Age-related changes in sound onset and offset intensity coding in auditory cortical fields A1 and CL of rhesus macaques

Abstract

Inhibition plays a key role in shaping sensory processing in the central auditory system and has been implicated in sculpting receptive field properties such as sound intensity coding and also in shaping temporal patterns of neuronal firing such as onset- or offset-evoked responses. There is substantial evidence supporting a decrease in inhibition throughout the ascending auditory pathway in geriatric animals. We therefore examined intensity coding of onset (ON) and offset (OFF) responses in auditory cortex of aged and young monkeys. A large proportion of cells in the primary auditory cortex (A1) and the caudolateral field (CL) displayed nonmonotonic rate-level functions for OFF responses in addition to nonmonotonic coding of ON responses. Aging differentially affected ON and OFF responses; the magnitude of effects was generally greater for ON responses. In addition to higher firing rates, neurons in old monkeys exhibited a significant increase in the proportion of monotonic rate-level functions and had higher best intensities than those in young monkeys. OFF responses in young monkeys displayed a range of intensity coding relationships with ON responses of the same cells, ranging from highly similar to highly dissimilar. Dissimilarity in ON/OFF coding was greater in CL and was reduced with aging, which was largely explained by a preferential decrease in the percentage of cells with nonmonotonic coding of ON and OFF responses. The changes we observed are consistent with previously demonstrated alterations in inhibition in the ascending auditory pathway of primates and could be involved in age-related deficits in the temporal processing of sounds. NEW & NOTEWORTHY Aging has a major impact on intensity coding of neurons in auditory cortex of rhesus macaques. Neural responses to sound onset and offset were affected to different extents, and their rate-level functions became more mutually similar, which could be accounted for by the loss of nonmonotonic intensity coding in geriatric monkeys. These findings were consistent with weakened inhibition in the central auditory system and could contribute to auditory processing deficits in elderly subjects.

Effects of Ketamine Administration on Auditory Information Processing in the Neocortex of Nonhuman Primates

“…Friedman, Sehatpour ( 51 ) reported that the deficits in duration MMN processing may be specifically related to impaired premorbid function, whereas deficits in MMN to frequency deviants may continue to worsen even during early disease stages ( 52 , 53 ). Furthermore, a similar imbalance in the onset and offset responses in K10 has been reported in an electrophysiological study on the primary auditory area of aged monkeys ( 54 ). This study also showed that the increase in firing rates of auditory cortex neurons in aged monkeys was significantly higher than that in young monkeys, a result consistent with those of previous studies ( 55 – 57 ).…”

Changes in Cortical Directional Connectivity during Difficult Listening in Younger and Older Adults

“…Additionally, connectivity significantly decreased in older adults for facilitative connections only in the 0 dB SNR conditions, not at all for the sharpening connections, and for suppressive connections in both the speech in quiet and 0 dB SNR conditions. The general decrease in suppressive connectivity is consistent with the aging-related decrease in GABA-based inhibition seen in many auditory studies, both animal (Willott et al, 1991;Caspary et al, 1995;Hughes et al, 2010;Caspary et al, 2013;Richardson et al, 2013;Parthasarathy et al, 2019;Ramamurthy & Recanzone, 2020) and human (Lalwani et al, 2019;Ross et al, 2020;Dobri & Ross, 2021;Harris et al, 2022). More interesting, perhaps, is the dynamic tradeoff between facilitative and sharpening connectivity seen in older adults when shifting from listening to speech in quiet (maximal facilitative and minimal sharpening) to speech in noise (reduced facilitative but increased sharpening).…”

Effects of Aging on Cortical Representations of Continuous Speech

“…Gamma-aminobutyric acid (GABA)-mediated inhibition plays a major role in maintaining synchrony and spectral sensitivity in auditory circuits. Both animal (Hughes et al 2010; Caspary et al 2013; Richardson et al 2013; Parthasarathy et al 2019; Ramamurthy and Recanzone 2020) and human (Lalwani et al 2019; Dobri and Ross 2021) studies have reported a reduction in age-related inhibitory circuits and function. This mechanism could apply to any of the three main processing stages and for both attended and unattended talkers.…”