Dataset Information

Distributed cortical adaptation during learning of a brain-computer interface task.

ABSTRACT: The majority of subjects who attempt to learn control of a brain-computer interface (BCI) can do so with adequate training. Much like when one learns to type or ride a bicycle, BCI users report transitioning from a deliberate, cognitively focused mindset to near automatic control as training progresses. What are the neural correlates of this process of BCI skill acquisition? Seven subjects were implanted with electrocorticography (ECoG) electrodes and had multiple opportunities to practice a 1D BCI task. As subjects became proficient, strong initial task-related activation was followed by lessening of activation in prefrontal cortex, premotor cortex, and posterior parietal cortex, areas that have previously been implicated in the cognitive phase of motor sequence learning and abstract task learning. These results demonstrate that, although the use of a BCI only requires modulation of a local population of neurons, a distributed network of cortical areas is involved in the acquisition of BCI proficiency.

SUBMITTER: Wander JD

PROVIDER: S-EPMC3696802 | biostudies-other | 2013 Jun

REPOSITORIES: biostudies-other

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Distributed cortical adaptation during learning of a brain-computer interface task.

Wander Jeremiah D JD Blakely Timothy T Miller Kai J KJ Weaver Kurt E KE Johnson Lise A LA Olson Jared D JD Fetz Eberhard E EE Rao Rajesh P N RP Ojemann Jeffrey G JG

Proceedings of the National Academy of Sciences of the United States of America 20130610 26

The majority of subjects who attempt to learn control of a brain-computer interface (BCI) can do so with adequate training. Much like when one learns to type or ride a bicycle, BCI users report transitioning from a deliberate, cognitively focused mindset to near automatic control as training progresses. What are the neural correlates of this process of BCI skill acquisition? Seven subjects were implanted with electrocorticography (ECoG) electrodes and had multiple opportunities to practice a 1D ...[more]

PMID: 23754426

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Project description:Brain-computer interfaces (BCIs) benefit greatly from performance feedback, but current systems lack automatic, task-independent feedback. Cortical responses elicited from user error have the potential to serve as state-based feedback to BCI decoders. To gain a better understanding of local error potentials, we investigate responsive cortical power underlying error-related potentials (ErrPs) from the human cortex during a one-dimensional center-out BCI task, tracking the topography of high-gamma (70-100 Hz) band power (HBP) specific to BCI error. We measured electrocorticography (ECoG) in three human subjects during dynamic, continuous control over BCI cursor velocity. Subjects used motor imagery and rest to move the cursor toward and subsequently dwell within a target region. We then identified and labeled epochs where the BCI decoder incorrectly moved the cursor in the direction opposite of the subject's expectations (i.e., BCI error). We found increased HBP in various cortical areas 100-500 ms following BCI error with respect to epochs of correct, intended control. Significant responses were noted in primary somatosensory, motor, premotor, and parietal areas and generally regardless of whether the subject was using motor imagery or rest to move the cursor toward the target. Parts of somatosensory, temporal, and parietal areas exclusively had increased HBP when subjects were using motor imagery. In contrast, only part of the parietal cortex near the angular gyrus exclusively had an increase in HBP during rest. This investigation is, to our knowledge, the first to explore cortical fields changes in the context of continuous control in ECoG BCI. We present topographical changes in HBP characteristic specific to the generation of error. By focusing on continuous control, instead of on discrete control for simple selection, we investigate a more naturalistic setting and provide high ecological validity for characterizing error potentials. Such potentials could be considered as design elements for co-adaptive BCIs in the future as task-independent feedback to the decoder, allowing for more robust and individualized BCIs.

Project description:ObjectiveMotor imagery-based brain-computer interfaces (BCIs) use an individual's ability to volitionally modulate localized brain activity, often as a therapy for motor dysfunction or to probe causal relations between brain activity and behavior. However, many individuals cannot learn to successfully modulate their brain activity, greatly limiting the efficacy of BCI for therapy and for basic scientific inquiry. Formal experiments designed to probe the nature of BCI learning have offered initial evidence that coherent activity across spatially distributed and functionally diverse cognitive systems is a hallmark of individuals who can successfully learn to control the BCI. However, little is known about how these distributed networks interact through time to support learning.ApproachHere, we address this gap in knowledge by constructing and applying a multimodal network approach to decipher brain-behavior relations in motor imagery-based brain-computer interface learning using magnetoencephalography. Specifically, we employ a minimally constrained matrix decomposition method - non-negative matrix factorization - to simultaneously identify regularized, covarying subgraphs of functional connectivity, to assess their similarity to task performance, and to detect their time-varying expression.Main resultsWe find that learning is marked by diffuse brain-behavior relations: good learners displayed many subgraphs whose temporal expression tracked performance. Individuals also displayed marked variation in the spatial properties of subgraphs such as the connectivity between the frontal lobe and the rest of the brain, and in the temporal properties of subgraphs such as the stage of learning at which they reached maximum expression. From these observations, we posit a conceptual model in which certain subgraphs support learning by modulating brain activity in sensors near regions important for sustaining attention. To test this model, we use tools that stipulate regional dynamics on a networked system (network control theory), and find that good learners display a single subgraph whose temporal expression tracked performance and whose architecture supports easy modulation of sensors located near brain regions important for attention.SignificanceThe nature of our contribution to the neuroscience of BCI learning is therefore both computational and theoretical; we first use a minimally-constrained, individual specific method of identifying mesoscale structure in dynamic brain activity to show how global connectivity and interactions between distributed networks supports BCI learning, and then we use a formal network model of control to lend theoretical support to the hypothesis that these identified subgraphs are well suited to modulate attention.

Dataset Information

Distributed cortical adaptation during learning of a brain-computer interface task.

Publications

Distributed cortical adaptation during learning of a brain-computer interface task.

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