Ann. N.Y. Acad. Sci. ISSN 0077-8923

A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S Issue: The Neurosciences and Music V

Motor responses to a steady beat Rebecca S. Schaefer1 and Katie Overy2,3 1 SAGE Center for the Study of the Mind, University of California, Santa Barbara, California. 2 Institute for Music in Human and Social Development, Reid School of Music,University of Edinburgh, Edinburgh, United Kingdom. 3 Don Wright Faculty of Music, University of Western Ontario, London, Ontario, Canada

Address for correspondence: Katie Overy, Institute for Music in Human and Social Development, Reid School of Music, University of Edinburgh, 12 Nicolson Square Edinburgh, Edinburgh, Scotland EH8 9DF, United Kingdom. [email protected]

It is increasingly well established that music containing an isochronous pulse elicits motor responses at the levels of both brain and behavior. Such motor responses are often used in pedagogical and clinical practice to induce movement, particularly where motor functions are impaired. However, the complex nature of such apparently universal human responses has, arguably, not received adequate research attention to date. In particular, it should be noted that many adults, including those with disabilities, find it somewhat difficult to synchronize their movements with a beat with perfect accuracy; indeed, perfecting the skill of being musically “in time” can take years of training during childhood. Further research is needed on the nature of both the specificity and range of motor responses that can arise from the perception of a steady auditory pulse, with different populations, musical stimuli, conditions, and required levels of accuracy in order to better understand and capture the potential value of the musical beat as a pedagogical and therapeutic tool. Keywords: beat perception; movement responses; cerebellum; rehabilitation; pedagogy

Introduction A remarkable aspect of most musical styles from around the globe is the almost ubiquitous use of a steady pulse, underlying widely diverse musical structures and contexts. A striking feature of this steady pulse is its capacity to coordinate human attention and movement in time, thus facilitating group activities such as singing, physical labor, and dancing. One reason that humans are able to synchronize with such a beat is that they can use the regularity of a series of pulses to predict the onset of an upcoming pulse, allowing a nod, tap, or sway to arrive in time with, and often even with slight anticipation of, the beat.1 When a group of individuals synchronizes to the same beat or even simply listens to a piece of music, this creates an environment in which the behavior of others can be better predicted, previously described as an environment of “minimized prediction error.”2 This situation, in which coordination between individuals is facilitated, can create a sense of affiliation3 and lead to increased cooperation in both adults4 and children.5

Within this musical scenario, the connection between pulse and movement is clearly a central feature—from the regular motor actions required to create a physical, acoustic pulse to the induced motor responses upon hearing a steady pulse. Music containing a steady beat can, of course, elicit a wide range of movements in listeners, from isolated movements such as clapping and tapping, to whole body movements such as jumping and dancing. Advances in auditory brain imaging research have begun to elucidate the relationship between rhythm perception and the engagement of neural regions that are involved in active movement. For example, specific motor network regions, such as the basal ganglia, premotor cortex, supplementary motor area, and cerebellum, are consistently reported as being involved in simply listening to rhythms, in the absence of any movement.6–9 The effects of rhythmic complexity on motor networks have also been described,10 as have distinctions between regions engaged when finding versus tracking the beat.11 Studies into the neural mechanisms involved when entraining doi: 10.1111/nyas.12717

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movement to sound have reported that synchronizing dance steps or simple wrist movements to music leads to increased cerebellar activation, when compared to the same movement carried out without music.12,13 In addition, adjusting the synchronization of finger taps to a tempo-varying metronome has been found to engage two distinct networks: one that includes motor network areas such as the primary motor, premotor, and supplementary motor areas and the cerebellum, and another involving medial cortical areas such as the medial prefrontal and posterior cingulate cortices, interpreted as related to higher social–cognitive aspects of synchronization.14 This link between auditory rhythm perception and motor response carries potential for a wide range of therapeutic and educational applications, and thus, when considering the musical features that might be necessary for genuine musical engagement to take place in a pedagogical or clinical context, a steady beat presents an excellent candidate. Indeed, music therapists and educators have focused on the use of the beat in practice for many years, in support of motor timing skills. For example, a steady auditory beat, presented either within music or using a metronome, lies at the basis of neurologic music therapy (NMT),15 with applications for a range of different therapeutic goals. Rhythms with a steady beat are also increasingly used in movement rehabilitation of (most commonly) gait and upper-limb function,16 as well as in rehabilitating aphasic speech.17,18 It has also often been suggested that children with language and literacy difficulties can benefit from beat-based rhythm and motor activities.19–22 However, there are a number of factors that still need to be addressed with regard to the use of moving to a beat as part of a music intervention, and more specifically, in determining how the beat can be used effectively. For example, specific features of a rhythmic stimulus are likely to have specific effects on the nature of the motor responses, whole-body responses may sometimes be more appropriate than finger-tapping paradigms, and the developmental stage or level of ability of the participants must be taken into consideration. In particular, it should be noted that many adults, including those with disabilities, can find it somewhat difficult to synchronize their movements with a beat with perfect accuracy. Even in healthy adults, a range of

