Roles of centromedian parafascicular nuclei of thalamus and cholinergic interneurons in the dorsal striatum in associative learning of environmental events
- 1.2k Downloads
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.
KeywordsThalamostriatal projection CM–Pf Dorsal striatum Cholinergic interneurons Surprise Non-human primates
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.
- Crittenden JR, Graybiel AM (2016) Disease-associated changes in the striosome and matrix compartments of the dorsal striatum. In: Steiner H, Tseng KY (eds) Handbook of basal ganglia structure and function. Elsevier, Amsterdam, pp 801–821Google Scholar
- Crittenden JR, Lacey CJ, Feng-Ju Weng E, Garrison CA, Lin Y, Graybiel AM (2017) Striatal cholinergic interneurons modulate spike-timing in striosomes and matrix by an amphetamine-sensitive mechanism Frontiers in Neuroanatomy (in press)Google Scholar
- Haber S, McFarland NR (2001) The place of the thalamus in frontal cortical-basal ganglia circuits. Neurosci Rev J Bringing Neurobiol Neurol Psychiatry 7:315–324Google Scholar
- Houk JC, Adams JL, Barto AG (1995) A model of how the basal ganglia generate and use neural signals that predict reinforcement. In: Houk JC et al (eds) Models of information processing in the Basal Ganglia. The MIT Press, Cambridge, pp 249–270Google Scholar
- Pashler H (1998) The psychology of attention. The MIT Press, Cambridge, p 494Google Scholar
- Perez-Rosello T, Figueroa A, Salgado H, Vilchis C, Tecuapetla F, Guzman JN, Galarraga E, Bargas J (2005) Cholinergic control of firing pattern and neurotransmission in rat neostriatal projection neurons: role of CaV2.1 and CaV2.2 Ca2+ channels. J Neurophysiol 93:2507–2519PubMedCrossRefGoogle Scholar
- Rescorla RA, Wagner AR (1972) Current research and theory. In: Black AH, Prokasy WF (eds) Classical conditioning II. Appleton Century Crofts, New York, pp 64–99Google Scholar
- Shen W, Plotkin JL, Francardo V, Ko WK, Xie Z, Li Q, Fieblinger T, Wess J, Neubig RR, Lindsley CW, Conn PJ, Greengard P, Bezard E, Cenci MA, Surmeier DJ (2015) M4 muscarinic receptor signaling ameliorates striatal plasticity deficits in models of l-DOPA-induced dyskinesia. Neuron 88:762–773PubMedPubMedCentralCrossRefGoogle Scholar
- Sutton RS (1988) Learning to predict by the method of temporal differences. Mach Learn 3:9–44Google Scholar
- Sutton RS, Barto AG (1998) Reinforcement Learning. The MIT press, CambridgeGoogle Scholar