Dataset Information

Structural dynamics and stability of corticocortical and thalamocortical axon terminals during motor learning.

ABSTRACT: Synaptic plasticity is the cellular basis of learning and memory. When animals learn a novel motor skill, synaptic modifications are induced in the primary motor cortex (M1), and new postsynaptic dendritic spines relevant to motor memory are formed in the early stage of learning. However, it is poorly understood how presynaptic axonal boutons are formed, eliminated, and maintained during motor learning, and whether long-range corticocortical and thalamocortical axonal boutons show distinct structural changes during learning. In this study, we conducted two-photon imaging of presynaptic boutons of long-range axons in layer 1 (L1) of the mouse M1 during the 7-day learning of an accelerating rotarod task. The training-period-averaged rate of formation of boutons on axons projecting from the secondary motor cortical area increased, while the average rate of elimination of those from the motor thalamus (thalamic boutons) decreased. In particular, the elimination rate of thalamic boutons during days 4-7 was lower than that in untrained mice, and the fraction of pre-existing thalamic boutons that survived until day 7 was higher than that in untrained mice. Our results suggest that the late stabilization of thalamic boutons in M1 contributes to motor skill learning.

SUBMITTER: Hasegawa R

PROVIDER: S-EPMC7304593 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Structural dynamics and stability of corticocortical and thalamocortical axon terminals during motor learning.

Hasegawa Ryota R Ebina Teppei T Tanaka Yasuhiro R YR Kobayashi Kenta K Matsuzaki Masanori M

PloS one 20200619 6

Synaptic plasticity is the cellular basis of learning and memory. When animals learn a novel motor skill, synaptic modifications are induced in the primary motor cortex (M1), and new postsynaptic dendritic spines relevant to motor memory are formed in the early stage of learning. However, it is poorly understood how presynaptic axonal boutons are formed, eliminated, and maintained during motor learning, and whether long-range corticocortical and thalamocortical axonal boutons show distinct struc ...[more]

PMID: 32559228

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Project description:Unified visual perception relies on the integration of bottom-up and top-down inputs in the primary visual cortex (V1), with top-down inputs known to provide behavior-related modulation on visual processing. However, the organization of top-down inputs in V1 remains unclear. Here, using optogenetics-assisted circuit mapping, we characterized how multiple top-down inputs from higher-order cortical and thalamic areas engage excitatory and inhibitory neurons in V1. Systematic layer- and cell-type-specific profiling of the innervation properties of top-down inputs ultimately revealed that each top-down input employs a unique laminar profile when innervating V1. These profiles partially overlap in superficial layers, bypass layer 4 (L4), and clearly segregate upon reaching deep layers. Specifically, inputs from the medial secondary visual cortex (V2M) and anterior cingulate cortex (ACA) preferentially activate L6 neurons, while inputs from the ventrolateral orbitofrontal cortex (ORBvl) and lateral posterior thalamic nucleus (LP) activate L5 neurons. Having defined the inputs, we conducted independent optogenetic activation studies and discovered that ORBvl and LP inputs selectively activate two types of pyramidal neurons (Pyrs) in L5: Pyr <-- ORBvl and Pyr <-- LP neurons, each with specific electrophysiological properties and gene expression profiles. Retrograde mapping subsequently revealed that Pyr <-- ORBvl neurons preferentially innervate subcortical areas and Pyr <-- LP neurons innervate cortical areas, indicating parallel processing of ORBvl and LP inputs in Pyr-type-specific subnetworks. Further, we found mutual inhibition between these two subnetworks, as LP inputs indirectly inhibit Pyr <-- ORBvl neurons and ORBvl inputs inhibit Pyr <-- LP neurons through local inhibitory neurons. Our study thus deepens understanding of the neuronal mechanisms involved in top-down modulation of visual processing by providing a valuable resource characterizing the layer- and cell-type-specific organization of top-down inputs in V1 and by revealing that L5 Pyr-type-specific subnetworks engage in parallel processing of corticocortical and thalamocortical top-down inputs.

Dataset Information

Structural dynamics and stability of corticocortical and thalamocortical axon terminals during motor learning.

Publications

Structural dynamics and stability of corticocortical and thalamocortical axon terminals during motor learning.

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