title: Distinct Functional Modules for Discrete and Rhythmic Forelimb Movements in the Mouse Motor Cortex.
abstract: Movements of animals are composed of two fundamental dynamics: discrete and rhythmic movements. Although the movements with distinct dynamics are thought to be differently processed in the CNS, it is unclear how they are represented in the cerebral cortex. Here, we investigated the cortical representation of movement dynamics by developing prolonged transcranial optogenetic stimulation (pTOS) using awake, channelrhodopsin-2 transgenic mice. We found two domains that induced discrete forelimb movements in the forward and backward directions, and these sandwiched a domain that generated rhythmic forelimb movements. The forward discrete movement had an intrinsic velocity profile and the rhythmic movement had an intrinsic oscillation frequency. Each of the forward discrete and rhythmic domains possessed intracortical synaptic connections within its own domain, independently projected to the spinal cord, and weakened the neuronal activity and movement induction of the other domain. pTOS-induced movements were also classified as ethologically relevant movements. Forepaw-to-mouth movement was mapped in a part of the forward discrete domain, while locomotion-like movement was in a part of the rhythmic domain. Interestingly, photostimulation of the rhythmic domain resulted in a nonrhythmic, continuous lever-pull movement when a lever was present. The motor cortex possesses functional modules for distinct movement dynamics, and these can adapt to environmental constraints for purposeful movements. Significance statement: Animal behavior has discrete and rhythmic components, such as reaching and locomotion. It is unclear how these movements with distinct dynamics are represented in the cerebral cortex. We investigated the dynamics of movements induced by long-duration transcranial photostimulation on the dorsal cortex of awake channelrhodopsin-2 transgenic mice. We found two domains causing forward and backward discrete forelimb movements and a domain for rhythmic forelimb movements. A domain for forward discrete movement and a domain for rhythmic movement mutually weakened neuronal activity and movement size. The photostimulation of the rhythmic domain also induced nonrhythmic, lever-pull movement, when the lever was present. Thus, the motor cortex has functional modules with distinct dynamics, and each module retains flexibility for adaptation to different environments.
authors.affiliation: Division of Brain Circuits, National Institute for Basic Biology, Myodaiji, Okazaki 444-8585, Japan, Department of Basic Biology, SOKENDAI, The Graduate University for Advanced Studies, Okazaki 444-8585, Japan.
authors.forename: Riichiro
authors.identifier: http://orcid.org/0000-0002-8719-4498
authors.initials: R
authors.lastname: Hira
authors.affiliation: Division of Brain Circuits, National Institute for Basic Biology, Myodaiji, Okazaki 444-8585, Japan, Laboratory of Cell Recognition and Pattern Formation, Graduate School of Biostudies, Kyoto University, Kyoto 606-8501, Japan, and.
authors.forename: Shin-Ichiro
authors.initials: S
authors.lastname: Terada
authors.affiliation: Division of Brain Circuits, National Institute for Basic Biology, Myodaiji, Okazaki 444-8585, Japan, Physical and Health Education, Graduate School of Education, the University of Tokyo, Tokyo 113-0033, Japan.
authors.forename: Masashi
authors.initials: M
authors.lastname: Kondo
authors.affiliation: Division of Brain Circuits, National Institute for Basic Biology, Myodaiji, Okazaki 444-8585, Japan, Department of Basic Biology, SOKENDAI, The Graduate University for Advanced Studies, Okazaki 444-8585, Japan, mzakim@nibb.ac.jp.
authors.forename: Masanori
authors.initials: M
authors.lastname: Matsuzaki
mesh_terms: D000818:Animals; D000075402:Channelrhodopsins; D003216:Conditioning, Operant / Q000502:physiology; D004525:Efferent Pathways / Q000502:physiology*; D005260:Female; D005552:Forelimb / Q000294:innervation* / Q000502:physiology*; D008297:Male; D051379:Mice; D008822:Mice, Transgenic; D009044:Motor Cortex / Q000502:physiology*; D009068:Movement / Q000502:physiology*; D062308:Optogenetics; D010775:Photic Stimulation; D012399:Rotation; D013116:Spinal Cord / Q000166:cytology / Q000502:physiology; D018800:Thy-1 Antigens / Q000235:genetics
chemical_list: D000075402:Channelrhodopsins; D018800:Thy-1 Antigens
keywords: channelrhodopsin; complex movement; motor cortex; mouse; photostimulation