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A neurodevelopmental disorders perspective into music, social attention, and social bonding

Published online by Cambridge University Press:  30 September 2021

Anna Kasdan
Affiliation:
Vanderbilt Brain Institute, Vanderbilt University, Nashville, TN37232, USA. anna.v.kasdan@vanderbilt.edu; reyna.gordon@vanderbilt.edu; miriam.lense@vanderbilt.eduannakasdan.com
Reyna L. Gordon
Affiliation:
Vanderbilt Brain Institute, Vanderbilt University, Nashville, TN37232, USA. anna.v.kasdan@vanderbilt.edu; reyna.gordon@vanderbilt.edu; miriam.lense@vanderbilt.eduannakasdan.com Department of Otolaryngology – Head and Neck Surgery, Vanderbilt University Medical Center, Nashville, TN37232, USA. https://www.vumc.org/music-cognition-lab/person/faculty
Miriam D. Lense
Affiliation:
Vanderbilt Brain Institute, Vanderbilt University, Nashville, TN37232, USA. anna.v.kasdan@vanderbilt.edu; reyna.gordon@vanderbilt.edu; miriam.lense@vanderbilt.eduannakasdan.com Department of Otolaryngology – Head and Neck Surgery, Vanderbilt University Medical Center, Nashville, TN37232, USA. https://www.vumc.org/music-cognition-lab/person/faculty

Abstract

Our commentary addresses how two neurodevelopmental disorders, Williams syndrome and autism spectrum disorder, provide novel insights into the credible signaling and music and social bonding hypotheses presented in the two target articles. We suggest that these neurodevelopmental disorders, characterized by atypical social communication, allow us to test hypotheses about music, social bonding, and their underlying neurobiology.

Type
Open Peer Commentary
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Neurodevelopmental disorders characterized by atypical social profiles provide a unique window into the relationship between sociability, music, and the evolutionary origins of music. Here, we focus on two neurodevelopmental disorders characterized by atypical development of social communication – Williams syndrome and autism spectrum disorder (ASD). We (1) provide additional consideration about music as a credible signal for parent–infant interactions (Mehr, Krasnow, Bryant, & Hagen, target article) and (2) extend neurobiological predictions about music and social bonding (MSB; Savage et al., target article).

Individuals with Williams syndrome, a genetic neurodevelopmental disorder caused by the deletion of ~28 genes on chromosome 7, exhibit marked hypersociability accompanied by difficulties in social pragmatics (Barak & Feng, Reference Barak and Feng2016). Individuals with ASD, an etiological heterogenous set of neurodevelopmental disorders, exhibit deficits in social communication and interactions (Barak & Feng, Reference Barak and Feng2016). Music is a relative strength and interest in both Williams syndrome and ASD. Individuals with Williams syndrome exhibit increased emotional responsiveness to music and increased neural responses to musical stimuli compared to typical peers (Kasdan, Gordon, & Lense, Reference Kasdan, Gordon and Lense2020; Lense, Gordon, Key, & Dykens, Reference Lense, Gordon, Key and Dykens2014), although behavioral studies of musical skills show mixed findings and substantial individual differences (Hopyan, Dennis, Weksberg, & Cytrynbaum, Reference Hopyan, Dennis, Weksberg and Cytrynbaum2001; Martens, Reutens, & Wilson, Reference Martens, Reutens and Wilson2010). Individuals with ASD generally exhibit age-appropriate melody and rhythm skills (Jamey et al., Reference Jamey, Foster, Sharda, Tuerk, Nadig and Hyde2019; Tryfon et al., Reference Tryfon, Foster, Ouimet, Doyle-Thomas, Anagnostou, Sharda and Hyde2017) and better pitch interval detection compared to controls (Heaton, Reference Heaton2005). Additionally, individuals with ASD show preserved emotional processing of music at both behavioral and neural levels, despite overall impairments in emotion recognition (Caria, Venuti, & De Falco, Reference Caria, Venuti and De Falco2011; Molnar-Szakacs & Heaton, Reference Molnar-Szakacs and Heaton2012).

As in typical development, music is used in these populations to leverage social attention and bonding, including during parent–child interactions (Steinberg, Shivers, Liu, Cirelli, & Lense, Reference Steinberg, Shivers, Liu, Cirelli and Lense2020). Because of impaired social communication of children with ASD and Williams syndrome, parents adapt and increase their social signaling in order to capture and modulate their children's attention and emotions; this frequently involves adapting the “musicality” of the social signal such as through increased rhythmic predictability and pitch contours (e.g., increased use of infant-directed speech; Cohen et al., Reference Cohen, Cassel, Saint-Georges, Mahdhaoui, Laznik, Apicella and Chetouani2013; Quigley, McNally, & Lawson, Reference Quigley, McNally and Lawson2016). Music and song activities provide an ecologically valid means for scaffolding parental signaling during these shared social interactions (Lense & Camarata, Reference Lense and Camarata2020). This is consistent with and extends the idea of music as a credible signal for parent–infant interactions (Mehr et al.). The core features of music (e.g., discrete pitches and predictable and hierarchical rhythms) incorporated into both credible signaling and MSB hypotheses can predictably, reliably, and efficiently structure social rhythmic signals such as vocalizations, movement, gaze, and touch (Lense & Camarata, Reference Lense and Camarata2020).

