Thalamocortical Axonal Activity in Motor Cortex Exhibits Layer-Specific Dynamics during Motor Learning
Open accessAbstract
The thalamus is the hub through which neural signals are transmitted from the basal ganglia and cerebellum to the neocortex. However, thalamocortical axonal activity during motor learning remains largely undescribed. We conducted two-photon calcium imaging of thalamocortical axonal activity in the motor cortex of mice learning a self-initiated lever-pull task. Layer 1 (L1) axons came to exhibit activity at lever-pull initiation and termination, while layer 3 (L3) axons did so at lever-pull initiation. L1 population activity had a sequence structure related to both lever-pull duration and reproducibility. Stimulation of the substantia nigra pars reticulata activated more L1 than L3 axons, whereas deep cerebellar nuclei (DCN) stimulation did the opposite. Lesions to either the dorsal striatum or the DCN impaired motor learning and disrupted temporal dynamics in both layers. Thus, layer-specific thalamocortical signals evolve with the progression of learning, which requires both the basal ganglia and cerebellar activities.
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Optogenetic stimulation of thalamic cell bodies with lever pulling might improve thalamic activity by compensating dispersed inputs from basal ganglia and cerebellum that are crucial for motor learning.
“Optogenetic stimulation of thalamic cell bodies with lever pulling might improve thalamic activity by compensating dispersed inputs from basal ganglia and cerebellum that are crucial for motor learning (Bosch‐Bouju et al., 2013 ; Tanaka et al., 2018 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as Tanaka et al., 2018
Inputs from basal ganglia and cerebellum mediating motor thalamus are crucial for motor learning.
“Inputs from basal ganglia and cerebellum mediating motor thalamus are crucial for motor learning (Bosch‐Bouju et al., 2013 ; Tanaka et al., 2018 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as Tanaka et al., 2018
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Short latency cerebellar modulation of the basal ganglia
Chen, C. H., Fremont, R., Arteaga-Bracho, E. E., & Khodakhah, K. (2014) · Nature Neuroscience · doi:10.1038/nn.3868 · Cited by 286 · see citing works
The thalamus as a monitor of motor outputs.
Guillery, R. W., & Sherman, S. M. (2002) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1171 · Cited by 128 · see citing works
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Neocortical Layer 1: an elegant solution to top-down and bottom-up integration
Schuman, B., Dellal, S., Prönneke, A., Machold, R., & Rudy, B. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-100520-012117 · Cited by 148 · see citing works
Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity
Kato, D., Wake, H., Lee, P. R., Tachibana, Y., Ono, R., Sugio, S., Tsuji, Y., Tanaka, Y. H., Tanaka, Y. R., Masamizu, Y., et al. (2020) · Glia · doi:10.1002/glia.23713 · Cited by 114 · see citing works
“Optogenetic stimulation of thalamic cell bodies with lever pulling might improve thalamic activity by compensating dispersed inputs from basal ganglia and cerebellum that are crucial for motor learning (Bosch-Bouju et al., 2013; Tanaka et al., 2018).”
BackgroundSelf-citationGovek, K. W., Chen, S., Sgourdou, P., Yao, Y., Woodhouse, S., Chen, T., Fuccillo, M. V., Epstein, D. J., & Camara, P. G. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111768 · Cited by 28 · see citing works
- Authors
- Tanaka, Y. H., Tanaka, Y. R., Kondo, M., Terada, S.-I., Kawaguchi, Y., & Matsuzaki, M.
- Affiliations
- National Institute for Basic Biology (JP)
- The Graduate University for Advanced Studies, SOKENDAI (JP)
- Corresponding author
- Matsuzaki, Masanori
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2018-10
- Volume
- 100
- Issue
- 1
- Pages
- 244-258.e12
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2889231692
- Cited by
- 77
- References
- 2
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 6 · 2023: 7 · 2022: 14 · 2021: 16 · 2020: 12 · 2019: 7
- FWCI
- 5.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- MEXT (22115005, 15H01455, 17H05553, 17H06025, 17H06309, 17H06311, 16H01624, 18H04934, 23300148, 15H02350, 16K18370, 268449, 253960)
- AMED (JP18dm0207027, JP18dm0107150)
- Takeda Foundation
- Konica Minolta Science and Technology Foundation
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- thalamocortical connections, motor learning, motor cortex, cortical layers, layer 1, layer 3, substantia nigra pars reticulata, deep cerebellar nuclei, dorsal striatum, basal ganglia, cerebellum, two-photon calcium imaging
- MeSH terms
- Animals, Axons, Brain, Cerebral Cortex, Learning, Male, Mice, Inbred C57BL, Motor Activity, Motor Cortex, Thalamus, Mice
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