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Motor-related brain activity during action observation: a neural substrate for electrocorticographic brain-computer interfaces after spinal cord injury.

ABSTRACT: After spinal cord injury (SCI), motor commands from the brain are unable to reach peripheral nerves and muscles below the level of the lesion. Action observation (AO), in which a person observes someone else performing an action, has been used to augment traditional rehabilitation paradigms. Similarly, AO can be used to derive the relationship between brain activity and movement kinematics for a motor-based brain-computer interface (BCI) even when the user cannot generate overt movements. BCIs use brain signals to control external devices to replace functions that have been lost due to SCI or other motor impairment. Previous studies have reported congruent motor cortical activity during observed and overt movements using magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI). Recent single-unit studies using intracortical microelectrodes also demonstrated that a large number of motor cortical neurons had similar firing rate patterns between overt and observed movements. Given the increasing interest in electrocorticography (ECoG)-based BCIs, our goal was to identify whether action observation-related cortical activity could be recorded using ECoG during grasping tasks. Specifically, we aimed to identify congruent neural activity during observed and executed movements in both the sensorimotor rhythm (10-40 Hz) and the high-gamma band (65-115 Hz) which contains significant movement-related information. We observed significant motor-related high-gamma band activity during AO in both able-bodied individuals and one participant with a complete C4 SCI. Furthermore, in able-bodied participants, both the low and high frequency bands demonstrated congruent activity between action execution and observation. Our results suggest that AO could be an effective and critical procedure for deriving the mapping from ECoG signals to intended movement for an ECoG-based BCI system for individuals with paralysis.

SUBMITTER: Collinger JL

PROVIDER: S-EPMC3928793 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Motor-related brain activity during action observation: a neural substrate for electrocorticographic brain-computer interfaces after spinal cord injury.

Collinger Jennifer L JL Vinjamuri Ramana R Degenhart Alan D AD Weber Douglas J DJ Sudre Gustavo P GP Boninger Michael L ML Tyler-Kabara Elizabeth C EC Wang Wei W

Frontiers in integrative neuroscience 20140219

After spinal cord injury (SCI), motor commands from the brain are unable to reach peripheral nerves and muscles below the level of the lesion. Action observation (AO), in which a person observes someone else performing an action, has been used to augment traditional rehabilitation paradigms. Similarly, AO can be used to derive the relationship between brain activity and movement kinematics for a motor-based brain-computer interface (BCI) even when the user cannot generate overt movements. BCIs u ...[more]

PMID: 24600359

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Project description:OBJECTIVE:Brain-computer interface (BCI) technology aims to provide individuals with paralysis a means to restore function. Electrocorticography (ECoG) uses disc electrodes placed on either the surface of the dura or the cortex to record field potential activity. ECoG has been proposed as a viable neural recording modality for BCI systems, potentially providing stable, long-term recordings of cortical activity with high spatial and temporal resolution. Previously we have demonstrated that a subject with spinal cord injury (SCI) could control an ECoG-based BCI system with up to three degrees of freedom (Wang et al 2013 PLoS One). Here, we expand upon these findings by including brain-control results from two additional subjects with upper-limb paralysis due to amyotrophic lateral sclerosis and brachial plexus injury, and investigate the potential of motor and somatosensory cortical areas to enable BCI control. APPROACH:Individuals were implanted with high-density ECoG electrode grids over sensorimotor cortical areas for less than 30 d. Subjects were trained to control a BCI by employing a somatotopic control strategy where high-gamma activity from attempted arm and hand movements drove the velocity of a cursor. MAIN RESULTS:Participants were capable of generating robust cortical modulation that was differentiable across attempted arm and hand movements of their paralyzed limb. Furthermore, all subjects were capable of voluntarily modulating this activity to control movement of a computer cursor with up to three degrees of freedom using the somatotopic control strategy. Additionally, for those subjects with electrode coverage of somatosensory cortex, we found that somatosensory cortex was capable of supporting ECoG-based BCI control. SIGNIFICANCE:These results demonstrate the feasibility of ECoG-based BCI systems for individuals with paralysis as well as highlight some of the key challenges that must be overcome before such systems are translated to the clinical realm. ClinicalTrials.gov Identifier: NCT01393444.

