Phase-Specific Microstimulation Differentially Modulates Beta Oscillations and Affects Behavior

• Published in: Cell reports (Cambridge) Vol. 30; no. 8; pp. 2555 - 2566.e3
• Main Authors: Peles, Oren, Werner-Reiss, Uri, Bergman, Hagai, Israel, Zvi, Vaadia, Eilon
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 25.02.2020; Elsevier
• Subjects: Action Potentials - physiology; Animals; Behavior, Animal - physiology; Beta oscillations; Beta Rhythm - physiology; brain-machine interface; Conditioning, Operant; Electric Stimulation; Female; local field potential; Macaca mulatta; microsimulation; motor cortex; non-human primates; operant conditioning; local field potential; motor cortex; operant conditioning; non-human primates; Beta oscillations; brain-machine interface; microsimulation
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2020.02.005

It is widely accepted that Beta-band oscillations play a role in sensorimotor behavior. To further explore this role, we developed a hybrid platform to combine neural operant conditioning and phase-specific intracortical microstimulation (ICMS). We trained monkeys, implanted with 96 electrode arrays in the motor cortex, to volitionally enhance local field potential (LFP) Beta-band (20–30 Hz) activity at selected sites using a brain-machine interface. We find that Beta oscillations of LFP and single-unit spiking activity increase dramatically with brain-machine interface training and that pre-movement Beta power is anti-correlated with task performance. We also find that phase-specific ICMS modulates the power and phase of oscillations, shifting local networks between oscillatory and non-oscillatory states. Furthermore, ICMS induces phase-dependent effects in animal reaction times and success rates. These findings contribute to unraveling the functional role of cortical oscillations and to the future development of clinical tools for ameliorating abnormal neuronal activities in brain disease. [Display omitted] •Through operant conditioning, subjects learn to volitionally control M1 Beta oscillations•Pre-movement LFP Beta power is anti-correlated with task performance•Phase-specific stimulation differentially modulates LFP and spiking temporal patterns•Stimulation differentially affects behavior when diverging from the standard regime Peles et al. show that motor cortex Beta oscillations can be differentially modulated by combined neural operant conditioning and phase-specific intracortical microstimulation. Successfully manipulating this frequency band paves the way to understanding its functional role and to development of clinical tools for treating brain diseases, including Parkinson’s and schizophrenia.