Musical Sonification of Arm Movements in Stroke Rehabilitation Yields Limited Benefits

The possibility of using auditory information supplementary to visual feedback in order to inform patients about movements of their impaired arms is a promising new method, referred to as “sonification”.  This is way too new and novel to get to your rehab center for another 100 years. 

Sonification has been written about for 6 years. It is about time for our fucking failures of stroke associations to step up to the plate and write a stroke protocol on this. I can guarantee this won't occur. You ask your stroke patient if these limited benefits are good enough to try. THERAPISTS do not make the decision on rehab provided, the patient does by looking at the efficacy ratings of the rehab protocols.  Survivors are in charge of their rehab, do not limit their options.

Musical Sonification of Arm Movements in Stroke Rehabilitation Yields Limited Benefits

Nikou Nikmaram^1†, Daniel S. Scholz^1†, Michael Großbach¹, Simone B. Schmidt², Jakob Spogis³, Paolo Belardinelli³, Florian Müller-Dahlhaus^3,4, Jörg Remy⁵, Ulf Ziemann³, Jens D. Rollnik² and Eckart Altenmüller^1*

• ¹Institute of Music Physiology and Musicians’ Medicine, Hanover University of Music, Drama and Media, Hanover, Germany
• ²Institute for Neurorehabilitational Research (InFo), BDH-Clinic Hessisch Oldendorf, Associated Institute of Hannover Medical School (MHH), Hessisch Oldendorf, Germany
• ³Department of Neurology & Stroke, Hertie-Institute for Clinical Brain Research, Eberhard Karls University of Tübingen, Tübingen, Germany
• ⁴Department of Psychiatry and Psychotherapy, University Medical Center Mainz, Mainz, Germany
• ⁵SRH Hochschule der Populären Künste (HDPK), Berlin, Germany

Neurologic music therapy in rehabilitation of stroke patients has been shown to be a promising supplement to the often strenuous conventional rehabilitation strategies. The aim of this study was threefold: (i) replicate results from a previous study with a sample from one clinic (henceforth called Site 1; N = 12) using an already established recording system, and (ii) conceptually replicate previous findings with a less costly hand-tracking system in Site 2 (N = 30), and (iii) compare both sub-studies’ outcomes to estimate the efficiency of neurologic music therapy. Stroke patients in both sites were randomly assigned to treatment or control groups and received daily training of guided sequential upper limb movements additional to their standard stroke rehabilitation protocol. Treatment groups received sonification (i.e., changes in musical pitch) of their movements when they moved their affected hand up and down to reproduce a sequence of the first six notes of a C major scale. Controls received the same movement protocol, however, without auditory feedback. Sensors at the upper arm and the forearm (Xsens) or an optic sensor device (Leapmotion) allowed to measure kinematics of movements and movement smoothness. Behavioral measures pre and post intervention included the Fugl-Meyer assessment (FMA) and the Stroke Impact Scale (SIS) and movement data. Bayesian regression did not show evidence supporting an additional effect of sonification on clinical mobility assessments. However, combined movement data from both sites showed slight improvements in movement smoothness for the treatment group, and an advantage for one of the two motion capturing systems. Exploratory analyses of EEG-EMG phase coherence during movement of the paretic arm in a subset of patients suggested increases in cortico-muscular phase coherence specifically in the ipsilesional hemisphere after sonification therapy, but not after standard rehabilitation therapy. Our findings show that musical sonification is a viable treatment supplement to current neurorehabilitation methods, with limited clinical benefits. However, given patients’ enthusiasm during training and the low hardware price of one of the systems it may be considered as an add-on home-based neurorehabilitation therapy.

Introduction

Stroke survivors frequently suffer from severe disabilities. Stroke may lead to impairments in motor and sensory systems, emotion regulation, language perception, and cognitive functions (Morris and Taub, 2008). Impaired arm function caused by gross-motor disability is also a common consequence of stroke immensely affecting quality of life in a considerable number of patients. In this case, regaining control over body movements is one of the crucial components in post-stroke recovery. There is an urgent need for effective motor rehabilitation approaches to improve quality of life in stroke survivors. Different therapeutic approaches such as Constraint Induced Movement Therapy (CIMT), mental practice, robot-aided therapy, electromyographic biofeedback, and repetitive task training have been applied to improve arm function after stroke (Langhorne et al., 2009). Of note, in a recent review it has been suggested that neurologic music therapy might be more effective than conventional physiotherapy (for a recent review see Sihvonen et al., 2017).