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interindividual differences has been reported in beat perception,22,23 synchronization abilities, and synchronization styles.24 For such a universal human behavior, there seems to be a somewhat surprising lack of accuracy in the human population in achieving perfect timing—it seems that temporal precision is not necessarily a core feature of this behavior in everyday music making. Arguably, the process of entraining movement to an auditory rhythm incorporates several elements, such as hearing the beat (or beat induction), tracking the beat (detecting any changes in the phase and period of the pulse), using motor control to align movement to this beat, and being able to adjust the movement once a deviation between the auditory rhythm and the time structure of the movement is detected. Only a combination of these skills allows successful movement entrainment, and even then, the accuracy is variable (although this may improve greatly with practice). It may be beneficial to consider the synchronization process in these terms when considering the characteristics of rhythm-based interventions. Of course, clinical and pedagogical interventions always need to be tailored to their specific target groups, and as such, specialist knowledge on how an auditory beat might be processed by that population is an important consideration in the design of effective interventions. However, current research into beat processing and entrained movement for the specific populations who may benefit from rhythm-based interventions is in its early stages. Such investigations may involve a variety of methods, from self-reports of affect, to behavioral observations and measures, to brain imaging, with different approaches potentially elucidating different aspects of rhythm perception and entrained movement. For instance, when considering interventions aimed at children, research into young children’s spontaneous responses to a musical beat has the potential to inform how children perceive and process rhythms, and whether tempo, degrees of rhythm complexity, or group contexts can influence these responses and thus might be important for an intervention’s success. Although an engaging musical beat can lead children to spontaneously perform periodic, biphasic movements from a very early age,25 these movements are rarely accurately timed—the skill of being musically “in time” can take years of training during childhood. Supporting this developmental perspective, a recent study

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Figure 1. Musically cued versus self-paced (SP) wrist movements. The section shows the left cerebellum VI region activation cluster for the musically cued condition relative to the self-paced condition, displayed on the MRIcron reference T1 image in MNI space (FWE cluster-corrected at P < 0.05). The parameter estimate plot shows mean percent signal change of the self-paced (white) and music (grey, M) conditions relative to rest in cluster peak voxel (x = −27, y = −58, z = −23). For more details, see Schaefer et al.36

by Cirelli et al.26 investigated beat-induced electrical brain responses in children and adults and found that the cortical beta band showed similar but weaker responses to beat perception in 7-yearold children as compared to adults. Individuals with Parkinson’s disease (PD), for whom rhythm-based gait interventions have been relatively successful,27 have been reported to have impaired beat perception,28 while improved perceptual abilities have been reported for PD patients who participated in a musically cued movement intervention.29 However, a review of music-based interventions intended to rehabilitate gait in PD patients indicates that only those interventions employing gait-related practice actually improve gait,30 highlighting the fact that, although different kinds of rhythmic music may facilitate rehabilitation, the design of the intervention still needs to be specific to not only the target population but also the intended outcome. There are also indications that a certain level of cognitive functioning is necessary to be able to synchronize movement to sound; findings from patients with Alzheimer’s disease indicate that both musical and metronome cues can actually impair gait in this population, with post hoc analyses relating the level of impairment to the level of executive functioning.31 Difficulties in synchronizing movement to a metronome have also been interpreted as being due to an attentional impairment in patients with Huntington’s disease.32 Another important avenue of investigation is the capacity of different kinds of auditory stimuli to

