Aging Affects Adaptation to Sound-Level Statistics in Human Auditory Cortex

Abstract

Optimal perception requires efficient and adaptive neural processing of sensory input. Neurons in nonhuman mammals adapt to the statistical properties of acoustic feature distributions such that they become sensitive to sounds that are most likely to occur in the environment. However, whether human auditory responses adapt to stimulus statistical distributions and how aging affects adaptation to stimulus statistics is unknown. We used MEG to study how exposure to different distributions of sound levels affects adaptation in auditory cortex of younger (mean: 25 years; = 19) and older (mean: 64 years; = 20) adults (male and female). Participants passively listened to two sound-level distributions with different modes (either 15 or 45 dB sensation level). In a control block with long interstimulus intervals, allowing neural populations to recover from adaptation, neural response magnitudes were similar between younger and older adults. Critically, both age groups demonstrated adaptation to sound-level stimulus statistics, but adaptation was altered for older compared with younger people: in the older group, neural responses continued to be sensitive to sound level under conditions in which responses were fully adapted in the younger group. The lack of full adaptation to the statistics of the sensory environment may be a physiological mechanism underlying the known difficulty that older adults have with filtering out irrelevant sensory information. Behavior requires efficient processing of acoustic stimulation. Animal work suggests that neurons accomplish efficient processing by adjusting their response sensitivity depending on statistical properties of the acoustic environment. Little is known about the extent to which this adaptation to stimulus statistics generalizes to humans, particularly to older humans. We used MEG to investigate how aging influences adaptation to sound-level statistics. Listeners were presented with sounds drawn from sound-level distributions with different modes (15 vs 45 dB). Auditory cortex neurons adapted to sound-level statistics in younger and older adults, but adaptation was incomplete in older people. The data suggest that the aging auditory system does not fully capitalize on the statistics available in sound environments to tune the perceptual system dynamically.

Neural Responses and Perceptual Sensitivity to Sound Depend on Sound-Level Statistics

“…Discrimination performance was sensitive to the context's modal level. However, inconsistent with statistical adaptation measured neurophysiologically ( Figure 1) 10,11,17,18,21 , sound-level discrimination was better for low-intensity compared to higher-intensity target sounds in the high-modal context 24 . Neurophysiological work, in contrast, suggests that neurons are not very sensitive to low-intensity sounds when the ambient sound level is high ( Figure 1A).…”

“…The main analyses focused on neural and behavioral responses to noise bursts (targets) for which the sound level, and the sound level of the directly preceding noise, were identical across the two statistical contexts (black dots in Figure 2, middle/right). This allowed us to investigate the effects of longer-term sound-level statistics on neural responses and perception 21 .…”

“…Achieving a wide perceptual range with a limited neuronal range is thought to be accomplished by a dynamic adjustment of the response range (input-output function) of neurons to sound-level statistics in the environment ( Figure 1A) 10,11 . This process -called adaptation to stimulus statistics, dynamic range adaptation, or gain control 1,[12][13][14][15][16] -involves shifting the response range of neurons depending on the mean or modal sound level in an acoustic environment 10,11,[17][18][19][20][21][22] . When ambient sound levels are low, neurons are more sensitive and more responsive, but saturate for moderate-to highlevel sounds, compared to when ambient sound levels are moderate to high (red and teal lines in Figure 1A, respectively).…”

“…Figure 1: Schematic depiction of neural adaptation to sound-level statistics. Adopted from empirical data 10,11,21 . A: Predicted neural responses as a function of sound level for two sound-level contexts with different modal sound levels (low vs. high; inset).…”

“…Most research on adaptation of neural activity to sound-level statistics has been conducted using neurophysiological techniques in non-human mammals 10,11,13,[17][18][19][20]23 . We have recently demonstrated using magnetoencephalography that neural activity in human auditory cortex adapts to sound-level statistics (i.e., to the modal sound-level) 21 . However, whether such adaptive changes confer benefit to perceptual sensitivity is less clear.…”