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Rhythmic Auditory Stimulation in Rehabilitation 263

MICHAEL H. THAUTColorado State University

MUTSUMI ABIRUKyoto University, Kyoto, Japan

PHYSIOLOGICAL RESEARCH HAS SHOWN THAT AUDITORY

rhythm has a profound effect on the motor system.Evidence shows that the auditory and motor systemhave a rich connectivity across a variety of cortical,subcortical, and spinal levels. The auditory systemafast and precise processor or temporal informationprojects into motor structures in the brain, creatingentrainment between the rhythmic signal and themotor response. Based on these physiological con-nections, a large number of clinical studies haveresearched the effectiveness of rhythm and music toproduce functional change in motor therapy for stroke,Parkinsons disease, traumatic brain injury, and otherconditions. Results have been strong in favor of rhythmicauditory stimulation (RAS) to significantly improvegait and upper extremity function. Comparative stud-ies also have shown RAS to be more effective thanother sensory cues and other techniques in physicalrehabilitation.

Received October 23, 2009, accepted December 10, 2009.

Key words: rhythmic auditory stimulation, rhythmicentrainment, neurorehabilitation, movement disor-ders, gait

OVER THE PAST TWO DECADES RESEARCHERS havebegun to elucidate the neural basis of music inthe human brain. One of the core elements ofany musical language structure, rhythm has alwaysbeen one of the primary foci of these research efforts.The study of the neurobiology of rhythm was also thefirst area in which new research insights helped toestablish a new role for music in rehabilitation, movingfrom a more social science and cultural value drivenapproach that emphasized well being and relationship

building to a neuroscience based understanding ofmusic to retrain and re-educate the injured brain.

Although throughout cultural history music andmovement were always recognized as having a close andmutually influencing relationship, the concepts usuallywere confined to emotional, motivational, or purelyartistic concepts of expression and aesthetics. However,although only poorly understand until a few yearsago, there is indeed a rich physiological basis for theinfluence of auditory rhythm on the motor system.This basis has increasingly become into clearer focusand understanding. Early landmark studies by Paltsevand Elner (1967), Rossignol and Melvill (1976), andErmolaeva and Borgest (1980) were among the first toshed light on the rich connectivity between auditoryand motor areas in the brain and what role sound andauditory rhythm could play in priming and timing ofmovement.

We now know that the rich connectivity between theauditory rhythm and movement interfaces in distrib-uted and parallel fashion throughout the brain.Research has shown evidence on the brain stem levelfor the existence of audio-motor pathways via reticu-lospinal connections. Rossignol and Melvill (1976)demonstrated priming and timing of motor responsesvia this audiospinal path using sound cues and musicalrhythms. Auditory projections into the cerebellum alsohave been demonstrated via pontine nuclei. As one ofthe nuclei in the ascending auditory pathway, the infe-rior colliculus is a source of auditory information viathalamic projections to the striatum of the basal ganglia(Koziol & Budding, 2009). The striatum in turn proj-ects to the globus pallidus as the output system of thebasal ganglia whose projections reach cortical motorstructures such as supplementary motor area and pre-motor cortex. Auditory association areas also projectback to the basal ganglia, reciprocally influencing basalganglia function in regard to sequencing, timing, andbehavioral response selection. These pathways mayplay a critical role, for instance, in the facilitative effectof music and auditory rhythm on motor output inParkinsons disease (McIntosh, Brown, Rice, & Thaut,1997). Ermolaeva and Borgest (1980) mapped auditoryfiber connectivity to determine terminal zones relative

RHYTHMIC AUDITORY STIMULATION IN REHABILITATIONOF MOVEMENT DISORDERS: A REVIEW OF CURRENT RESEARCH

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to motor projections, finding rich connections betweenprimary and secondary auditory cortices and motorcortex. In an MEG-study investigating motor synchro-nization (finger tapping) to tempo shifts in metronomecues above and below the level of conscious awareness(Tecchio, Salustri, Thaut, Pasqualetti, & Rossini, 2000),we showed that the magnitude of the auditory fieldpotentials (neural responses to time variations) covar-ied in magnitude with the temporal size of the temposhift, indicating a spatial and temporal neural codingprocess for rhythmic time measurements. The sourcefor these neural responses was located in primaryauditory cortex. These findings, in conjunction withErmolaeva and Borgests earlier data, suggest that theimmediate motor adaptations to these tempo shifts inorder to maintain synchronization were at least in partalso mediated by cortical auditory-motor pathways.

