Roles of centromedian parafascicular nuclei of thalamus and cholinergic interneurons in the dorsal striatum in associative learning of environmental events.
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.
Brain Science Institute, Tamagawa University, Machida, Tokyo, Japan.|Department of Physiology, Kyoto Prefectural University of Medicine, Kyoto, Japan.|Department of Physiology, Faculty of Health and Sports Science, Juntendo University, Chiba, Japan.
Ko
K
Yamanaka
Department of Physiology, Kyoto Prefectural University of Medicine, Kyoto, Japan.|Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan.
Yukiko
Y
Hori
Department of Physiology, Kyoto Prefectural University of Medicine, Kyoto, Japan.|Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan.
Takafumi
T
Minamimoto
Department of Physiology, Kyoto Prefectural University of Medicine, Kyoto, Japan.|Division of Biomedical Science, Faculty of Medicine, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan.
Hiroshi
H
Yamada
Department of Physiology, Kyoto Prefectural University of Medicine, Kyoto, Japan.|Department of Food and Health Sciences, Faculty of Environmental and Symbiotic Sciences, Prefectural University of Kumamoto, Kumamoto, Japan.
Naoyuki
N
Matsumoto
Brain Science Institute, Tamagawa University, Machida, Tokyo, Japan.|Department of Physiology, Kyoto Prefectural University of Medicine, Kyoto, Japan.
Kazuki
K
Enomoto
Neurophysiology Research Group, Tokyo Metropolitan Institute of Gerontology, 35-2 Sakae-cho, Itabashi-ku, Tokyo, 173-0015, Japan.
Toshihiko
T
Aosaki
McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.
Ann M
AM
Graybiel
Brain Science Institute, Tamagawa University, Machida, Tokyo, Japan. mkimura@lab.tamagawa.ac.jp.|Department of Physiology, Kyoto Prefectural University of Medicine, Kyoto, Japan. mkimura@lab.tamagawa.ac.jp.
Minoru
M
Kimura
D000818:Animals; D001245:Association Learning / Q000502:physiology*; D059329:Cholinergic Neurons / Q000502:physiology*; D003342:Corpus Striatum / Q000502:physiology*; D007395:Interneurons / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology; D011323:Primates; D013787:Thalamic Nuclei / Q000502:physiology*
CM–Pf; Cholinergic interneurons; Dorsal striatum; Non-human primates; Surprise; Thalamostriatal projection