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Roles of centromedian parafascicular nuclei of thalamus and cholinergic interneurons in the dorsal striatum in associative learning of environmental events

  • Translational Neurosciences - Review Article
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Abstract

The thalamus provides a massive input to the striatum, but despite accumulating evidence, the functions of this system remain unclear. It is known, however, that the centromedian (CM) and parafascicular (Pf) nuclei of the thalamus can strongly influence particular striatal neuron subtypes, notably including the cholinergic interneurons of the striatum (CINs), key regulators of striatal function. Here, we highlight the thalamostriatal system through the CM–Pf to striatal CINs. We consider how, by virtue of the direct synaptic connections of the CM and PF, their neural activity contributes to the activity of CINs and striatal projection neurons (SPNs). CM–Pf neurons are strongly activated at sudden changes in behavioral context, such as switches in action–outcome contingency or sequence of behavioral requirements, suggesting that their activity may represent change of context operationalized as associability. Striatal CINs, on the other hand, acquire and loose responses to external events associated with particular contexts. In light of this physiological evidence, we propose a hypothesis of the CM–Pf–CINs system, suggesting that it augments associative learning by generating an associability signal and promotes reinforcement learning guided by reward prediction error signals from dopamine-containing neurons. We discuss neuronal circuit and synaptic organizations based on in vivo/in vitro studies that we suppose to underlie our hypothesis. Possible implications of CM–Pf–CINs dysfunction (or degeneration) in brain diseases are also discussed by focusing on Parkinson’s disease.

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Acknowledgements

We thank M. Haruno and Y. Sakai, Y. Kubota for critical reading and advice on the manuscript, R. Sakane, M. Funami and I. Kawashima for technical assistance. This study was supported by Grant-in-Aid for Scientific Research 23120010, 26290009, and 15K14320 to M.K., and for Young Scientists (B) 20700293 to Y.H., 24700425 to K.Y., by the Development of Biomarker Candidates for Social Behavior carried out under the Strategic Research Program for Brain Sciences from the Ministry of Education, Culture, Sports, Science and Technology of Japan (M.K.), and by National Institutes for Health grant R01 NS025529 to A.M.G.

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Authors and Affiliations

  1. Brain Science Institute, Tamagawa University, Machida, Tokyo, Japan

    Ko Yamanaka, Kazuki Enomoto & Minoru Kimura

  2. Department of Physiology, Kyoto Prefectural University of Medicine, Kyoto, Japan

    Ko Yamanaka, Yukiko Hori, Takafumi Minamimoto, Hiroshi Yamada, Naoyuki Matsumoto, Kazuki Enomoto & Minoru Kimura

  3. Department of Physiology, Faculty of Health and Sports Science, Juntendo University, Chiba, Japan

    Ko Yamanaka

  4. Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

    Yukiko Hori & Takafumi Minamimoto

  5. Division of Biomedical Science, Faculty of Medicine, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan

    Hiroshi Yamada

  6. Department of Food and Health Sciences, Faculty of Environmental and Symbiotic Sciences, Prefectural University of Kumamoto, Kumamoto, Japan

    Naoyuki Matsumoto

  7. Neurophysiology Research Group, Tokyo Metropolitan Institute of Gerontology, 35-2 Sakae-cho, Itabashi-ku, Tokyo, 173-0015, Japan

    Toshihiko Aosaki

  8. McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA

    Ann M. Graybiel

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  1. Ko Yamanaka
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  2. Yukiko Hori
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  9. Minoru Kimura
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Correspondence to Minoru Kimura.

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Yamanaka, K., Hori, Y., Minamimoto, T. et al. Roles of centromedian parafascicular nuclei of thalamus and cholinergic interneurons in the dorsal striatum in associative learning of environmental events. J Neural Transm 125, 501–513 (2018). https://doi.org/10.1007/s00702-017-1713-z

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  • DOI: https://doi.org/10.1007/s00702-017-1713-z

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