Journal Articles 2020 Cortical encoding of melodic expectations in human temporal cortex G. M. Di Liberto C. Pelofi R. Bianco P. Patel A. D. Mehta Zucker School of Medicine at Hofstra/Northwell, [email protected] See next page for additional authors Follow this and additional works at: https://academicworks.medicine.hofstra.edu/articles Part of the Neurosurgery Commons Recommended Citation Di Liberto GM, Pelofi C, Bianco R, atelP P, Mehta AD, Herrero JL, de Cheveigne A, Shamma S, Mesgarani N. Cortical encoding of melodic expectations in human temporal cortex. 2020 Jan 01; 9():Article 7471 [ p.]. Available from: https://academicworks.medicine.hofstra.edu/articles/7471. Free full text article. This Article is brought to you for free and open access by Donald and Barbara Zucker School of Medicine Academic Works. It has been accepted for inclusion in Journal Articles by an authorized administrator of Donald and Barbara Zucker School of Medicine Academic Works. For more information, please contact [email protected]. Authors G. M. Di Liberto, C. Pelofi, R. Bianco, .P Patel, A. D. Mehta, J. L. Herrero, A. de Cheveigne, S. Shamma, and N. Mesgarani This article is available at Donald and Barbara Zucker School of Medicine Academic Works: https://academicworks.medicine.hofstra.edu/articles/7471 RESEARCH ARTICLE Cortical encoding of melodic expectations in human temporal cortex Giovanni M Di Liberto1*, Claire Pelofi2,3†, Roberta Bianco4†, Prachi Patel5,6, Ashesh D Mehta7,8, Jose L Herrero7,8, Alain de Cheveigne´ 1,4, Shihab Shamma1,9*, Nima Mesgarani5,6* 1Laboratoire des syste`mes perceptifs, De´partement d’e´tudes cognitives, E´ cole normale supe´rieure, PSL University, CNRS, 75005 Paris, France; 2Department of Psychology, New York University, New York, United States; 3Institut de Neurosciences des Syste`me, UMR S 1106, INSERM, Aix Marseille Universite´, Marseille, France; 4UCL Ear Institute, London, United Kingdom; 5Department of Electrical Engineering, Columbia University, New York, United States; 6Mortimer B Zuckerman Mind Brain Behavior Institute, Columbia University, New York, United States; 7Department of Neurosurgery, Zucker School of Medicine at Hofstra/ Northwell, Manhasset, United States; 8Feinstein Institute of Medical Research, Northwell Health, Manhasset, United States; 9Institute for Systems Research, Electrical and Computer Engineering, University of Maryland, College Park, United States Abstract Humans engagement in music rests on underlying elements such as the listeners’ cultural background and interest in music. These factors modulate how listeners anticipate musical events, a process inducing instantaneous neural responses as the music confronts these *For correspondence: expectations. Measuring such neural correlates would represent a direct window into high-level [email protected] (GMDL); brain processing. Here we recorded cortical signals as participants listened to Bach melodies. We [email protected] (SS); [email protected] (NM) assessed the relative contributions of acoustic versus melodic components of the music to the neural signal. Melodic features included information on pitch progressions and their tempo, which † These authors contributed were extracted from a predictive model of musical structure based on Markov chains. We related equally to this work the music to brain activity with temporal response functions demonstrating, for the first time, Competing interests: The distinct cortical encoding of pitch and note-onset expectations during naturalistic music listening. authors declare that no This encoding was most pronounced at response latencies up to 350 ms, and in both planum competing interests exist. temporale and Heschl’s gyrus. Funding: See page 20 Received: 11 September 2019 Accepted: 20 January 2020 Published: 03 March 2020 Introduction Experiencing music as a listener, performer, or a composer is an active process that engages percep- Reviewing editor: Jonathan Erik Peelle, Washington University in tual and cognitive faculties, endowing the experience with memories and emotion (Koelsch, 2014). St. Louis, United States Through this active auditory engagement, humans analyze and comprehend complex musical scenes by invoking the cultural norms of music, segregating sound mixtures, and marshaling expectations Copyright Di Liberto et al. This and anticipation (Huron, 2006). However, this process rests on the ‘structural knowledge’ that listen- article is distributed under the ers acquire and encode through frequent exposure to music in their daily lives. Ultimately, this terms of the Creative Commons Attribution License, which knowledge is thought to shape listeners’ expectations and to determine what constitutes a ‘familiar’ permits unrestricted use and musical style that they are likely to understand and