title: Optogenetically induced spatiotemporal gamma oscillations and neuronal spiking activity in primate motor cortex.
abstract: Transient gamma-band (40-80 Hz) spatiotemporal patterns are hypothesized to play important roles in cortical function. Here we report the direct observation of gamma oscillations as spatiotemporal waves induced by targeted optogenetic stimulation, recorded by intracortical multichannel extracellular techniques in macaque monkeys during their awake resting states. Microelectrode arrays integrating an optical fiber at their center were chronically implanted in primary motor (M1) and ventral premotor (PMv) cortices of two subjects. Targeted brain tissue was transduced with the red-shifted opsin C1V1(T/T). Constant (1-s square pulses) and ramp stimulation induced narrowband gamma oscillations during awake resting states. Recordings across 95 microelectrodes (4 × 4-mm array) enabled us to track the transient gamma spatiotemporal patterns manifested, e.g., as concentric expanding and spiral waves. Gamma oscillations were induced well beyond the light stimulation volume, via network interactions at distal electrode sites, depending on optical power. Despite stimulation-related modulation in spiking rates, neuronal spiking remained highly asynchronous during induced gamma oscillations. In one subject we examined stimulation effects during preparation and execution of a motor task and observed that movement execution largely attenuated optically induced gamma oscillations. Our findings demonstrate that, beyond previously reported induced gamma activity under periodic drive, a prolonged constant stimulus above a certain threshold may carry primate motor cortex network dynamics into gamma oscillations, likely via a Hopf bifurcation. More broadly, the experimental capability in combining microelectrode array recordings and optogenetic stimulation provides an important approach for probing spatiotemporal dynamics in primate cortical networks during various physiological and behavioral conditions.
authors.affiliation: School of Engineering, Brown University, Providence, Rhode Island; Department of Chemistry, Brown University, Providence, Rhode Island;
authors.forename: Yao
authors.initials: Y
authors.lastname: Lu
authors.affiliation: Department of Neuroscience, Brown University, Providence, Rhode Island; Institute for Brain Science, Brown University, Providence, Rhode Island; Center for Neurorestoration and Neurotechnology, Department of Veterans Affairs Medical Center, Providence, Rhode Island; and.
authors.forename: Wilson
authors.initials: W
authors.lastname: Truccolo
authors.affiliation: Department of Neuroscience, Brown University, Providence, Rhode Island;
authors.forename: Fabien B
authors.initials: FB
authors.lastname: Wagner
authors.affiliation: Department of Neuroscience, Brown University, Providence, Rhode Island; Institute for Brain Science, Brown University, Providence, Rhode Island;
authors.forename: Carlos E
authors.initials: CE
authors.lastname: Vargas-Irwin
authors.affiliation: School of Engineering, Brown University, Providence, Rhode Island;
authors.forename: Ilker
authors.initials: I
authors.lastname: Ozden
authors.affiliation: Department of Neuroscience, Brown University, Providence, Rhode Island; Institute for Brain Science, Brown University, Providence, Rhode Island;
authors.forename: Jonas B
authors.initials: JB
authors.lastname: Zimmermann
authors.affiliation: School of Engineering, Brown University, Providence, Rhode Island;
authors.forename: Travis
authors.initials: T
authors.lastname: May
authors.affiliation: School of Engineering, Brown University, Providence, Rhode Island;
authors.forename: Naubahar S
authors.initials: NS
authors.lastname: Agha
authors.affiliation: McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts.
authors.forename: Jing
authors.initials: J
authors.lastname: Wang
authors.affiliation: School of Engineering, Brown University, Providence, Rhode Island; Institute for Brain Science, Brown University, Providence, Rhode Island; arto_nurmikko@brown.edu.
authors.forename: Arto V
authors.initials: AV
authors.lastname: Nurmikko
mesh_terms: D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D001703:Biophysics; D005583:Fourier Analysis; D065818:Gamma Rhythm / Q000502:physiology*; D008164:Luminescent Proteins; D008253:Macaca mulatta; D008297:Male; D009044:Motor Cortex / Q000166:cytology* / Q000502:physiology*; D009068:Movement; D053580:Muscle Strength / Q000502:physiology; D009474:Neurons / Q000502:physiology*; D062308:Optogenetics; D010775:Photic Stimulation; D012372:ROC Curve; D014161:Transduction, Genetic; D014851:Wakefulness
chemical_list: D008164:Luminescent Proteins
keywords: collective dynamics; cortical waves; gamma oscillations; neocortex