Abstract
Experience has a profound influence on how sound is processed in the brain. Yet little is known about how enriched experiences interact with developmental processes to shape neural processing of sound. We examine this question as part of a large cross-sectional study of auditory brainstem development involving more than 700 participants, 213 of whom were classified as musicians. We hypothesized that experience-dependent processes piggyback on developmental processes, resulting in a waxing-and-waning effect of experience that tracks with the undulating developmental baseline. This hypothesis led to the prediction that experience-dependent plasticity would be amplified during periods when developmental changes are underway (i.e., early and later in life) and that the peak in experience-dependent plasticity would coincide with the developmental apex for each subcomponent of the auditory brainstem response (ABR). Consistent with our predictions, we reveal that musicians have heightened response features at distinctive times in the life span that coincide with periods of developmental change. The effect of musicianship is also quite specific: we find that only select components of auditory brainstem activity are affected, with musicians having heightened function for onset latency, high-frequency phase-locking, and response consistency, and with little effect observed for other measures, including lower-frequency phase-locking and non-stimulus-related activity. By showing that musicianship imparts a neural signature that is especially evident during childhood and old age, our findings reinforce the idea that the nervous system's response to sound is “chiseled” by how a person interacts with his specific auditory environment, with the effect of the environment wielding its greatest influence during certain privileged windows of development.
Highlights
The auditory brain has an awesome capacity to change through experience
Are there limits to this plasticity throughout development? Are there biological guard rails that place limits on experience-dependent plasticity at some points in life or biological stimulants that promote plasticity at others? In this study, we examine these questions, focusing on the auditory brainstem and what it can reveal about sensitive periods in the auditory brain and its ability to respond to sound
The lack of musicianship effects for the click-evoked auditory brainstem response (ABR) reinforces that the effects of musicianship on peak V of the cABR are not driven by subclinical differences in peripheral audiometric function
Summary
The auditory brain has an awesome capacity to change through experience. But are there limits to this plasticity throughout development? Are there biological guard rails that place limits on experience-dependent plasticity at some points in life or biological stimulants that promote plasticity at others? In this study, we examine these questions, focusing on the auditory brainstem and what it can reveal about sensitive periods in the auditory brain and its ability to respond to sound.Except in cases of brain death, the auditory brainstem is always “on” and metabolically active (Sokoloff, 1977; Chandrasekaran and Kraus, 2010). The auditory brainstem response (ABR) is robust even under general anesthesia, during sleep, and while the participant’s attention is directed elsewhere (Smith and Mills, 1989; Skoe and Kraus, 2010; Hairston et al, 2013). Through the analysis of large datasets and more complex stimulus conditions, a different picture has emerged (Galbraith, 2008) With this approach, we have learned that the auditory brainstem captures the physics of the sound (timing, fundamental frequency, harmonics, etc.) as well as the meaning (i.e., behavioral significance) attributed to that sound. Across the lifespan, we observe differences in auditory brainstem function depending on the instrument a person plays or the language or languages a person speaks (Krishnan et al, 2010; Krizman et al, 2012a; Strait et al, 2012a), suggesting that the auditory brainstem’s fundamental ability to capture sound is chiseled by idiosyncratic experiences with sound
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