Project description:Brain-computer interfaces (BCIs) can provide sensory feedback of ongoing brain oscillations, enabling stroke survivors to modulate their sensorimotor rhythms purposefully. A number of recent clinical studies indicate that repeated use of such BCIs might trigger neurological recovery and hence improvement in motor function. Here, we provide a first meta-analysis evaluating the clinical effectiveness of BCI-based post-stroke motor rehabilitation. Trials were identified using MEDLINE, CENTRAL, PEDro and by inspection of references in several review articles. We selected randomized controlled trials that used BCIs for post-stroke motor rehabilitation and provided motor impairment scores before and after the intervention. A random-effects inverse variance method was used to calculate the summary effect size. We initially identified 524 articles and, after removing duplicates, we screened titles and abstracts of 473 articles. We found 26 articles corresponding to BCI clinical trials, of these, there were nine studies that involved a total of 235 post-stroke survivors that fulfilled the inclusion criterion (randomized controlled trials that examined motor performance as an outcome measure) for the meta-analysis. Motor improvements, mostly quantified by the upper limb Fugl-Meyer Assessment (FMA-UE), exceeded the minimal clinically important difference (MCID=5.25) in six BCI studies, while such improvement was reached only in three control groups. Overall, the BCI training was associated with a standardized mean difference of 0.79 (95% CI: 0.37 to 1.20) in FMA-UE compared to control conditions, which is in the range of medium to large summary effect size. In addition, several studies indicated BCI-induced functional and structural neuroplasticity at a subclinical level. This suggests that BCI technology could be an effective intervention for post-stroke upper limb rehabilitation. However, more studies with larger sample size are required to increase the reliability of these results.

Project description:Motor imagery (MI) and action observation have proven to be efficacious adjuncts to traditional physiotherapy for enhancing motor recovery following stroke. Recently, researchers have used a combined approach called imagined imitation (II), where an individual watches a motor task being performed, while simultaneously imagining they are performing the movement. While neurofeedback (NFB) has been used extensively with MI to improve patients' ability to modulate sensorimotor activity and enhance motor recovery, the effectiveness of using NFB with II to modulate brain activity is unknown. This project tested the ability of participants to modulate sensorimotor activity during electroencephalography-based II-NFB of a complex, multi-part unilateral handshake, and whether this ability transferred to a subsequent bout of MI. Moreover, given the goal of translating findings from NFB research into practical applications, such as rehabilitation, the II-NFB system was designed with several user interface and user experience features, in an attempt to both drive user engagement and match the level of challenge to the abilities of the subjects. In particular, at easy difficulty levels the II-NFB system incentivized contralateral sensorimotor up-regulation (via event related desynchronization of the mu rhythm), while at higher difficulty levels the II-NFB system incentivized sensorimotor lateralization (i.e., both contralateral up-regulation and ipsilateral down-regulation). Thirty-two subjects, receiving real or sham NFB attended four sessions where they engaged in II-NFB training and subsequent MI. Results showed the NFB group demonstrated more bilateral sensorimotor activity during sessions 2-4 during II-NFB and subsequent MI, indicating mixed success for the implementation of this particular II-NFB system. Here we discuss our findings in the context of the design features included in the II-NFB system, highlighting limitations that should be considered in future designs.

Dataset Information

Motor-related brain activity during action observation: a neural substrate for electrocorticographic brain-computer interfaces after spinal cord injury.

Publications

Motor-related brain activity during action observation: a neural substrate for electrocorticographic brain-computer interfaces after spinal cord injury.

Similar Datasets

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