Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Striatal Acetylcholine and Dopamine Interactions Produce Situationappropriate Action Selection

Author(s): Laura A. Bradfield*, Serena Becchi and Michael D. Kendig

Volume 22, Issue 9, 2024

Published on: 13 September, 2023

Page: [1491 - 1496] Pages: 6

DOI: 10.2174/1570159X21666230912093041

Price: $65

Abstract

Individuals often learn how to perform new actions for particular outcomes against a complex background of existing action-outcome associations. As such, this new knowledge can interfere or even compete with existing knowledge, such that individuals must use internal and external cues to determine which action is appropriate to the current situation. The question thus remains as to how this problem is solved at a neural level. Research over the last decade or so has begun to determine how the brain achieves situation-appropriate action selection. Several converging lines of evidence suggest that it is achieved through the complex interactions of acetylcholine and dopamine within the striatum in a manner that relies on glutamatergic inputs from the cortex and thalamus. Here we briefly review this evidence, then relate it to several very recent findings to provide new, speculative insights regarding the precise nature of striatal acetylcholine/dopamine interaction dynamics and their relation to situation- appropriate action selection.

Keywords: Action-outcome contingency, acetylcholine, dopamine, striatum, thalamus, action-outcome associations.

« Previous Next »
[1]
Balleine, B.W.; Peak, J.; Matamales, M.; Bertran-Gonzalez, J.; Hart, G. The dorsomedial striatum: an optimal cellular environment for encoding and updating goal-directed learning. Curr. Opin. Behav. Sci., 2021, 41, 38-44.
[http://dx.doi.org/10.1016/j.cobeha.2021.03.004]
[2]
Stayte, S.; Dhungana, A.; Vissel, B.; Bradfield, L.A. Parafascicular thalamic and orbitofrontal cortical inputs to striatum represent states for goal-directed action selection. Front. Behav. Neurosci., 2021, 15, 655029.
[http://dx.doi.org/10.3389/fnbeh.2021.655029] [PMID: 33841111]
[3]
Yin, H.H.; Ostlund, S.B.; Knowlton, B.J.; Balleine, B.W. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci., 2005, 22(2), 513-523.
[http://dx.doi.org/10.1111/j.1460-9568.2005.04218.x] [PMID: 16045504]
[4]
Yin, H.H.; Knowlton, B.J.; Balleine, B.W. Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning. Eur. J. Neurosci., 2005, 22(2), 505-512.
[http://dx.doi.org/10.1111/j.1460-9568.2005.04219.x] [PMID: 16045503]
[5]
Balleine, B.W.; Dickinson, A. Goal-directed instrumental action: Contingency and incentive learning and their cortical substrates. Neuropharmacology, 1998, 37(4-5), 407-419.
[http://dx.doi.org/10.1016/S0028-3908(98)00033-1] [PMID: 9704982]
[6]
Balleine, B.W. The meaning of behavior: Discriminating reflex and volition in the brain. Neuron, 2019, 104(1), 47-62.
[http://dx.doi.org/10.1016/j.neuron.2019.09.024] [PMID: 31600515]
[7]
Bradfield, L.A.; Bertran-Gonzalez, J.; Chieng, B.; Balleine, B.W. The thalamostriatal pathway and cholinergic control of goal-directed action: interlacing new with existing learning in the striatum. Neuron, 2013, 79(1), 153-166.
[http://dx.doi.org/10.1016/j.neuron.2013.04.039] [PMID: 23770257]
[8]
Bell, T.; Lindner, M.; Mullins, P.G.; Christakou, A. Functional neurochemical imaging of the human striatal cholinergic system during reversal learning. Eur. J. Neurosci., 2018, 47(10), 1184-1193.
[http://dx.doi.org/10.1111/ejn.13803] [PMID: 29265530]
[9]
Bell, T.; Lindner, M.; Langdon, A.; Mullins, P.G.; Christakou, A. Regional striatal cholinergic involvement in human behavioral flexibility. J. Neurosci., 2019, 39(29), 5740-5749.
[http://dx.doi.org/10.1523/JNEUROSCI.2110-18.2019] [PMID: 31109959]
[10]
Peak, J.; Chieng, B.; Hart, G.; Balleine, B.W. Striatal direct and indirect pathway neurons differentially control the encoding and updating of goal-directed learning. eLife, 2020, 9, e58544.
[http://dx.doi.org/10.7554/eLife.58544] [PMID: 33215609]
[11]
Matamales, M.; McGovern, A.E.; Mi, J.D.; Mazzone, S.B.; Balleine, B.W.; Bertran-Gonzalez, J. Local D2- to D1-neuron transmodulation updates goal-directed learning in the striatum. Science, 2020, 367(6477), 549-555.
[http://dx.doi.org/10.1126/science.aaz5751] [PMID: 32001651]
[12]
Tonegawa, S.; Pignatelli, M.; Roy, D.S.; Ryan, T.J. Memory engram storage and retrieval. Curr. Opin. Neurobiol., 2015, 35, 101-109.
[http://dx.doi.org/10.1016/j.conb.2015.07.009] [PMID: 26280931]
[13]
Zucca, S.; Zucca, A.; Nakano, T.; Aoki, S.; Wickens, J. Pauses in cholinergic interneuron firing exert an inhibitory control on striatal output in vivo. eLife, 2018, 7, e32510.
[http://dx.doi.org/10.7554/eLife.32510] [PMID: 29578407]
[14]
Ding, J.B.; Guzman, J.N.; Peterson, J.D.; Goldberg, J.A.; Surmeier, D.J. Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron, 2010, 67(2), 294-307.
[http://dx.doi.org/10.1016/j.neuron.2010.06.017] [PMID: 20670836]
[15]
Liu, C.; Cai, X.; Ritzau-Jost, A.; Kramer, P.F.; Li, Y.; Khaliq, Z.M.; