Entrainment and the Motor System

MICHAEL H. THAUT Director, Center for Biomedical Research in Music, ColoradoState University

ABSTRACT: Entrainment is a universal phenomenon that can beobserved in physical (e.g., pendulum clocks) and biological systems(e.g., fire flies) when one system’s motion or signal frequency entrainsthe frequency of another system. The use of entrainment fortherapeutic purposes was established for the first time in the early1990s by Thaut and colleagues in several research studies, showingthat the periodicity of auditory rhythmic patterns could entrainmovement patterns in patients with movement disorders (Thaut,Kenyon, Schauer, & McIntosh, 1999). Physiological, kinematic andbehavioral movement analysis showed very quickly that entrainmentcues not only changed the timing of movement but also improvedspatial and force parameters. We know now that anticipatoryrhythmic templates are critical coordinative constraints in the brainfor optimal motor planning and execution. Rhythmic entrainment isone of the most important underlying mechanisms for the successfulapplication of rhythmic-musical stimuli in motor rehabilitation formovement disorders associated with stroke, Parkinson’s disease,traumatic brain injury, cerebral palsy etc. Most importantly, temporalrhythmic entrainment has been successfully extended into applica-tions in cognitive rehabilitation and speech and language rehabili-tation, and thus become one of the major neurological mechanismslinking music and rhythm to brain rehabilitation. Multiple treatmenttechniques in Neurologic Music Therapy utilize entrainment conceptsin sensorimotor, cognitive, and speech/language training.

What is Entrainment?

In 1666, the Dutch physicist Christian Huygens, theinventor of the pendulum clock, discovered that the pendulumfrequencies of two clocks mounted on the same wall or boardbecame synchronized to each other. He surmised that thevibrations of air molecules would transmit small amounts ofenergy from one pendulum to the other and synchronize themto a common frequency. However, when set on differentsurfaces, the synchronization effect disappeared. As it turnedout, the transmitting medium was actually the vibrating boardor wall. For air molecule vibrations there would have been toomuch dampening of the energy transmission, as was laterdiscovered. The effect he observed was subsequently con-firmed by many other experiments and was called entrain-ment. In entrainment the different amounts of energytransferred between the moving bodies due to the asynchro-nous movement periods cause negative feedback. Thisfeedback drives an adjustment process in which the energyis gradually eliminated to zero until both moving bodies movein resonant frequency or synchrony. The stronger ‘oscillator’locks the weaker into its frequency. When both are equallystrong, the faster system slows down and the slower systemspeeds up until they lock into a common movement period(Pantaleone, 2002).

Technically, entrainment in physics refers to the frequencylocking of two oscillating bodies, that is, bodies that can movein stable periodic or rhythmic cycles. They have differentfrequencies or movement periods when moving independent-ly, but when interacting they assume a common period.Incidentally, Huygens’ pendulums assumed a common period180 degrees out of phase, which he humorously called ‘oddsympathy.’ It is now known that entrainment can occur invarious phase relationships of the movement onsets of theoscillating bodies—often one can observe a stable phaserelationship between the two bodies. A stable phaserelationship is achieved when both bodies start and stop theirmovement period at the same time. However, this is not anecessary prerequisite for entrainment to occur. The decidingfactor for entrainment is the common period of the oscillatingmovements of the two bodies. This phenomenon is ofconsiderable importance for clinical applications of rhythmicentrainment in motor rehabilitation (Kugler & Turvey, 1987;Thaut, Bin, & Azimi-Sadjadi, 1998).

Entrainment is a common phenomenon in the physicalworld—for example, coupled oscillators, fluid waves, and soon. Entrainment also occurs in nature, for example, firefliesflashing their light signal, or circadian rhythms entraining tolight-dark cycle within the 24-hour day period. Unfortunately,the term entrainment is often also used loosely connected tomany unrelated claims—usually in the context of claims forhealth or healing—with little or no scientific evidence, forexample, brain wave entrainment, altered states of conscious-ness, trance, drum circles, or binaural beat entrainment.Therefore, it is important for the clinician who follows anevidence-based intervention model to check the scientificvalidity for therapeutic claims.

