Auditory Cortical Changes Precede Brainstem Changes During Rapid Implicit Learning: Evidence From Human EEG

Abstract

The auditory system is sensitive to stimulus regularities such as frequently occurring sounds and sound combinations. Evidence of regularity detection can be seen in how neurons across the auditory network, from brainstem to cortex, respond to the statistical properties of the soundscape, and in the rapid learning of recurring patterns in their environment by children and adults. Although rapid auditory learning is presumed to involve functional changes to the auditory network, the chronology and directionality of changes are not well understood. To study the mechanisms by which this learning occurs, auditory brainstem and cortical activity was simultaneously recorded via electroencephalogram (EEG) while young adults listened to novel sound streams containing recurring patterns. Neurophysiological responses were compared between easier and harder learning conditions. Collectively, the behavioral and neurophysiological findings suggest that cortical and subcortical structures each provide distinct contributions to auditory pattern learning, but that cortical sensitivity to stimulus patterns likely precedes subcortical sensitivity.

What we do (not) know about the mechanisms underlying adaptive speech perception: A computational framework and review

“…Neuroimaging research has, on the whole, been more invested into contrastive comparisons (e.g., Bonte et al, 2017;Erb et al, 2013b;Guediche et al, 2015;Myers & Mesite, 2014): questions about the involvement of different types of information processing-operationalized as differential activation of different brain areas and networks that are associated with different functionality-are the bread and butter of neuroimaging. This approach has identified a wide range of brain regions as involved in different aspects of adaptive speech perception, ranging from subcortical areas (e.g., Guediche et al, 2015;Skoe et al, 2021) to networks associated with decision-making (e.g., Erb et al, 2013b;Myers & Mesite, 2014). This leaves open, however, what types of computations underlie the observed differential activations, or why different types of exposure lead to different types of behavioral changes.…”

“…In contrast to the assumption that cross-talker variability may be learned and stored, which is fundamental to all the theories of representational changes as described above, normalization proposals assume that listeners remove talker variability prior to mapping cues to linguistic categories. More recently, evidence from neuroimaging studies has lent support for low-level normalization mechanisms by showing engagement of subcortical structures in sensory adaptation (e.g., the brain stem, Skoe et al, 2021;and cerebellum, Guediche et al, 2015; for review, see Guediche et al, 2014). Studies using intracranial electrocorticography have found evidence of talker-normalized (spectral) cues in the auditory cortex before they are mapped onto categories (e.g., Sjerps et al, 2019;Tang et al, 2017a).…”

Short- and long-term experience-dependent neuroplasticity interact during the perceptual learning of concurrent speech

“…This notion aligns with recent studies suggesting cortical changes precede those in brainstem (Reetzke et al . 2018; Skoe et al 2021) by several days/weeks, as well as theoretical accounts that learning proceeds in a top-down guided manner (Ahissar and Hochstein 2004), with sensory change in the brainstem only emerging at expert stages of learning (Reetzke et al . 2018).…”

“…It is also possible that auditory plasticity is stronger and emerges earlier at cortical relative to brainstem levels (e.g., Reetzke et al . 2018; Skoe et al . 2021; Bidelman et al .…”

Descending Control in the Auditory System: A Perspective

“…In ferrets, changes in non-primary auditory cortex neurons precede changes in primary auditory cortex (Elgueda et al, 2019 ). In humans, non-primary AC has a larger influence than primary AC on speech perception (Hamilton et al, 2021 ), and cortical changes precede midbrain changes as demonstrated by Skoe et al's contribution to this issue (Skoe et al, 2021 ).…”