Elsevier

Hearing Research

Volume 308, February 2014, Pages 109-121
Hearing Research

Review
Biological impact of auditory expertise across the life span: Musicians as a model of auditory learning

https://doi.org/10.1016/j.heares.2013.08.004Get rights and content

Highlights

  • Musicians provide a model of experience-dependency in human auditory processing.

  • We review neural markers of musicianship across the life span together with cellular learning mechanisms identified in animal models.

  • Interactive auditory enrichment may prime musicians for auditory learning.

Abstract

Experience-dependent characteristics of auditory function, especially with regard to speech-evoked auditory neurophysiology, have garnered increasing attention in recent years. This interest stems from both pragmatic and theoretical concerns as it bears implications for the prevention and remediation of language-based learning impairment in addition to providing insight into mechanisms engendering experience-dependent changes in human sensory function. Musicians provide an attractive model for studying the experience-dependency of auditory processing in humans due to their distinctive neural enhancements compared to nonmusicians. We have only recently begun to address whether these enhancements are observable early in life, during the initial years of music training when the auditory system is under rapid development, as well as later in life, after the onset of the aging process. Here we review neural enhancements in musically trained individuals across the life span in the context of cellular mechanisms that underlie learning, identified in animal models. Musicians' subcortical physiologic enhancements are interpreted according to a cognitive framework for auditory learning, providing a model in which to study mechanisms of experience-dependent changes in human auditory function.

This article is part of a Special Issue entitled <Music: A window into the hearing brain>.

Introduction

Learning is a fundamental human capacity; not only does it underlie the gradual development of basic skills from infancy (e.g., language) but it also accounts for our attraction to new experiences, the resources we invest in educational opportunities and the effort we put into maintaining a dynamic nervous system in hopes of keeping aging's cognitive detriments at bay. In light of our continuous reliance on learning, it is surprising how much of its neurobiological underpinnings—especially within the auditory system—still eludes us. We have made considerable headway toward defining neuronal correlates of learning in addition to identifying the characteristics that contribute to an organism's readiness to learn. The bulk of this work has been cellular in nature, carried out in animal models; we have only recently begun to apply principles derived from this research to outcomes of learning in humans (e.g., Zatorre et al., 2012). The study of musicians' auditory processing provides a window into auditory learning, not only shedding light on neural mechanisms underlying learning in humans but further contributing to a definition of what makes a good learner.

Investigations into human learning through the study of musicians profit from an almost infinite variety of auditory experts. Musicians' auditory learning approaches vary not only according to instrument, style and level of expertise but also according to their reliance on memory, improvisation, aural learning/mimicry and engagement of the visual modality. Furthermore, music is an inherently rewarding auditory activity, in part due to its activation of the brain's mesolimbic reward network (Koelsch et al., 2006, Menon and Levitin, 2005, Salimpoor et al., 2011, Salimpoor et al., 2013). This may account for why humans view music as one of the top ten most pleasurable things, sometimes even ranking music above the notable rewards of money and food (Dube and Lebel, 2003). This property of music confers emotional benefits that promote its practice and performance and, by co-activating mesolimbic neuromodulatory control centers, promotes long-term learning success (for review see Puschmann et al., 2012).

Here we interpret principles derived from cellular studies of learning in the context of how auditory experience in the form of music training shapes the structure and function of the human brain. By considering cellular approaches for studying learning alongside the biological evidence of lifelong, interactive auditory enrichment in musicians, we can infer the processes by which the human brain is shaped by the development of expertise and test their boundaries. The parallel consideration of cellular and far-field approaches may encourage further investigations into the capacity of interactive, acoustically rich and cognitively engaging auditory activities, such as that provided through music training, to shape basic auditory mechanisms. We begin by reviewing progress toward identifying neuronal substrates of learning in animal models and the potential for musicians to provide further conceptual advances as a model of auditory learning in humans.

Section snippets

Biological mechanisms of auditory learning

Neurobiological approaches have uncovered a variety of neuronal substrates of learning, the activity of which is modified by development, experience, gene expression and the neuromodulatory system, among others. We herein discuss major themes in this line of research and their application to musicians, comprising neurogenesis, synaptic plasticity, gene expression and factors guiding metaplasticity (i.e., the potential for plastic changes to take place).

Auditory learning in musicians: what can music teach us?

Despite our progress toward identifying neuronal mechanisms that underscore experience-related plasticity and subsequent learning potential, the complexity of interactions among these mechanisms and their different relationships to development and environmental factors make it difficult to determine how they work in concert to shape system-wide behavior. Furthermore, the bulk of this work has taken place in animal models, challenging its generalization to everyday learning in humans. Here we

Moving forward: what do musicians still have to teach us about auditory learning?

The insights provided by basic science give us a strong starting point from which to consider restructuring auditory training approaches and learning strategies, especially with regard to sensitive developmental periods during which they can be most effective (e.g., see Sanes and Woolley, 2011). But how do principles taken from cellular approaches translate into recommendations for human habits that raise one's learning potential? Considering musicians as a model of auditory learning may yield

Conclusions

Here we have interpreted principles derived from cellular studies alongside evidence for the impact of auditory expertise on human brain structure and function. While the most effective approach would comprise a thorough integration of knowledge gained from cellular work with outcomes from far-field metrics in humans, present knowledge cannot bridge these approaches. Many reports have revealed effects of learning on subcortical physiology using cellular measurements in animal models but to our

Acknowledgments

This research was funded by the National Institutes of Health grant F31DC011457-01 to D.S., the National Science Foundation grants BCS-0921275, 1057556and 0842376 to N.K., the Grammy Foundation and the Knowles Hearing Center. The authors thank Samantha O'Connell for her contributions to data collection in preschoolers and Alexandra Parbery-Clark, Karen Chan, Trent Nicol and Jennifer Krizman for their comments on the manuscript.

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    Present address: Neural Systems Laboratory, Institute for Systems Research, University of Maryland, College Park, MD, USA.

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