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trigger movement. For example, the subjective experience of “groove” in music (created by the addition of syncopated rhythms to a steady beat pattern) has been reported to be inversely related to selfreported difficulty with moving along to music,33 while increased volume levels at bass drum frequencies have been found to lead to larger movement choices.34 Stimulus effects have also been found at the level of neural processing, with the performance of simple wrist flexions to music found to result in differing neural activation in motor regions, compared to moving with a metronome.35 As mentioned earlier, increased cerebellar activation has previously been reported for movement entrained to music as compared to the same movement without music,12,13 suggesting that extra neural engagement may be necessary to align movement to sound. In the two studies referred to, the location of the increased cerebellar activation was slightly different; for Brown et al.,12 the main cluster of activity related to entraining movement to music was located in the vermis of cerebellum III, whereas for Schaefer et al.,13 the increased activation was found in left cerebellum VI (Fig. 1). This difference could possibly be explained by the use of different movements: the former study looked at a relatively complex sequence of tango dance steps, whereas the latter study focused on a simple, regular, wristflexion movement requiring very little attention or practice. The latter is in line with the type of intuitive, periodic, biphasic movement that inherently and automatically induces a beat, suggesting

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that the cerebellum VI activation may be related to auditory motor connectivity in the case of a simple, almost pre-attentive movement. It is noteworthy that the movement itself already includes some aspect of temporal control, and it is possible that the self-pacing or generating of a beat during uncued movement activates an internally generated representation or image of a temporal structure.36 Thus, a possible implication of the additional cerebellar activation is that aligning periodic movement to a beat requires extra processing, even when the movement is very simple or even automatic. This extra processing may be negligible in healthy individuals, especially if accuracy is not crucial, but for patient populations, or situations where extreme accuracy is needed (such as in ensemble musical performance), the effort of entraining might become more obvious. From the above discussion a number of conclusions can tentatively be drawn, and future directions can be proposed. First, it is clear that the beat in musical rhythm is not perceived in the same way by all populations; nor is the level of attention that is necessary for accurate beat tracking always present, or the motor control that is necessary to adjust movement to sound. Moreover, moving to a beat, although often considered to be a spontaneous, automatic process, is not a trivial ability, even in healthy adults, who show a range of interindividual differences in accuracy. Moving in time with the precision that is necessary for musical performance is learned over many years, requiring much practice. Further research is needed on how the beat in musical rhythm can be most useful or effective for specific intervention target groups, rather than assuming that the same kinds of musical activities might be valuable and effective for all. A decomposition of the process of synchronizing movement with sound may be helpful to further clarify this issue. As such, the ability to perceive a beat, track a beat, move to sound, and make adjustments when accuracy goes astray, could perhaps be investigated separately in groups for whom rhythmbased interventions are developed. For example, the mechanisms by which cued movement may be found to be beneficial (for instance, in the case of recovering movement abilities) may be found to be different for different patient groups.16 Although recent research findings are beginning to shed light

