Age‐related changes in the guinea pig auditory cortex: relationship with brainstem changes and comparison with tone‐induced hearing loss

Abstract

Elderly people often show degraded hearing performance and have difficulties in understanding speech, particularly in noisy environments. Although loss in peripheral hearing sensitivity is an important factor in explaining these low performances, central alterations also have an impact but their exact contributions remained unclear. In this study, we focus on the functional effects of aging on auditory cortex responses. Neuronal discharges and local field potentials were recorded in the auditory cortex of aged guinea pigs (> 3 years), and several parameters characterizing the processing of auditory information were quantified: the acoustic thresholds, response strength, latency and duration of the response, and breadth of tuning. Several of these parameters were also quantified from auditory brainstem responses collected from the same animals, and recordings obtained from a population of animals with trauma-induced hearing loss were also included in this study. The results showed that aging and acoustic trauma reduced the response strength at both brainstem and cortical levels, and increased the response latencies more at the cortical level than at the brainstem level. In addition to the brainstem hearing loss, aging induced a 'cortical hearing loss' as judged by additive changes in the threshold and frequency response seen in the cortex. It also increased the duration of neural responses and reduced the receptive field bandwidth, effects that were not found in traumatized animals. These effects substantiate the notion that presbycusis involves both peripheral hearing loss and biological aging in the central auditory system.

Neural correlates of moderate hearing loss: time course of response changes in the primary auditory cortex of awake guinea-pigs

“…We compared the ABRs obtained from our hearing impaired animals with a large database of ABRs obtained (with exactly the same equipment) in control guinea pigs ( n = 46) of the same age (4.7 ± 0.6 months) and weight (585 ± 113 g) than the ones used here. The control animals had typical ABR audiograms similar to those previously published (Gourévitch et al, 2009; Gourévitch and Edeline, 2011). Compared to control animals, the animals used in the present experiment had a consistent hearing deficit (15–20 dB on average) in the 4–8 kHz range (Figure 1).…”

“…Auditory brainstem responses (ABRs) were recorded as previously described (Gourévitch et al, 2009; Gourévitch and Edeline, 2011). Briefly, ABR were recorded via subcutaneous electrodes (SC25, Neuro-Services); using a Centor-USB interface and software (DeltaMed, France).…”

“…At the thalamocortical level, electrophysiological studies have documented that exposure to loud, traumatic sounds generating partial hearing loss produced alterations in frequency tuning (Rajan, 1998, 2001; Kimura and Eggermont, 1999; Noreña and Eggermont, 2003; Scholl and Wehr, 2008; Gourévitch and Edeline, 2011) and tonotopic map reorganizations (Noreña and Eggermont, 2005). These changes in functional properties may result both from physiological modifications already occurring at subcortical levels (Wang et al, 1996, 2002; Kamke et al, 2003; Vale et al, 2003) and/or from morphological alterations of cortical cells such as modifications in dendritic morphology and in dendritic spine numbers (Fetoni et al, 2013).…”

“…In all but three cases (Sun et al, 2008; Noreña et al, 2010; Rosen et al, 2012), the electrophysiological experiments performed so far after hearing loss have assessed the functional properties of auditory cortex neurons under general anesthesia a few hours (Kimura and Eggermont, 1999; Noreña and Eggermont, 2003) to a few days (Rajan, 1998, 2001) or months (Robertson and Irvine, 1989; Gourévitch and Edeline, 2011) after hearing loss. The apparent discrepancy between all these results might be simply due to the use of different delays between the beginning of hearing loss and the time at which the recordings are collected.…”

The miR-34a/Bcl-2 Pathway Contributes to Auditory Cortex Neuron Apoptosis in Age-Related Hearing Loss

“…Most previous research has focused on the peripheral system, such as the presbycusis and spiral ganglion [Puel et al, 2002;Zou et al, 2008;Menardo et al, 2012;Chen et al, 2013;Xiong et al, 2014]. However, central nervous system changes can also be involved in AHL, which could [Kapsimali et al, 2007] explain the poor speech recognition in clinical observations [Gourevitch and Edeline, 2011;Eckert et al, 2012]. However, the detailed mechanisms in the central auditory cortex underlying AHL remain largely unknown.…”