Motivational factors seem to play an important role for the beneficial effects of neurologic music therapy. From the patients’ informal descriptions of their experience with music-supported training, it appears that this is frequently highly enjoyable and a highlight of their rehabilitation process, regardless of the form of auditory stimulation, be it piano tones, or sonification of movement with other timbres [for a review see Altenmüller and Stewart (2018)]. However, effects of music supported therapy in stroke rehabilitation are not always consistent. In a recent review, seven controlled studies that evaluated the efficacy of music as an add-on therapy in stroke rehabilitation were identified (Sihvonen et al., 2017). In these studies, training of finger dexterity of the paretic hand was done using either a piano-keyboard, or, for wrist movements, drum-pads tuned to a C major scale. Superiority of the music group over fine motor training without music and over conventional physiotherapy was evident in one study after intervention comprising five 30-min sessions per week for 3 weeks (Schneider et al., 2010). The beneficial effect seen in the music group could be specifically attributed to the musical component of the training rather than the motor training per se, since patients practicing with mute instruments remained inferior to the music group. Here, the Fugl-Meyer Assessment (FMA) was applied before and after 20 sessions of either music supported therapy on a keyboard or equivalent therapy without sound. FMA scores of the motor functions of the upper limb improved by 16 in the music group and by 5 in the control group, both improvements being statistically significant although to a lesser degree in the control group (p = 0.02 vs. p = 0.04; Tong et al. (2015)).

With regard to the neurophysiological mechanisms of neurological music therapy, it was demonstrated that patients undergoing music supported therapy not only regained their motor abilities at a faster rate but also improved in timing, precision and smoothness of fine motor skills as well as showing increases in neuronal connectivity between sensorimotor and auditory cortices as assessed by means of EEG-EEG-coherence (Altenmüller et al., 2009; Schneider et al., 2010).

These findings are corroborated by a case study of a patient who underwent music supported training 20 months after suffering a stroke. Along with the clinical improvement, functional magnetic resonance imaging (fMRI) demonstrated activation of motor and premotor areas, when listening to simple piano tunes, thus providing additional evidence for the establishment of an auditory-sensorimotor co-representation due to the training procedure (Rojo et al., 2011). Likewise, in a larger group of 20 chronic stroke patients, increases in motor cortex excitability following 4 weeks of music-supported therapy were demonstrated using transcranial magnetic stimulation (TMS), which were accompanied by marked improvements of fine motor skills (Amengual et al., 2013).

In addition to functional reorganization of the auditory-sensorimotor network, recent findings have reported changes in cognition and emotion after music-supported therapy in chronic stroke patients. Fujioka et al. (2018) demonstrated in a 10-week-long randomized controlled trial (RCT), including 14 patients with music supported therapy and 14 patients receiving conventional physiotherapy, that both groups only showed minor improvements. However, the music group performed significantly better in the trail making test, indicating an improvement in cognitive flexibility, and furthermore showed enhanced social and communal participation in the Stroke Impairment Scale and in PANAS (Positive and Negative Affect Schedule, Watson et al., 1988), lending support to the prosocial and motivational effects of music. In another RCT with an intervention of only 4 weeks, Grau-Sánchez et al. (2018) demonstrated no superiority in fine motor skills in the music group as compared to a control group, but instead an increase in general quality of life as assessed by the Profile of Mood states and the stroke specific quality of live questionnaire. Despite growing evidence, the neurophysiological mechanisms of neurological music therapy remain poorly understood.

Most of the existing studies on music-supported therapy have focused on rehabilitation of fine motor functions of the hand. Much less evidence exists on post-stroke rehabilitation of gross motor functions of the upper limbs. In a previous study we thus developed a movement sonification therapy in order to train upper arm and shoulder functions (Scholz et al., 2015). Gross movements of the arm were transformed into discrete sounds, providing a continuous feedback in a melodic way, tuned to a major scale (i.e., patients could use movements of their paretic arms as a musical instrument). In this way, sound perception substituted for defective proprioception. In a first pilot study in subacute stroke patients we were able to demonstrate that musical sonification therapy reduced joint pain in the Fugl-Meyer pain subscale (difference between groups: −10; d = 1.96) and improved smoothness of movements (d = 1.16) in comparison to movement therapy without sound (Scholz et al., 2016). Here, we extend these findings by comparing the effects of the established musical sonification setup (Scholz et al., 2016) with a newly developed, less expensive sonification device in a group of subacute stroke patients with upper limb motor impairments. The only apparent differences between both data acquisition methods were the improved sound quality and the loss of need to strap sensors to patient limbs. In order to further elucidate the neurophysiological underpinnings of musical sonification therapy we simultaneously recorded EEG and EMG data from a subset of patients to analyze cortico-muscular phase coherence during upper limb movements (Chen et al., 2018; Pan et al., 2018). According to previous studies (Pan et al., 2018) we hypothesized that cortico-muscular phase coherence increases in the ipsilesional hemisphere after musical sonification therapy.