Cortico-Cortical Interactions during Acquisition and Use of a Neuroprosthetic Skill.

Jeremiah D Wander,Jeffrey G Ojemann,Lise A Johnson,Eberhard E Fetz,Rajesh P N Rao,Devapratim Sarma,Felix Darvas,Olaf Sporns

doi:10.1371/journal.pcbi.1004931

Jeremiah D Wander, Jeffrey G Ojemann + Show 6 more

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https://doi.org/10.1371/journal.pcbi.1004931

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Abstract

A motor cortex-based brain-computer interface (BCI) creates a novel real world output directly from cortical activity. Use of a BCI has been demonstrated to be a learned skill that involves recruitment of neural populations that are directly linked to BCI control as well as those that are not. The nature of interactions between these populations, however, remains largely unknown. Here, we employed a data-driven approach to assess the interaction between both local and remote cortical areas during the use of an electrocorticographic BCI, a method which allows direct sampling of cortical surface potentials. Comparing the area controlling the BCI with remote areas, we evaluated relationships between the amplitude envelopes of band limited powers as well as non-linear phase-phase interactions. We found amplitude-amplitude interactions in the high gamma (HG, 70–150 Hz) range that were primarily located in the posterior portion of the frontal lobe, near the controlling site, and non-linear phase-phase interactions involving multiple frequencies (cross-frequency coupling between 8–11 Hz and 70–90 Hz) taking place over larger cortical distances. Further, strength of the amplitude-amplitude interactions decreased with time, whereas the phase-phase interactions did not. These findings suggest multiple modes of cortical communication taking place during BCI use that are specialized for function and depend on interaction distance.

Highlights

Direct communication between brain and machine provides a powerful platform for both the development of clinical therapies and scientific inquiry
Other than a recent study demonstrating the need for corticostriatal interaction during the brain-computer interface (BCI) learning process in a rodent model [12], we have little understanding of the networks involved in acquisition of the neuroprosthetic skill
When performing short time windowed covariance (STWC) interactions on response-locked trials, we identified 31 total electrodes, from a total of 9 of the 10 subjects that exhibited significant STWC interactions with the controlling electrode (CTL) electrode (p < 0.05; see randomization methods for detail)

Summary

Introduction

Direct communication between brain and machine provides a powerful platform for both the development of clinical therapies and scientific inquiry. By providing the brain with a completely novel output pathway, experimentalists have an opportunity to observe the ways in which the brain responds to and develops control over this new output mechanism [1]. A number of studies have demonstrated that the use of a brain-computer interface (BCI) is a learned skill [2,3,4,5,6], and that the brain can learn this skill more effectively when the transformation that maps neural activity to BCI control is consistent [7]. The mechanisms underlying learning of BCI control have many similarities to those for learning motor control [10]. There have been no systematic studies of cortico-cortical interaction during BCI use. Other than a recent study demonstrating the need for corticostriatal interaction during the BCI learning process in a rodent model [12], we have little understanding of the networks involved in acquisition of the neuroprosthetic skill

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