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Defining the Role of Attention in Hierarchical Auditory Processing

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Defining the Role of Attention in Hierarchical Auditory Processing Review Defining the Role of Attention in Hierarchical Auditory Processing Caitlin N. Price 1,2,* and Deborah Moncrieff 1,2 1 Institute for Intelligent Systems, University of Memphis, Memphis, TN 38152, USA; [email protected] 2 School of Communication Sciences & Disorders, University of Memphis, Memphis, TN 38152, USA * Correspondence: [email protected] Abstract: Communication in noise is a complex process requiring efficient neural encoding through- out the entire auditory pathway as well as contributions from higher-order cognitive processes (i.e., attention) to extract speech cues for perception. Thus, identifying effective clinical interventions for individuals with speech-in-noise deficits relies on the disentanglement of bottom-up (sensory) and top-down (cognitive) factors to appropriately determine the area of deficit; yet, how attention may interact with early encoding of sensory inputs remains unclear. For decades, attentional the- orists have attempted to address this question with cleverly designed behavioral studies, but the neural processes and interactions underlying attention’s role in speech perception remain unresolved. While anatomical and electrophysiological studies have investigated the neurological structures contributing to attentional processes and revealed relevant brain–behavior relationships, recent elec- trophysiological techniques (i.e., simultaneous recording of brainstem and cortical responses) may provide novel insight regarding the relationship between early sensory processing and top-down at- tentional influences. In this article, we review relevant theories that guide our present understanding of attentional processes, discuss current electrophysiological evidence of attentional involvement in auditory processing across subcortical and cortical levels, and propose areas for future study that will inform the development of more targeted and effective clinical interventions for individuals with speech-in-noise deficits. Citation: Price, C.N.; Moncrieff, D. Keywords: speech perception in noise; central auditory deficits; theories of attention; electrophysiology Defining the Role of Attention in Hierarchical Auditory Processing. Audiol. Res. 2021, 11, 112–128. https://doi.org/10.3390/audiolres 1. Introduction 11010012 Attentional selection of relevant inputs is a phenomenon that has been extensively studied in the auditory, somatosensory, and visual sensory modalities. In the auditory Received: 5 February 2021 Accepted: 10 March 2021 domain, attentional selection applies in everyday communicative interactions as the listener Published: 13 March 2021 must attend to signals of interest while ignoring, or suppressing, competing signals present in the soundscape. Difficulties extracting important speech information from background Publisher’s Note: MDPI stays neutral noise have been linked to a variety of communication disorders in individuals of all ages with regard to jurisdictional claims in for several decades. In children, these difficulties may impair a child’s ability to access published maps and institutional affil- the phonological structure of language [1,2] and contribute to developmental learning iations. and reading difficulties [3]. In adults with [4,5] and without hearing impairment [6,7], difficulties hearing and communicating in noise may underlie greater social isolation [8], depression [9], poorer quality of life [10], and accelerated cognitive decline [11,12]. Both bottom-up perceptual and top-down cognitive processes contribute to a listener’s ability to extract a salient auditory signal from a competing stream of background informa- Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. tion. Uni- and bi-directional components of the auditory brain that contribute to adequate This article is an open access article processing of speech in background noise mature at different rates across development distributed under the terms and and are subject to a variety of acquired factors across adulthood and aging. Moore [13] conditions of the Creative Commons noted that the ascending pathway matures early in most children with normal hearing but Attribution (CC BY) license (https:// some children develop auditory perceptual skills as late as 10–12 years of age due to slower creativecommons.org/licenses/by/ maturation of top-down mechanisms [13,14]. 