The Auditory System and Rhythm Perception

The ability of the auditory system to rapidly construct stabletemporal templates is well known (Thaut & Kenyon, 2003).The auditory system is superbly constructed to detect temporalpatterns in auditory signals with extreme precision and speed,as required by the nature of sound as only existing in temporalvibration patterns (Moore, 2003). The auditory system is fasterand more precise than the visual and tactile systems (Shelton& Kumar, 2010). Since sound waves that are most importantfor speech and music and other perceptual tasks are based onperiodic motions that repeat themselves in regularly recurringcycles, the auditory system is also perceptually geared towardsdetecting and constructing rhythmic sound patterns. However,the observation of timing in the auditory system does not stopits function there. From culture and history we know andexperience every day that the auditory and the motor systemshave a special relationship. For example, Thaut, Miller, andSchauer (1998) demonstrated that finger and arm movementsinstantaneously entrain to the period of a rhythmic stimulus

Michael H. Thaut, PhD, is professor of music and professor of neuroscience as wellas the Director at The Center for Biomedical Research in Music, Colorado StateUniversity.

� 2013, by the American Music Therapy Association

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(e.g., metronome beat) and stay locked to the metronomefrequency even when subtle tempo changes are induced intothe metronome that are consciously not perceived. Thesefindings have been confirmed by other studies (Large, Jones, &Kelso, 2002).

Two early electrophysiological studies (Paltsev & Elner1967, Rossignol & Melvill Jones, 1976) also showed howsound signals and rhythmic music can prime and time muscleactivation via reticulospinal pathways. The pathway connec-tions between the auditory and the motor system—which hadnot been given much emphasis when compared to visual andproprioceptive systems in motor control—have been re-searched much more carefully in the past 20 years ever sinceour discovery between 1991 and 1993 that rhythmicentrainment in human movement is possible and can beeffectively applied to improve motor function in movementdisorders (Thaut, McIntosh, Prassas, & Rice, 1992; Thaut,McIntosh, Prassas, & Rice, 1993; Thaut, Schleiffers, & Davis,1991). It is now well-established that the auditory system hasrichly distributed fiber connections to motor centers from thespinal cord upwards on brain stem, subcortical and corticallevels (Felix, Fridberger, Leijon, Berrebi, & Magnusson, 2011;Koziol & Budding, 2009; Schmahmann & Pandya, 2006).

Clinical Applications of Entrainment

In a number of experiments between 1991 and 1993, Thautand colleagues demonstrated that auditory rhythm and musiccan entrain the human motor system and be used to improvefunctional control of movement in healthy subjects andsubjects with stroke (see Thaut et al., 1991; Thaut et al.,1992; Thaut et al., 1993). This entrainment process in humanmovement—especially with patients with severe motordysfunction like stroke—was previously not known and neverapplied clinically. We realized that we had discovered a newconnection when we searched for existing research referencesand could not find any neuroscience or medical literatureabout rhythmic entrainment, with the two exceptions alreadymentioned above.

In healthy subjects, movement stability and variability inmuscle activation improved significantly in response torhythmic cueing but in smaller magnitude than we found inlater studies in patients with gait dysfunction (Thaut et al.,1992). Gait patterns in hemiparetic stroke training, however,showed massive entrainment effects resulting in highlysignificant improvements in velocity, stride length, cadence,stride symmetry as well significant reductions in variabilityand amplitude of motor unit recruitment (i.e., muscleactivation) (Thaut et al., 1993). Based on these findings wedeveloped a standard gait training protocol—rhythmic audi-tory stimulation (RAS)—which proved to be very effectivewhen compared to traditional gait therapies (Thaut et al.,2007). Immediate entrainment effects could be translated intolong-term training effects over three weeks (Thaut, McIntosh,& Rice, 1997) and six weeks (Thaut et al., 2007) respectively.Patients entered the studies in the sub-acute stage approxi-mately two weeks post stroke. These clinical findings havebeen replicated by a number of other research groupssubstantiating the existence of rhythmic auditory-motorcircuitry for entrainment (Ford, Wagenaar, & Newell, 2007;

Roerdink, Bank, Peper, & Beek, 2011; Roerdink, Lamoth,Kwakkel, van Wieringen, & Beek, 2007).

Of greatest importance was the finding that the injuredbrain can indeed access rhythmic entrainment mechanisms.These observations led to studying rhythmic motor circuits inthe brain more carefully. It is now well accepted that rhythmprocessing and auditory-motor interactions take place inwidely distributed and hierarchically organized neural net-works, extending from brain stem and spinal levels tocerebellar, basal ganglia, and cortical loops (Konoike et al.,2012; Thaut, 2003).

