title: Subtype-specific plasticity of inhibitory circuits in motor cortex during motor learning.
abstract: Motor skill learning induces long-lasting reorganization of dendritic spines, principal sites of excitatory synapses, in the motor cortex. However, mechanisms that regulate these excitatory synaptic changes remain poorly understood. Here, using in vivo two-photon imaging in awake mice, we found that learning-induced spine reorganization of layer (L) 2/3 excitatory neurons occurs in the distal branches of their apical dendrites in L1 but not in the perisomatic dendrites. This compartment-specific spine reorganization coincided with subtype-specific plasticity of local inhibitory circuits. Somatostatin-expressing inhibitory neurons (SOM-INs), which mainly inhibit distal dendrites of excitatory neurons, showed a decrease in axonal boutons immediately after the training began, whereas parvalbumin-expressing inhibitory neurons (PV-INs), which mainly inhibit perisomatic regions of excitatory neurons, exhibited a gradual increase in axonal boutons during training. Optogenetic enhancement and suppression of SOM-IN activity during training destabilized and hyperstabilized spines, respectively, and both manipulations impaired the learning of stereotyped movements. Our results identify SOM inhibition of distal dendrites as a key regulator of learning-related changes in excitatory synapses and the acquisition of motor skills.
authors.affiliation: 1] Neurobiology Section, University of California, San Diego, La Jolla, California, USA. [2] Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, California, USA. [3] Department of Neurosciences, University of California, San Diego, La Jolla, California, USA.
authors.forename: Simon X
authors.initials: SX
authors.lastname: Chen
authors.affiliation: 1] Neurobiology Section, University of California, San Diego, La Jolla, California, USA. [2] Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, California, USA. [3] Department of Neurosciences, University of California, San Diego, La Jolla, California, USA.
authors.forename: An Na
authors.initials: AN
authors.lastname: Kim
authors.affiliation: 1] Neurobiology Section, University of California, San Diego, La Jolla, California, USA. [2] Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, California, USA. [3] Department of Neurosciences, University of California, San Diego, La Jolla, California, USA.
authors.forename: Andrew J
authors.identifier: 0000000193511456
authors.initials: AJ
authors.lastname: Peters
authors.affiliation: 1] Neurobiology Section, University of California, San Diego, La Jolla, California, USA. [2] Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, California, USA. [3] Department of Neurosciences, University of California, San Diego, La Jolla, California, USA. [4] Japan Science and Technology Agency, PRESTO, University of California, San Diego, La Jolla, California, USA.
authors.forename: Takaki
authors.initials: T
authors.lastname: Komiyama
mesh_terms: D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D049229:Dendritic Spines / Q000502:physiology*; D059330:GABAergic Neurons / Q000502:physiology*; D047569:Laser Scanning Cytometry; D007858:Learning / Q000502:physiology*; D051379:Mice; D008810:Mice, Inbred C57BL; D009043:Motor Activity / Q000502:physiology*; D009044:Motor Cortex / Q000502:physiology*; D009433:Neural Inhibition / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D062308:Optogenetics; D013004:Somatostatin / Q000378:metabolism*
chemical_list: D013004:Somatostatin