[Systematic review] The potential of real-time fMRI neurofeedback for stroke rehabilitation – Full Text

Abstract

Real-time functional magnetic resonance imaging (rt-fMRI) neurofeedback aids the modulation of neural functions by training self-regulation of brain activity through operant conditioning. This technique has been applied to treat several neurodevelopmental and neuropsychiatric disorders, but its effectiveness for stroke rehabilitation has not been examined yet. Here, we systematically review the effectiveness of rt-fMRI neurofeedback training in modulating motor and cognitive processes that are often impaired after stroke. Based on predefined search criteria, we selected and examined 33 rt-fMRI neurofeedback studies, including 651 healthy individuals and 15 stroke patients in total. The results of our systematic review suggest that rt-fMRI neurofeedback training can lead to a learned modulation of brain signals, with associated changes at both the neural and the behavioural level. However, more research is needed to establish how its use can be optimized in the context of stroke rehabilitation.

1. Introduction

The number of stroke survivors is continuously increasing with the ageing of the population: about 15 million people worldwide suffer from stroke every year, of whom 5 million die, whereas another 5 million become chronically disabled (WHO, 2012). Behavioural deficits in cognitive and motor domains are highly prevalent and persistent in stroke survivors (Bickerton et al., 2014; Demeyere, Riddoch, Slavkova, Bickerton, & Humphreys, 2015; Demeyere et al., 2016; Jaillard, Naegele, Trabucco-Miguel, LeBas, & Hommel, 2009; Planton et al., 2012; Verstraeten, Mark, & Sitskoorn, 2016). Neurophysiological and neuroimaging studies suggested that stroke causes network-wide changes across structurally intact regions, directly or indirectly connected to the site of infarction (Carrera & Tononi, 2014; Carter et al., 2010; Gillebert & Mantini, 2013; Grefkes et al., 2008; Ward & Cohen, 2004). Disruptions in even one of the many networks or brain regions implicated in the different aspects of motor function and cognition can have a major impact on quality of life (Achten, Visser-Meily, Post, & Schepers, 2012; Hochstenbach, Mulder, Limbeek, Donders, & Schoonderwaldt, 1998). Accordingly, both local tissue damage and secondary changes in brain function should be considered when developing rehabilitation strategies to improve the recovery rate and generally increase the quality of life in stroke survivors (Chechlacz, Mantini, Gillebert, & Humphreys, 2015; Chechlacz et al., 2013; Corbetta et al., 2015; Gillebert & Mantini, 2013). In this regard, the use of neurofeedback may be a promising approach.

1.1. Neurofeedback

Neurofeedback works as a closed loop system that provides real-time information regarding the participant’s own brain activity and/or connectivity, which can be used to develop self-learning strategies to modulate these brain signals (Weiskopf, Mathiak, et al., 2004). It follows the principle of operant conditioning, a method of learning that occurs through reinforcing specific behaviour with rewards and punishments (Skinner, 1938). If the participant learns to control activity of the brain areas targeted through neurofeedback, this may ultimately lead to a measurable behavioural change that is related to the function of those areas (DeCharms et al., 2005; Haller, Birbaumer, & Veit, 2010; Hartwell et al., 2016).

The origins of neurofeedback are rooted in electroencephalography (EEG), which measures dynamic changes of electrical potentials over the participant’s scalp (Nowlis & Kamiya, 1970). This technique is portable and inexpensive, and provides estimates of brain activity at high temporal resolution. EEG neurofeedback has been widely used over the years to induce long-lasting behavioural changes, both in healthy volunteers and in patients (Gruzelier, 2014; Nelson, 2007). However, because of the low spatial resolution associated with this technique, it is very challenging to selectively target brain areas of interest. As such, the effects of EEG neurofeedback are often not specific (Rogala et al., 2016; Scharnowski & Weiskopf, 2015). Other neuroimaging techniques used for neurofeedback include magnetoencephalography (MEG) (Buch et al., 2012; Okazaki et al., 2015) and functional near-infrared spectroscopy (fNIRS) (Kober et al., 2014; Mihara et al., 2013). However, as also for EEG, their spatial resolution is relatively limited and they do not permit to target precise brain regions.

The field of neurofeedback has rapidly developed and delved into new avenues by the introduction of real-time functional magnetic resonance imaging (rt-fMRI) technology (Cox, Jesmanowicz, & Hyde, 1995). Accordingly, in the past years there has been a steady increase of studies focussing on rt-fMRI neurofeedback applications to induce behavioural changes (Sulzer et al., 2013). Rt-fMRI neurofeedback uses the blood-oxygenation level-dependent (BOLD) signal to present contingent feedback to the participant and to enable modulation of brain activity (Fig. 1). Various acquisition parameters are available, and chosen based on a trade-off between spatial and temporal resolution, and signal-to-noise ratio (Weiskopf, Scharnowski, et al., 2004). The analysis is performed almost immediately or with a delay of a few seconds depending on the available computational resources. With a much higher spatial resolution than EEG, fMRI allows for a refined delineation of both cortical and subcortical target regions. These properties can be valuable for neurofeedback applications (Stoeckel et al., 2014). Recent studies suggest that rt-fMRI is a mature technology to use in the context of neurofeedback training (for a review, see e.g., Ruiz, Buyukturkoglu, Rana, Birbaumer, & Sitaram, 2014; Weiskopf, 2012). As a result, doors are being opened to the application of rt-fMRI neurofeedback in ameliorating disrupted brain functions in stroke survivors.[…]

Fig. 1

Fig. 1. Real-time fMRI neurofeedback is a closed-loop system that can be used to voluntarily modulate brain-activity through the principle of operant conditioning. (A) The participants use self-generated or prior instructed strategies to attempt to change their brain activity. (B) fMRI data are acquired and (C) processed in real-time. Computer programs select the relevant signals and (D) return these to the participants after varied degrees of pre-processing to allow them to adjust their control strategies.

Continue —>  The potential of real-time fMRI neurofeedback for stroke rehabilitation: A systematic review – ScienceDirect

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