Subtype-specific plasticity of inhibitory circuits in motor cortex during motor learning

This study identifies opposite changes in two main subtypes of inhibitory neurons in the mouse motor cortex during motor learning. With learning, the number of synapses made by somatostatin-expressing inhibitory neurons (SOM-IN) onto the distal dendritic branches of pyramidal neurons decreased, wher...

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Published in:	Nature neuroscience Vol. 18; no. 8; pp. 1109 - 1115
Main Authors:	Chen, Simon X, Kim, An Na, Peters, Andrew J, Komiyama, Takaki
Format:	Journal Article
Language:	English
Published:	New York Nature Publishing Group US 01.08.2015 Nature Publishing Group
Subjects:	14/69 631/378/1595/2618 631/378/2632/1663 631/378/3920 64/60 Animal Genetics and Genomics Animals Behavior, Animal - physiology Behavioral Sciences Biological Techniques Biomedicine Dendritic Spines - physiology GABAergic Neurons - physiology Laser Scanning Cytometry Learning - physiology Mice Mice, Inbred C57BL Motor Activity - physiology Motor Cortex - physiology Motor learning Neural Inhibition - physiology Neural transmission Neurobiology Neuronal Plasticity - physiology Neurons Neuroplasticity Neurosciences Observations Optogenetics Psychological aspects Somatostatin - metabolism La Jolla California United States > US California
ISSN:	1097-6256, 1546-1726
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Abstract	This study identifies opposite changes in two main subtypes of inhibitory neurons in the mouse motor cortex during motor learning. With learning, the number of synapses made by somatostatin-expressing inhibitory neurons (SOM-IN) onto the distal dendritic branches of pyramidal neurons decreased, whereas the number of perisomatic contacts made by parvalbumin-positive cells increased. The authors also found that optogenetic disruption of SOM-IN activity resulted in impairment of learning-related dendritic spine reorganization and motor learning. 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.
AbstractList	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. This study identifies opposite changes in two main subtypes of inhibitory neurons in the mouse motor cortex during motor learning. With learning, the number of synapses made by somatostatin-expressing inhibitory neurons (SOM-IN) onto the distal dendritic branches of pyramidal neurons decreased, whereas the number of perisomatic contacts made by parvalbumin-positive cells increased. The authors also found that optogenetic disruption of SOM-IN activity resulted in impairment of learning-related dendritic spine reorganization and motor learning. 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. Motor skill learning induces long-lasting reorganization of dendritic spines, major 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 L2/3 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) that mainly inhibit distal dendrites of excitatory neurons showed a decrease in axonal boutons immediately after the training begins, whereas parvalbumin-expressing inhibitory neurons (PV-INs) that mainly inhibit perisomatic regions of excitatory neurons exhibited a gradual increase in the axonal boutons during training. Optogenetic enhancement and suppression of SOM-IN activity during training destabilized and hyper-stabilized 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.
Audience	Academic
Author	Chen, Simon X Komiyama, Takaki Kim, An Na Peters, Andrew J
AuthorAffiliation	2 JST, PRESTO, University of California, San Diego, La Jolla, CA 92093, USA 1 Neurobiology Section, Center for Neural Circuits and Behavior, and Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093, USA
AuthorAffiliation_xml	– name: 2 JST, PRESTO, University of California, San Diego, La Jolla, CA 92093, USA – name: 1 Neurobiology Section, Center for Neural Circuits and Behavior, and Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093, USA
Author_xml	– sequence: 1 givenname: Simon X surname: Chen fullname: Chen, Simon X organization: Neurobiology Section, University of California, San Diego, Center for Neural Circuits and Behavior, University of California, San Diego, Department of Neurosciences, University of California, San Diego – sequence: 2 givenname: An Na surname: Kim fullname: Kim, An Na organization: Neurobiology Section, University of California, San Diego, Center for Neural Circuits and Behavior, University of California, San Diego, Department of Neurosciences, University of California, San Diego – sequence: 3 givenname: Andrew J orcidid: 0000-0001-9351-1456 surname: Peters fullname: Peters, Andrew J organization: Neurobiology Section, University of California, San Diego, Center for Neural Circuits and Behavior, University of California, San Diego, Department of Neurosciences, University of California, San Diego – sequence: 4 givenname: Takaki surname: Komiyama fullname: Komiyama, Takaki email: tkomiyama@ucsd.edu organization: Neurobiology Section, University of California, San Diego, Center for Neural Circuits and Behavior, University of California, San Diego, Department of Neurosciences, University of California, San Diego, Japan Science and Technology Agency, PRESTO, University of California, San Diego
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26098758$$D View this record in MEDLINE/PubMed
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Snippet	This study identifies opposite changes in two main subtypes of inhibitory neurons in the mouse motor cortex during motor learning. With learning, the number of... Motor skill learning induces long-lasting reorganization of dendritic spines, principal sites of excitatory synapses, in the motor cortex. However, mechanisms... Motor skill learning induces long-lasting reorganization of dendritic spines, major sites of excitatory synapses, in the motor cortex. However, mechanisms that...
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Title	Subtype-specific plasticity of inhibitory circuits in motor cortex during motor learning
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