Movement-Related Sensorimotor High-Gamma Activity Mainly Represents Somatosensory Feedback

Abstract

Somatosensation plays pivotal roles in the everyday motor control of humans. During active movement, there exists a prominent high-gamma (HG >50 Hz) power increase in the primary somatosensory cortex (S1), and this provides an important feature in relation to the decoding of movement in a brain-machine interface (BMI). However, one concern of BMI researchers is the inflation of the decoding performance due to the activation of somatosensory feedback, which is not elicited in patients who have lost their sensorimotor function. In fact, it is unclear as to how much the HG component activated in S1 contributes to the overall sensorimotor HG power during voluntary movement. With regard to other functional roles of HG in S1, recent findings have reported that these HG power levels increase before the onset of actual movement, which implies neural activation for top-down movement preparation or sensorimotor interaction, i.e., an efference copy. These results are promising for BMI applications but remain inconclusive. Here, we found using electrocorticography (ECoG) from eight patients that HG activation in S1 is stronger and more informative than it is in the primary motor cortex (M1) regardless of the type of movement. We also demonstrate by means of electromyography (EMG) that the onset timing of the HG power in S1 is later (49 ms) than that of the actual movement. Interestingly, we show that the HG power fluctuations in S1 are closely related to subtle muscle contractions, even during the pre-movement period. These results suggest the following: (1) movement-related HG activity in S1 strongly affects the overall sensorimotor HG power, and (2) HG activity in S1 during voluntary movement mainly represents cortical neural processing for somatosensory feedback.

Modulation of gamma spectral amplitude and connectivity during reaching predicts peak velocity and movement duration

“…The occurrence of gamma synchronization during the planning phase has been reported in previous studies (Donner et al, 2009;Gaetz et al, 2013;Gunduz et al, 2016;Ryun et al, 2017) and supports the idea that gamma ERS might be associated with top-down mechanisms engaged for movement preparation and, thus, with the creation of an efferent copy of the upcoming movement. Indeed, our task instructions (that is, to perform fast, uncorrected, out-and backmovements to targets appearing in an unpredictable order) mostly engaged feedforward specification of a force-scaling factor according to movement extent (Ghez and Gordon, 1987;Gordon et al, 1994bGordon et al, , 1994a.…”

Characterization of Hand Clenching in Human Sensorimotor Cortex Using High-, and Ultra-High Frequency Band Modulations of Electrocorticogram

“…However, the existence of early-ERS in HFB posterior to the central sulcus of P2 can be viewed as evidence of S1 activation in top-down movement preparation. There is still controversy as to whether pre-movement activations of S1 truthfully represent the top-down efference copy or merely reflect the somatosensory feedback of subtle muscle contractions before movement onset (Ryun et al, 2017 ).…”

Power Modulations of ECoG Alpha/Beta and Gamma Bands Correlate With Time-Derivative of Force During Hand Grasp

“…In summary, there were modest differences between ECoG channels anterior and posterior to the central sulcus, and the differences changed to some extent depending on the phase of the grasp. In a recent study (Ryun et al, 2017a), it was also discovered that HG activity in S1 was more dominant than in M1 during active, voluntary movement. Others have also confirmed that humans' sensory information is present in M1 recordings, in addition to motor responses in S1 (Schieber and Hibbard, 1993;Sanes et al, 1995;Schroeder et al, 2017).…”