In subsequent experiments, researchers studied rhythmicentrainment in gait of persons with Parkinson’s disease (PD)(McIntosh, Brown, Rice, & Thaut, 1997; Miller, Thaut,McIntosh, & Rice, 1996; Thaut et al., 1996). Although PDpresents itself with a different neuropathology and differentmovement dysfunctions, we also discovered for the first timewith this patient group strong entrainment effects thatbenefited mobility, most noticeably in improvements inbradykinesia, more stable stride symmetry and stride length,and strengthening of motor unit recruitment. Long-termmaintenance of improvements over four to five weeks wasdemonstrated in a later study (McIntosh, Rice, Hurt, & Thaut,1998).

RAS is now recognized as state-of the art mobility treatmentfor PD (Hoemberg, 2005). After successful experimentsentraining endogenous biological rhythms of neural gaitoscillators a new question emerged. Can rhythmic entrain-ment also be applied to entrain whole body movements,especially arm and hand movements that are not driven byunderlying biological rhythms? We found the answer byturning upper extremity movements, which are usuallydiscrete and non-rhythmic by nature, into repetitive cyclicalmovement units which now could be matched to rhythmictime cues.

In our research group we carried out two experimentsstudying hemiparetic arm reaching movements of patientswith stroke. In one study we investigated the immediate effectof rhythm on kinematic movement patterns, especiallyreaching trajectories, variability of movement timing, andelbow range of motion. Elbow range as well as both cyclicalmovement timing and smoothness of reaching trajectoriesimproved significantly (Thaut, Kenyon, Hurt, McIntosh, &Hoemberg, 2002). In a second study we measured the effect ofrepetitive rhythmic arm training using a Patterned SensoryEnhancement (PSE) protocol. Outcomes were assessed withthe Wolf Motor Function Action Test (WMFT) and the self-reporting Motor Activity Log (MAL). Both measures improvedsignificantly in a within subject design (Malcolm, Massie, &Thaut, 2009). The improvements were comparable in size to aparallel study we carried out using Constraint InducedTherapy (CIT) (Massie, Malcolm, Greene, & Thaut, 2009).We also compared trunk flexion and shoulder rotation in adiscrete arm reaching versus cyclical reaching task cued byauditory rhythm. The rhythmic cyclical task reduced trunkflexion and increased shoulder and trunk rotation comparableto normal patterns whereas in the discrete task subjects reliedmostly on extended forward flexion of the trunk to reach thetargets (Massie et al., 2009). Lastly, CIT significantly increased

32 Music Therapy Perspectives (2013), Vol. 31

shoulder abduction, bringing the arm into a more circularoutward motion, compared to pretest measures whereas PSEdecreased shoulder abduction, helping to bring the arm into amore forward trajectory. These findings might be interpretedas CIT being an excellent protocol to overcome nonuse of theparetic side, to stimulate associated brain plasticity, andincrease quantity of movement whereas auditory rhythm alsoaddresses recovery of the quality of movement, such asincrease in trunk rotation during reaching, which CIT does notfacilitate. These findings have also been supported by similarfindings in other research groups (Peng et al, 2011; Schneider,Schoenle, Altenmueller, & Muente, 2007; Whitall, McCombeWaller, Silver, & Macko, 2000).

Mechanisms of Entrainment in Motor Control

The comprehensive effect of rhythmic entrainment onmotor control raises some important theoretical questions asto the mechanisms modulating these changes. We know thatfiring rates of auditory neurons, triggered by auditory rhythmand music, entrain the firing patterns of motor neurons, thusdriving the motor system into different frequency levels.However, that is not all. There are two additional mechanismsare of great clinical importance in regard to entrainment. Thefirst is that auditory stimulation primes the motor system in astate of readiness to move. Priming increases subsequentresponse quality.