appreciate (Morrison et al., 2008; redistribution provided that the Hannon et al., 2012; Pearce, 2018). There is convincing evidence that musical structures can be original author and source are learnt through the passive exposure of music in everyday life (Bigand and Poulin-Charronnat, 2006; credited. Rohrmeier et al., 2011), a phenomenon that was included in several models musical learning. The Di Liberto et al. eLife 2020;9:e51784. DOI: https://doi.org/10.7554/eLife.51784 1 of 26 Research article Neuroscience connectionist model from Tillman and colleagues, which simulated implicit learning of pitch struc- tures occurring in Western music, was shown to successfully predict behavioral and neurophysiologi- cal results on music perception (Tillmann et al., 2000). Further developments led to models that accurately reflect listeners’ expectations on each upcoming note by considering both the listener’s musical background (long-term model) and proximal knowledge (short-term model) (Pearce, 2005; Huron, 2006). A similar learning process has been demonstrated in many domains of human learning (e.g., lan- guage; Saffran et al., 1997; Toro et al., 2005; Finn et al., 2014), as well as in animals that must learn their species-specific songs and vocalizations (Woolley, 2012). Theoretically, this is often con- ceptualized as learning the statistical regularities of the sensory environment (Romberg and Saffran, 2010; Erickson and Thiessen, 2015; Bretan et al., 2017; Skerritt-Davis and Elhilali, 2018) so as to predict upcoming events, in a process referred to as ‘statistical learning’. Supporting evidence is that failed predictions due to deviations in the sensory sequence produce measurable brain activa- tions that have been associated with the detection and strength of these irregularities, that is predic- tion error (Vuust et al., 2012; Clark, 2013; Moldwin et al., 2017; Omigie et al., 2019; Quiroga- Martinez et al., 2019b; Quiroga-Martinez et al., 2019a), and with learning (Storkel and Rogers, 2000; Attaheri et al., 2015; Qi et al., 2017). Decades of research have established that listeners have strong and well-defined musical expect- ations (Schmuckler, 1989; Cuddy and Lunney, 1995; Margulis, 2005; Morgan et al., 2019) which depend on a person’s musical culture (Carlsen, 1981; Kessler et al., 1984; Krumhansl et al., 2000; Eerola et al., 2009). Neurophysiology studies demonstrated that violation of music expectations elicits consistent event-related potentials (ERPs), such as the mismatch negativity (MMN) or the early right-anterior negativity (ERAN), which typically emerges between 100 and 250 ms after the onset of the violation (Koelsch, 2009; Vuust et al., 2012). Such brain responses have been measured for a range of violations of auditory regularities, including out-of-key notes embedded in chords (e.g. Neapolitan sixth in Koelsch et al., 2000), unlikely chords (e.g. double dominant in Koelsch et al., 2007), and single tones (Miranda and Ullman, 2007; Omigie et al., 2013; Omigie et al., 2019). These physiological markers enabled researchers to investigate the encoding of music expectations during development (Koelsch et al., 2003) as well as the impact of attention (Loui et al., 2005), short-term context (Koelsch and Jentschke, 2008), and musical experience (Koelsch et al., 2002) on music perception. ERP studies (Besson and Macar, 1987; Paller et al., 1992; Miranda and Ullman, 2007; Pearce et al., 2010b; Carrus et al., 2013) often limit the range of expectations’ violations strength that are tested to severe violations because of the need for repeated stimulus presentations. One issue with this approach is that notes eliciting strong violations could be considered by the listener as production mistakes (e.g., a pianist playing the wrong note), thus the corresponding cortical cor- relates may characterise only a limited aspect of the neural underpinnings of melodic perception. In fact, music sequences induce a wide range of violation strengths (Pearce and Wiggins, 2012) because the (valid) sequential events are not all equally likely (and hence not equally predictable), whether we consider note or chord sequences (Temperley, 2008) in both classical music (Rohrmeier and Cross, 2008) or more popular music genres (Temperley and Clercq, 2013). Here, we study the brain responses to continuous naturalistic musical stimuli, thus allowing us to explore the full range of expectations’ strengths. This study seeks to determine whether the neural response reflects this range of strengths by regressing the musical information with it. Music is a complex, multi-layered signal that have structures allowing predictions of a variety of properties. One layer concerns the notes sequences forming melodies,
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