Abstract Classic work using the stop-signal task has shown that humans can use inhibitory control to cancel already initiated movements. Subsequent work revealed that inhibitory control can be proactively recruited in anticipation of a potential stop-signal, thereby increasing the likelihood of successful movement cancellation. However, the exact neurophysiological effects of proactive inhibitory control on the motor system are still unclear. On the basis of classic views of sensorimotor β-band activity, as well as recent findings demonstrating the burst-like nature of this signal, we recently proposed that proactive inhibitory control is implemented by influencing the rate of sensorimotor β-bursts during movement initiation. Here, we directly tested this hypothesis using scalp EEG recordings of β-band activity in 41 healthy human adults during a bimanual RT task. By comparing motor responses made in two different contexts—during blocks with or without stop-signals—we found that premovement β-burst rates over both contralateral and ipsilateral sensorimotor areas were increased in stop-signal blocks compared to pure-go blocks. Moreover, the degree of this burst rate difference indexed the behavioral implementation of proactive inhibition (i.e., the degree of anticipatory response slowing in the stop-signal blocks). Finally, exploratory analyses showed that these condition differences were explained by a significant increase in β bursting that was already present during baseline period before the movement initiation signal. Together, this suggests that the strategic deployment of proactive inhibitory motor control is implemented by upregulating the tonic inhibition of the motor system, signified by increased sensorimotor β-bursting both before and after signals to initiate a movement.
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Cortico-subcortical β burst dynamics underlying movement cancellation in humans
Dominant neuroanatomical models hold that humans regulate their movements via loop-like cortico-subcortical networks, which include the subthalamic nucleus (STN), motor thalamus, and sensorimotor cortex (SMC). Inhibitory commands across these networks are purportedly sent via transient, burst-like signals in the β frequency (15–29 Hz). However, since human depth-recording studies are typically limited to one recording site, direct evidence for this proposition is hitherto lacking. Here, we present simultaneous multi-site recordings from SMC and either STN or motor thalamus in humans performing the stop-signal task. In line with their purported function as inhibitory signals, subcortical β-bursts were increased on successful stop-trials. STN bursts in particular were followed within 50 ms by increased β-bursting over SMC. Moreover, between-site comparisons (including in a patient with simultaneous recordings from SMC, thalamus, and STN) confirmed that β-bursts in STN temporally precede thalamic β-bursts. This highly unique set of recordings provides empirical evidence for the role of β-bursts in conveying inhibitory commands along long-proposed cortico-subcortical networks underlying movement regulation in humans.
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- Award ID(s):
- 1752355
- NSF-PAR ID:
- 10321104
- Date Published:
- Journal Name:
- eLife
- Volume:
- 10
- ISSN:
- 2050-084X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Introduction Bi-directional brain-computer interfaces (BD-BCI) to restore movement and sensation must achieve concurrent operation of recording and decoding of motor commands from the brain and stimulating the brain with somatosensory feedback. Methods A custom programmable direct cortical stimulator (DCS) capable of eliciting artificial sensorimotor response was integrated into an embedded BCI system to form a safe, independent, wireless, and battery powered testbed to explore BD-BCI concepts at a low cost. The BD-BCI stimulator output was tested in phantom brain tissue by assessing its ability to deliver electrical stimulation equivalent to an FDA-approved commercial electrical cortical stimulator. Subsequently, the stimulator was tested in an epilepsy patient with subcortical electrocorticographic (ECoG) implants covering the sensorimotor cortex to assess its ability to elicit equivalent responses as the FDA-approved counterpart. Additional safety features (impedance monitoring, artifact mitigation, and passive and active charge balancing mechanisms) were also implemeneted and tested in phantom brain tissue. Finally, concurrent operation with interleaved stimulation and BCI decoding was tested in a phantom brain as a proof-of-concept operation of BD-BCI system. Results The benchtop prototype BD-BCI stimulator's basic output features (current amplitude, pulse frequency, pulse width, train duration) were validated by demonstrating the output-equivalency to an FDA-approved commercial cortical electrical stimulator ( R 2 > 0.99). Charge-neutral stimulation was demonstrated with pulse-width modulation-based correction algorithm preventing steady state voltage deviation. Artifact mitigation achieved a 64.5% peak voltage reduction. Highly accurate impedance monitoring was achieved with R 2 > 0.99 between measured and actual impedance, which in-turn enabled accurate charge density monitoring. An online BCI decoding accuracy of 93.2% between instructional cues and decoded states was achieved while delivering interleaved stimulation. The brain stimulation mapping via ECoG grids in an epilepsy patient showed that the two stimulators elicit equivalent responses. Significance This study demonstrates clinical validation of a fully-programmable electrical stimulator, integrated into an embedded BCI system. This low-cost BD-BCI system is safe and readily applicable as a testbed for BD-BCI research. In particular, it provides an all-inclusive hardware platform that approximates the limitations in a near-future implantable BD-BCI. This successful benchtop/human validation of the programmable electrical stimulator in a BD-BCI system is a critical milestone toward fully-implantable BD-BCI systems.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7554/eLife.70270