The second, more specific aspect of entrainment refers tothe changes in motor planning and motor execution it creates.Rhythmic stimuli create stable anticipatory time scales ortemplates. Anticipation is a critical element in improvingmovement quality. Rhythm provides precise anticipatory timecues for the brain to plan and be ready. Furthermore,successful movement anticipation is based on foreknowledgeof the duration of the cue period. We may remember thatduring entrainment two movement oscillators—in our caseneurally based—of different periods entrain to a commonperiod. In auditory entrainment, the motor period entrains tothe period of the auditory rhythm. Entrainment is alwaysdriven by frequency or period entrainment—that is, thecommon periods may or may not be in perfect phase lock(i.e., the onset of the motor response would be perfectlysynchronized to the auditory beat). Beat entrainment is acommonly misunderstood concept. Entrainment is not definedby beat or phase entrainment—it is defined by periodentrainment (Large et al., 2002; Nozaradan, Peretz, Missal,& Mouraux, 2011; Thaut & Kenyon, 2003).

Period entrainment offers the solution to why auditoryrhythm also changes the spatial kinematic and dynamic forcemeasures of muscle activation. For a while, we lacked aconceptual link to connect time cuing via rhythmic stimuli tospatio-dynamic parameters of motor control before theanalysis of acceleration and velocity profiles of our subjectsoffered an intriguing explanation. Why is time cuing viaperiod entrainment so helpful for the patients’ overall motorcontrol in space, time and force? The answer is simple andcomplex at the same time: rhythmic cues give the brain a timeconstraint—they fix the duration of the movement. Fore-knowledge of the duration of the movement period changescomputationally everything in motor planning for the brain.

Velocity and acceleration are mathematical time derivatives ofmovement position. We realized that by fixating movementtime through a rhythmic interval the brain’s internal time-keeper now has an additional externally triggered timekeeperwith a precise reference interval, a continuous time reference(CTR). This period presents time information to the brain atany stage of the movement. The brain knows at any point ofthe movement how much time has elapsed and how muchtime is left, enabling better mapping and scaling of optimalvelocity and acceleration parameters across the movementinterval. The brain tries to optimize the movement now bymatching it to the given template. This process will result innot only changes in movement speed, but also in smootherand less variable movement trajectories and muscle recruit-ment. We can conclude that auditory rhythm, via physiolog-ical period entrainment of the motor system, acts as a forcingfunction to optimize all aspects of motor control. Rhythm notonly influences movement timing—time as the centralcoordinative unit of motor control—but also modulatespatterns of muscle activation and control of movement inspace (Thaut et al., 1999).

With this understanding of the underlying mechanisms ofentrainment, it is less important if the patients synchronizetheir motor response exactly to the beat—it is important thatthey entrain to the rhythmic period because the periodtemplate contains the critical information to optimize motorplanning and motor execution. Consequently, patients mayactually move, as Huygens called, in any stage of ‘oddsympathy’ to the actual beat.

More Clinical Applications of Entrainment

Rhythmic entrainment extends beyond motor control.Speech rate control affecting intelligibility, oral motor control,articulation, voice quality, and respiratory strength may greatlybenefit from rhythmic entrainment using rhythm and music.Recent findings in aphasia rehabilitation suggest that therhythmic component in Melodic Intonation Therapy is equallyimportant as the activation of intact right hemispheric speechcircuitry through singing (Stahl, Kotz, Henseler, Turner, &Geyer, 2011). Neurologic Music Therapy has an excellentstandardized repertoire of evidence-based techniques forspeech and language training that is based at least in part onrhythmic entrainment mechanisms.

Lastly, the potential of temporal entrainment of cognitivefunction has only recently emerged as an important driver oftherapeutic change. Neurologic Music Therapy techniques incognitive rehabilitation are relying largely on the role oftiming in music and rhythm. In the context of new researchfindings, the time structure of music and rhythm may beconsidered a temporal scaffold to regulate attention, memory,and executive function.

In conclusion, entrainment for therapeutic purposes hasbeen used since the early 1990s, with strong researchevidence that the periodicity of auditory rhythmic patternscould improve movement patterns in patients with movementdisorders. Clinical research studies have demonstrated thatauditory rhythmic cueing changes in motor patterns in gaitand upper extremity movements. Changes in motor patternsare possible due to priming of the motor system and

Entrainment and the Motor System 33

anticipatory rhythmic templates in the brain that allow foroptimal motor planning and execution with an externalrhythmic cue. The ability for the brain to use rhythmicinformation to anticipate and plan the execution of a motorpattern has made rhythmic entrainment a valuable tool inmotor rehabilitation. More recently, temporal rhythmicentrainment has been extended into applications in cognitiverehabilitation and speech and language rehabilitation, withinitial successes indicating that mechanisms of rhythmicentrainment may be an essential tool for rehabilitation in alldomains.

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