mild effect on learning the concept of a radial arm maze task, transient hyperactivity, and no effect on social interaction (Johne et al, 2022). Early life insults, however, not only induce compensatory changes but also lead to compromised functional integrity of neural networks developing after birth with behavioral, neurophysiological and neuroanatomical consequences (Harich et al, 2008;Helgers et al, 2020), with the influence of hearing playing an important role (Kral et al, 2005;Kral & Sharma, 2012).…”

“…Furthermore, it is anatomically and reciprocally connected to virtually all sensory and motor systems, as well as to a variety of subcortical structures (Fassbender & Schweitzer, 2006;Li et al, 2015;Miller & Cohen, 2001;Russo & Nestler, 2013). In rats with induced hearing loss in adulthood, electrophysiological recordings in the medial PFC (mPFC) showed substantially altered neuronal activity, both at the neuronal and network level (Johne et al, 2022).…”