Auditory temporal acuity improves with age in the male mouse auditory thalamus: A role for perineuronal nets?

Abstract

The ability to perceive and interpret environmental sound accurately is conserved across many species and is fundamental for understanding communication via vocalizations. Auditory acuity and temporally controlled neuronal firing underpin this ability. Deterioration in neuronal firing precision likely contributes to poorer hearing performance, yet the role of neural processing by key nuclei in the central auditory pathways is not fully understood. Here, we record from the auditory thalamus (medial geniculate body [MGB]) of young and middle‐aged, normally hearing male CBA/Ca mice. We report changes in temporal processing of auditory stimuli, with neurons recorded from ventral and medial MGB subdivisions of older animals more likely to synchronize to rapid temporally varying stimuli. MGB subdivisions also showed increased probability of neuronal firing and shorter response latencies to clicks in older animals. Histological investigation of neuronal extracellular specializations, perineuronal nets (PNNs) and axonal coats, in the MGB identified greater organization of PNNs around MGB neurons and the presence of axonal coats within older animals. This supports the observation that neural responses recorded from ventral and medial MGB of older mice were more likely to synchronize to temporally varying stimuli presented at faster repetition rates than those recorded from young adult animals. These changes are observed in animals with normal hearing thresholds, confirming that neural processing differs between the MGB subdivisions and such processing is associated with age‐related changes to PNNs. Understanding these age‐related changes and how they occur have important implications for the design of effective therapeutic interventions to improve speech intelligibility into later life.

The Density of Perineuronal Nets Increases With Age in the Inferior Colliculus in the Fischer Brown Norway Rat

“…As the current study is the first investigation of PNs in the aging IC it is difficult to draw direct comparisons of our results to the past studies listed above. However, our data reflects similar age-related increases of PNs found in the auditory thalamus, somatosensory, visual and prefrontal cortices and the dentate gyrus (Tanaka and Mizoguchi, 2009;Yamada and Jinno, 2013;Karetko-Sysa et al, 2014;Ueno et al, 2018;Quraishe et al, 2019). Additionally, Fader et al (2016) found that the density of PNs in the IC began to increase between 3 (mature adult) and 9 (middle-age) month old mice.…”

“…PNs can regulate and promote functional synaptic plasticity (Bukalo et al, 2001;Balmer et al, 2009;de Vivo et al, 2013;Blosa et al, 2015;Bosiacki et al, 2019). Interestingly, a recent study has shown that PN expression in the medial subdivisions of the auditory thalamus may be responsible for precise neural firing in the aging brain (Quraishe et al, 2019). In the IC, both GABAergic and glutamatergic IC cells (1) receive GABAergic input from numerous subcortical sources and (2) change the subunit composition of their postsynaptic GABA A receptors in a non-linear fashion early and throughout life (Milbrandt et al, 1996(Milbrandt et al, , 1997Caspary et al, 1999;Kelly and Caspary, 2005;Robinson et al, 2019).…”

Macrophages in the cochlea; an immunological link between risk factors and progressive hearing loss

“…Using a frequency‐specific noise to create an injury in the cochlea, it is possible to reliably map the injury site, due to tonotopy of the cochlea. While with noise injury there is a small frequency shift, this shift is reproducible (Quraishe et al, 2019). The resulting tissue damage and the local cellular response from the insult, in and around the area of damage, can be investigated.…”

“…The level of noise exposure, both intensity and duration, is variable; whereby a significant exposure such as 4 h at 118 dB for four consecutive days, designed to induce long‐lasting auditory damage and result in a permanent threshold shift (Fuentes‐Santamaria et al, 2017), is likely to elicit a very different inflammatory response compared to lower level noise exposure that only produces temporary threshold shifts (Frye et al, 2018). Although this may be further altered by the age, at which the subject is exposed to the noise or insult (Quraishe et al, 2019). Higher intensity exposures may provide insight into the damage caused by repeat exposure to a significant event, for example, a blast, whereas the lower level noise is more representative of daily noise exposure associated with certain industries.…”

Lemniscal Corticothalamic Feedback in Auditory Scene Analysis

“…Along with musical training, corticothalamic feedback modulation may generally reinforce experience-dependent sound processing. Although speech processing ability degrades with aging, which is associated with impaired temporal coding and altered inhibitory signaling in the auditory system (Caspary et al, 2008;Gordon-Salant et al, 2011;Richardson et al, 2013;Presacco et al, 2016), temporal precision is actually improved in the MGB of aged-animals, which could indicate a compensation for the degraded hearing abilities via top-down modulation (Kommajosyula et al, 2019(Kommajosyula et al, , 2021Quraishe et al, 2020). Agedmusicians showed less degraded performance on the tasks that typically decline with aging (e.g., signal-in-noise, gap or mistuning detection) (Parbery-Clark et al, 2009;Zendel and Alain, 2012), which may reflect compensation via enhanced corticothalamic feedback.…”