Other lines of research, especially from psychophysics,have shown that auditory (musical) rhythm may be auseful stimulus to cue motor function, due to the speedand high resolution of time processing in the auditorysystem. Taken together, conceptual understanding ofthese research findings have converged on an oscillator-entrainment model where rhythmic processes in neuralmotor networks become entrained to rhythmic time-keeper networks in the auditory system. The time-keeper networks are driven peripherally from rhythmicinputs, such as metronome or music.

Early studies to investigate these models clinicallywere carried out by Safranek, Koshland, and Raymond(1982; modulatory effect of rhythmic cuing on EMGin arm movements) and Mandel, Nymark, Balmer,Grinnell, and ORiain (1990; rhythmic feedback vs.EMG feedback in stoke gait rehabilitation). In ourresearch, we first studied the effect of rhythmic cuingon EMG activations in arm movements (Thaut,Schleiffers, & Davis, 1991) and stride parameters andelectromyography (EMG) patterns in the gait of nor-mal individuals (Thaut, McIntosh, Rice, & Prassas,1992a). We found improvement in stride symmetryand also in EMG patterns, especially the amplitudevariability in muscle contractions across the move-ment cycle. Similar results were seen in measure-ments with individual stroke, cerebellar, andtransverse myelitis patients (Thaut, McIntosh, Rice,& Prassas, 1992b). Based on these observations webegan to study Rhythmic Auditory Stimulation (RAS)as a rehabilitation technique in motor therapy. Wedeveloped standard protocols for RAS as a gait train-ing technique, which now has become standard inneurologic music therapy (NMT) and other rehabili-tation disciplines. Extensions of RAS to techniques

dealing with upper extremity and coordination train-ing have been developed successfully and are clinicallyemployed (Thaut, 2005).

RAS Gait Rehabilitation Post CVA

In a first rehabilitation study with 10 hemiparetic strokepatients who were post CVA from 4 weeks to 24 months,we used a frequency entrainment design to study theeffect of RAS on gait patterns (Thaut, McIntosh, Rice,& Prassas, 1993). Five of the participants had eitherthrombotic or hemorrhagic events affecting right cere-bral hemisphere, typically in the middle cerebral arterydistribution. Patients walked for six meters at free speedto determine their baseline walking ability. During thesecond walk RAS was matched to their baseline gaitcadence to determine if immediate entrainment effectswould occur without interference from practice. Thesame trial was repeated three times with each trialspaced a week apart. Results from this study showed aclear pattern of auditory-motor synchronization emergefor most participants. Stride time symmetry as well asstride length symmetry improved significantly, as wellas weight bearing time on the paretic side (p < .05).Stride time variability decreased to a significant degree.Participants also showed a more balanced muscular acti-vation pattern on EMG between the paretic and non-paretic limbs. Furthermore, a decrease in integratedamplitude variability of EMG was noted on the pareticside (p < .05). Other gait kinematic improvements withRAS included significant increase in center of mass ver-tical displacement and a significant reduction in lateraldisplacement, resulting in a smoother forward gait tra-jectory (Prassas, Thaut, McIntosh, & Rice, 1997).

The potential therapeutic effect of RAS subsequentlywas studied in a six-week daily training study with 10stroke patients in a RAS gait training group, and amatched control group of 10 patients using conven-tional physical therapy gait training (Thaut, McIntosh,& Rice, 1997). Patients entered the study within anaverage of 15 days post CVA, as soon as they couldwalk for five meters with hand-held assistance. Resultsshowed a significantly stronger (p < .05) improvementin gait velocity and stride length for the RAS group anda nonsignificant trend for improved stride symmetry.Gait velocity in the RAS group had improved by 164%over pretest vs. 107% in the control group. Stride lengthhad improved by 88% with RAS vs. 34% with conven-tional physical therapy. Symmetry improvements were32% for RAS and 16% for the control group. Also, thereduction of variability of EMG activation patterns inthe gastrocnemius muscle was significantly stronger at

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