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on these issues, we are only just beginning to understand the neural mechanisms of rhythmic and metrical organization in music. Thus, future research should uncover increasingly detailed information with which to understand the potential value of the musical beat as a pedagogical and therapeutic tool. Acknowledgments We acknowledge the support of the European Commission under the Marie Curie Intra-European Fellowship Program (Grant FP7-2010-PEOPLE-IEF 276529). R.S.S. also acknowledges the support of the SAGE Center for the Study of the Mind at the University of California, Santa Barbara. Conflicts of interest The authors declare no conflicts of interest. References 1. Repp, B.H. 2005. Sensorimotor synchronization: a review of the tapping literature. Psychon. Bull. Rev. 12: 969–992. 2. Overy, K. & I. Molnar-Szakacs. 2009. Being together in time: musical experience and the mirror neuron system. Music Percept. 26: 489–504. 3. Wiltermuth, S. & C. Heath. 2009. Synchrony and cooperation. Psychol. Sci. 20: 1–5. 4. Kokal, I., A. Engel, S. Kirschner & C. Keysers. 2011. Synchronized drumming enhances activity in the caudate and facilitates prosocial commitment—if the rhythm comes easily. PloS One 6: e27272. 5. Kirschner, S. & M. Tomasello. 2010. Joint music making promotes prosocial behavior in 4-year-old children. Evolut. Human Behav. 31: 354–364. 6. Bengtsson, S.L., N. Ull´eF, H.H. Ehrsson, et al. 2009. Listening to rhythms activates motor and premotor cortices. Cortex 45: 62–71. 7. Chen, J.L., V.B. Penhune & R.J. Zatorre. 2008. Listening to musical rhythms recruits motor regions of the brain. Cerebral Cortex 18: 2844–2854. 8. Grahn, J.A. & M. Brett. 2007. Rhythm and beat perception in motor areas of the brain. J. Cogn. Neurosci. 19: 893–906. 9. Grahn, J.A. & J.B. Rowe. 2009. Feeling the beat: premotor and striatal interactions in musicians and nonmusicians during beat perception. J. Neurosci. 29: 7540–7548. 10. Chen, J.L., V.B. Penhune, R.J. Zatorre. 2008. Moving on time: brain network for auditory-motor synchronization is modulated by rhythm complexity and musical training. J. Cogn. Neurosci. 20: 226–239. 11. Grahn, J.A. & J.B. Rowe. 2013. Finding and feeling the musical beat: striatal dissociations between detection and prediction of regularity. Cerebral Cortex 23: 913–921. 12. Brown, S., M.J. Martinez & L.M. Parsons. 2006. The neural basis of human dance. Cerebral Cortex 16: 1157–1167. 13. Schaefer, R.S., A.M. Morcom, N. Roberts & K. Overy. 2014. Moving to music: effects of heard and imagined musical cues

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26. Cirelli, L.K., D. Bosnyak, F.C. Manning, et al. 2014. Beatinduced fluctuations in auditory cortical beta-band activity: using EEG to measure age-related changes. Front. Psychol. 5: 742. 27. Nombela, C, L.E. Hughes, A.M. Owen & J.A. Grahn. 2013. Into the groove: can rhythm influence Parkinson’s disease? Neurosci. Biobehav. Rev. 37: 2564–2570. 28. Grahn, J.A. & M. Brett. 2009. Impairment of beat-based rhythm discrimination in Parkinson’s disease. Cortex 45: 54–61. 29. Benoit, C.-E., S. Dalla Bella, N. Farrugia, et al. 2014. Musically cued gait-training improves both perceptual and motor timing in Parkinson’s disease. Front. Human Neurosci. 8: 494. 30. DeDreu, M.J., A.S.D. vander Wilk, E. Poppe, et al. 2012. Rehabilitation, exercise therapy and music in patients with Parkinson’s disease: a meta-analysis of the effects of musicbased movement therapy on walking ability, balance and quality of life. Parkinsonism Relat. Disorders 18:(Suppl 1): S114–S119. 31. Wittwer, J.E., K.E. Webster & K. Hill. 2013. Effect of rhythmic auditory cueing on gait in people with Alzheimer disease. Arch. Phys. Med. Rehab. 94: 718–724. 32. Johnson, K.A., J.E. Bennett, N. Georgiou, et al. 2000. Bimanual co-ordination in Huntington’s disease. Exp. Brain Res. 134: 483–489. 33. Janata, P., S.T. Tomic & J.M. Haberman. 2012. Sensorimotor coupling in music and the psychology of the groove. J. Exp. Psychol. Gen. 141: 54–75. 34. VanDyck, E., D. Moelants, M. Demey, et al. 2013. The impact of the bass drum on human dance movement. Music Percept. 30: 349–359. 35. Schaefer, R.S., A.M. Morcom, N. Roberts & K. Overy. 2014. “Motor network effects of movement cueing.” In The Neurosciences and Music V—Cognitive Stimulation and Rehabilitation. Dijon, France. 36. Schaefer, R.S., A.M. Morcom, N. Roberts & K. Overy. 2014. “fMRI measures of cued movement.” In Proceedings of the ICMPC-APSCOM 2014 Joint Conference. M. K. Song, Ed.: 176. Seoul: College of Music, Yonsei University.

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Motor responses to a steady beat.

It is increasingly well established that music containing an isochronous pulse elicits motor responses at the levels of both brain and behavior. Such ...
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