4.0/). Audiol. Res. 2021, 11, 112–128. https://doi.org/10.3390/audiolres11010012 https://www.mdpi.com/journal/audiolres Audiol. Res. 2021, 11, FOR PEER REVIEW 2 Audiol. Res. 2021, 11 Moore [13] noted that the ascending pathway matures early in most children with normal113 hearing but some children develop auditory perceptual skills as late as 10–12 years of age due to slower maturation of top-down mechanisms [13,14]. BothBoth MooreMoore [[15]15] andand HumesHumes [[16]16] attributeattribute difficultiesdifficulties inin auditoryauditory perception,perception, partic-partic- ularlyularly inin complexcomplex listening situations, to to underlying underlying pathologies pathologies within within various various levels levels of ofthe the auditory auditory system system (depicted (depicted in Figure in Figure 1). Humes1). Humes [16] describes [ 16] describes these as these the peripheral, as the pe- ripheral,central-auditory, central-auditory, and cognitive and cognitive hypotheses. hypotheses. The peripheral The peripheral hypothesis hypothesis suggests suggests that thatchanges changes in the in peripheral the peripheral auditory auditory system system result resultin poorer in poorerperipheral peripheral encoding encoding of acoustic of acousticsignals degrading signals degrading the quality the of quality speech of inputs speech to inputs higher to processing higher processing centers. centers. The central- The central-auditoryauditory hypothesis hypothesis posits positsthat structural that structural or functional or functional changes changes within within the auditory the auditory path- pathwayway from from the brainstem the brainstem to auditory to auditory cortex cortex result result in altered in altered neural neural transmission transmission and and fea- featureture extraction extraction vital vital for for the the optimization optimization of cu ofes cues (i.e., (i.e., temporal, temporal, spectral, spectral, spatial) spatial) to im- to improveprove speech speech understanding understanding in incomplex complex listening listening environments. environments. Lastly, Lastly, the the cognitive cognitive hy- hypothesispothesis implies implies that that a ageneral general cognitive cognitive defi deficitcit influences influences the efficiencyefficiency ofof informationinformation processing,processing, labeling,labeling, andand storagestorage withinwithin memorymemory [[16].16]. AA breakdownbreakdown inin processingprocessingat at any any levellevel ofof thethe systemsystem couldcould lead lead to to errors errors in in perceptual perceptual understanding. understanding. Auditory Brainstem Sound Cortex Periphery Pathways Peripheral Neural Transmission & Information Processing, Encoding Feature Extraction Labeling, & Storage Attention Figure 1. Attention is thought to influence the initial encoding and subsequent processing of auditory inputsFigure across 1. Attention all levels is thought of the auditory to influence system. the Adapted initial encoding from Humes, and subsequent 1996 with permission processing fromof audi- the Americantory inputs Academy across all of levels Audiology. of the auditory system. Adapted from Humes, 1996 with permission from the American Academy of Audiology. As speech-in-noise (SIN) deficits are present even in normal hearing listeners [6,7], theseAs difficulties speech-in-noise cannot be (SIN) attributed deficits to are audibility presen withint even in the normal peripheral hearing system listeners alone. [6,7], The underlyingthese difficulties issue cannot likely involvesbe attributed a central-auditory to audibility within or cognitive the peripheral deficit orsystem an interaction alone. The betweenunderlying the issue two. Whenlikely involves the efficiency a central-auditory and synchrony or ofcognitive bottom-up, deficit perceptual or an interaction process- ingbetween of auditory the two. stimuli When isthe disrupted, efficiency listeningand synchrony and learning of bottom-up, difficulties perceptual are exacerbated processing dueof auditory to an impaired stimuli abilityis disrupted, to extract listening necessary and learning acoustic difficulties features for are comprehension. exacerbated due For to instance,an impaired school-aged ability to extract children necessary with listening acoustic and features learning for difficultiescomprehension. demonstrate For instance, less preciseschool-aged and robust children early with sensory listening encoding and learning of speech difficulties signals demonstrate at the level ofless the precise auditory and brainstemrobust early [17 sensory–20] as wellencoding as weaker of speech cortical signal processings at the [level17] despite of the auditory normal peripheral brainstem hear- [17– ing20] sensitivity.as well as weaker Likewise, cortical young processing adults with [17] normal despite hearing normal who peripheral perform hearing poorly sensitiv- on SIN tasksity. Likewise, demonstrate young less robustadults brainstemwith normal [21,22 hearing] and cortical who perform responses poorly in noise on [22 SIN,23], tasks and olderdemonstrate adults who less arerobust poor brainstem SIN performers [21,22] and demonstrate cortical responses weaker
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