Journal
NATURE NEUROSCIENCE
Volume 18, Issue 8, Pages 1109-+Publisher
NATURE PUBLISHING GROUP
DOI: 10.1038/nn.4049
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Funding
- Japan Science and Technology Agency (PRESTO)
- Pew Charitable Trusts
- Alfred P. Sloan Foundation
- David & Lucile Packard Foundation
- Human Frontier Science Program
- McKnight Foundation
- US National Institutes of Health [R01 NS091010A]
- University of California San Diego Center for Brain Activity Mapping
- New York Stem Cell Foundation (NYSCF)
- Neuroplasticity of Aging Training Grant [AG000216]
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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.
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