Maintenance of Hand Motor Recovery Following Action Observation Treatment for Stroke

Special Article - Neurorehabilitation

Austin J Clin Neurol 2017; 4(4): 1114.

Maintenance of Hand Motor Recovery Following Action Observation Treatment for Stroke

Riley JD1*, Falcon MI2, Small SL1, Collins K3, Chen EE1, Buccino G4 and Solodkin A1,2

¹Department of Neurology, University of California Irvine, USA

²Department of Anatomy & Neurobiology, University of California Irvine, USA

³Department of Rehabilitation Sciences, University of East Anglia, UK

4Department of Medical and Surgical Sciences, University Magna Graecia, Italy

*Corresponding author: Riley JD, Department of Neurology, University of California Irvine, 100 Irvine Hall Irvine, CA, 92697, USA

Received: May 31, 2017; Accepted: June 26, 2017; Published: July 06, 2017

Abstract

Background: Current approaches to stroke rehabilitation can be effective at conferring functional gains; and yet these gains are commonly lost once therapy has ended. It is therefore imperative to develop rehabilitative methods that foster the maintenance of functional gains over the long-term. We propose that shifting emphasis away from behavioral compensation and toward remediation could lead to significant advances in maintenance of therapeutic gains. Whereas it has been shown that Action Observation Therapy (AOT) is effective at improving motor functioning following stroke, the present study tests the hypothesis that AOT can improve function and preserve functional gains for at least six months following therapy.

Methods: Structural and resting functional MRI scans and measures of hand motor function were obtained in 21individuals with chronic stroke prior to, immediately following, and six months to one year after a one month course of either AOT or a control therapy (neuro developmental therapy; NDT).

Results: AOT resulted in significant gains in motor function immediately after therapy and six months to one year later. Modest gains were seen following NDT at both time points. Individuals receiving AOT performed significantly better than those receiving NDT on the Nine Hole Peg Test at maintenance. Importantly, maintenance of gains with AOT was related to baseline stability of resting functional connectivity, unlike the NDT group.

Conclusion: This study suggests that AOT, but not a standard physical therapy approach, may remediate neural networks critical for motor function after stroke, and that these gains are maintained over the long term.

Keywords: Mirror neuron system; Stroke rehabilitation; Network stability; Functional connectivity

Introduction

Stroke remains a major source of disability in the United States; with approximately 6.5 million individuals living with long-term impairments [1]. Following initial hospitalization and stabilization; stroke survivors usually undergo rehabilitative physical therapy with an emphasis on recovery of Activities of Daily Living (ADLs). Neuro Developmental Therapy (NDT); for example; is a widely used treatment; and has been shown to be as effective as other therapies [2]. Although functional gains are often seen initially; it is all too common for the stroke survivor to stagnate or even regress following the completion of such therapy [3]. Maintenance of gains following rehabilitative therapy is a crucial but often an unsuccessful component of stroke care. It is therefore imperative to develop rehabilitative therapies that maximize functional gains; returning the individual to self-sufficiency as quickly as possible; while at the same time maintaining these gains over the long term.

Currently; improved function may occur during the course of standard therapy; only to be lost upon completion. Physical therapy for upper extremity weakness generally focuses on training an individual to compensate for weakness by shifting functionality to remaining motor effectors; typically through some degree of trunk rotation/displacement; scapular elevation; shoulder abduction; and/ or internal rotation [4]. While this may expedite improvement in ADLs; it has limitations for long-term maintenance. The required motor adaptations confer a risk of developing new; less natural motor patterns that may lead to decreased range of motion; pain; and learned disuse [4]. Furthermore; following such therapy; stroke survivors often have limited access to further therapy; partly due to the high cost of providers [5] and of specialized therapeutic equipment [6].