The two hypotheses espoused for the evolution of musicality, which highlight the social attention components of musical activities, also inform directions regarding the therapeutic use of music in ASD and Williams syndrome. Investigations of MSB must consider the bidirectionality of the interaction and the needs and goals of both social partners. For example, musical activities between parents and their child with a neurodevelopmental disability are increasingly recognized as modulating parent behaviors such as parent responsiveness (e.g., physically supporting child's play through contingent imitation) (Boorom, Muñoz, Xin, Watson, & Lense, Reference Boorom, Muñoz, Xin, Watson and Lense2020; Thompson, Shanahan, & Gordon, Reference Thompson, Shanahan and Gordon2019) and parent mood (Williams, Berthelsen, Nicholson, Walker, & Abad, Reference Williams, Berthelsen, Nicholson, Walker and Abad2012), thus enhancing the likelihood of child engagement downstream. Music and song may be a particularly meaningful platform for social communication in light of the altered language and social communication abilities in ASD and Williams syndrome (Mervis & Velleman, Reference Mervis and Velleman2011; Tager-Flusberg, Reference Tager-Flusberg2000). Consistent with tenets of the MSB hypothesis for the efficacy of music in large groups, music-based activities may scale to larger interaction contexts beyond the parent–child dyad, and to new interaction partners, because of the effective and rewarding aspects of musical activities for participants (Lense & Camarata, Reference Lense and Camarata2020).

Neurobiologically, individuals with Williams syndrome and ASD exhibit brain structural and functional differences in regions important for rhythm processing (e.g., basal ganglia and somatomotor connectivity; Campbell et al., Reference Campbell, Daly, Toal, Stevens, Azuma, Karmiloff-Smith and Murphy2009; Estes et al., Reference Estes, Shaw, Sparks, Friedman, Giedd, Dawson and Dager2011; Vega, Hohman, Pryweller, Dykens, & Thornton-Wells, Reference Vega, Hohman, Pryweller, Dykens and Thornton-Wells2015). These differences in brain structure and connectivity may be functionally linked to social and musical profiles. Children with ASD who underwent a music intervention exhibited higher communication scores and functional connectivity between auditory and motor regions (cortical and subcortical) compared to a non-music intervention control group following the intervention (Sharda et al., Reference Sharda, Tuerk, Chowdhury, Jamey, Foster, Custo-Blanch and Hyde2018). In addition, individuals with ASD exhibit increased functional connectivity between left frontal and temporal regions for song compared to speech (Lai, Pantazatos, Schneider, & Hirsch, Reference Lai, Pantazatos, Schneider and Hirsch2012). Different neural mechanisms for processing music and language may provide a basis for using music-based activities in these populations (Sharda, Midha, Malik, Mukerji, & Singh, Reference Sharda, Midha, Malik, Mukerji and Singh2015). Additionally, behavioral work suggests links between beat perception and adaptive communication abilities in Williams syndrome (Lense & Dykens, Reference Lense and Dykens2016) and appropriate sensorimotor rhythmic synchronization under some circumstances in ASD (Tryfon et al., Reference Tryfon, Foster, Ouimet, Doyle-Thomas, Anagnostou, Sharda and Hyde2017). These behavioral studies further support investigation into if and how musical rhythm activities may modulate neural connectivity between sensorimotor and reward related regions in these populations. The neuroanatomical hubs of the MSB hypothesis (e.g., basal ganglia, implicated in both the reward system and in processing “beat-based” rhythms; Matthews, Witek, Lund, Vuust, & Penhune, Reference Matthews, Witek, Lund, Vuust and Penhune2020) provide a relevant framework for assessing how these regions may relate to music's social bonding function in individuals with atypical social communication.

Brain-to-brain synchrony (i.e., “neural resonance” component of the MSB hypothesis) is an important neurobiological mechanism for successful communication (Hasson, Ghazanfar, Galantucci, Garrod, & Keysers, Reference Hasson, Ghazanfar, Galantucci, Garrod and Keysers2012; Nguyen et al., Reference Nguyen, Schleihauf, Kayhan, Matthes, Vrtička and Hoehl2020). When considering music as a credible signal for parent–infant interactions, social interactions emphasizing musical elements (e.g., song) may strengthen neural synchrony across the dyad. This may be particularly effective for individuals with Williams syndrome or ASD for whom music may be a more salient cue for social interactions. Predictable musical experiences paired with salient social signals (e.g., eye gaze; Leong et al., Reference Leong, Byrne, Clackson, Georgieva, Lam and Wass2017) may facilitate rewarding interactions between dyads. Populations with neurodevelopmental disorders may offer a unique lens into how brain-to-brain synchrony in parent–child dyads is modulated by musical and non-musical activities. Both the credible signaling (Mehr et al., target article) and MSB (Savage et al., target article) hypotheses provide relevant frameworks for understanding the neurobiology underlying musicality and social communication in Williams syndrome and ASD.

Financial support

This study was supported in part by the National Institute of Mental Health (NIMH), National Center for Complementary and Integrative Health (NCCIH) [R61MH123029], National Institute on Deafness and Other Communication Disorders (NIDCD) [R21DC016710], the National Institutes of Health Office of the Director (DP2HD098859), National Endowment for the Arts Research Lab (1863278-38), and the National Science Foundation (NSF) [1926794] and NSF GRFP. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funders.

Conflict of interest

None.

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