Most contemporary physical therapy does not address the underlying neurophysiologic changes occurring in the brain following stroke; and thus has only indirect and unfocused effects on development of sustainable neuronal substrates. One effort aimed at remediation is Constraint Induced Motor Therapy (CIMT). In CIMT; the unaffected arm is intermittently restrained to encourage greater use of the affected arm; leading to improvement in function following stroke. However; these gains appear to be compensatory in nature [7] and arm restraint is often perceived as unpleasant for the stroke survivor [8]; thus complicating the potential for long term gains. Indeed; accumulating evidence suggests that CIMT is not superior to standard therapy in providing long term functional gains [9,10]. Electrical stimulation therapies aim to improve motor function by influencing neuronal activity directly [11]. Although some benefits appear to outlast the stimulation period [12]; the degree to which they are maintained is unclear [13]. Cellular based strategies (e.g., stem cells) offer the potential for true neuronal remediation [14]; but these require further testing before their immediate and long term efficacy will be known. Given the extensive study of emerging therapies such as these; it is striking that their effect on long-term maintenance has not received much attention.

Action Observation Treatment (AOT) is an emerging therapeutic technique that has the potential to address many of these shortcomings [15,16]. At a neuronal network level; AOT aims to the extent possible; to stimulate the brain network involved in observation and imitation of motor actions; and by doing so; to reestablish motor functioning targeting the pre-stroke state via the repair or reorganization of neural circuitry. The rationale for this approach comes from neurophysiological data from macaque [17]; in which neurons in the posterior parietal lobe and inferior premotor cortex process perceived motor actions. This “mirror neuron system” is increasingly understood to play a role in action observation and imitation in humans [18,19]. We hypothesize that using AOT to harness this motor circuit for stroke rehabilitation represents a promising remediative approach; and has particular promise for both immediate therapeutic benefits and maintenance of these gains over the long term. Indeed; previous studies have supported the effectiveness of AOT in functional recovery following stroke [20-22]. In this work; we seek to expand upon these findings; comparing AOT to a widely used rehabilitative treatment; furthermore; we include multiple neuroimaging techniques in order to gain insight into the mechanism underlying functional gains associated with AOT.

Resting State Functional Connectivity (rsFC) provides insight into the baseline coupling between brain regions; and thus the organization of neural networks of an individual [23]. Previous studies have provided evidence that rsFC relates to both underlying neural activity as well as the structural connectivity of the brain [24]. To date; rsFC has been predominantly quantified using an average measure over the course of a scan; but such connectivity is in fact not stable; but rather tends to vary over time [25]. One way to characterize such dynamic rsFC is by assessing the stability and variance of interactions between regions over time. For example; Shen and colleagues [26] found that homotopic functional connectivity; facilitated by direct anatomical connections; was more stable over time when compared to other types of connections. Furthermore; the degree of variability of brain signal has been shown to be related to cognitive functioning in both healthy [27] and damaged [28] brains. Investigating the stability and variance of functional connectivity can therefore provide critical insight into the mechanisms underlying changes in the brain.

Objective

We hypothesize training motor observation and imitation in ecological patient-specific tasks via AOT will depend on the stability of brain networks in order to perform motor tasks following ischemic stroke. We further expect a direct effect of this approach on the long term; with an extended maintenance phase following therapy.

Materials and Methods

Twenty-one volunteers (age 57.9 ± 9.7 years; mean ± standard deviation) with chronic stroke were recruited for this study. Individuals were screened using the mini-mental state exam (MMSE) [29]; the short version of the Token Test [30]; the Edinburgh handedness inventory [31] and Hamilton depression inventory [32]. Inclusion criteria included age ≥ 18 years; single stroke by clinical history; lesion in the middle cerebral artery distribution; stroke onset ≥ 6 months earlier; moderate to severe hand impairment (50 ≥ Fugl- Meyer Score ≥ 20); normal state of consciousness; normal corrected visual and auditory acuity; language comprehension (short Token test ≥ 26); and upper extremity protective responses. Exclusion criteria included history of significant central neurological illness other than stroke; history of significant arm injury with residual functional impairment; history of spinal cord injury; cognitive impairment (Mini Mental Status Exam < 23); untreated depression (Center for Epidemiologic Studies Depression scale ≥ 16; visual neglect; significant carotid stenosis; metallic implants; pregnancy; and severe spasticity in affected arm (Ashworth Scale ≥ 3). Patient demographics are in Table 1. All participants provided informed consent prior to inclusion in the study; and all procedures were approved by the Institutional Review Boards of the University of Chicago and the University of California; Irvine.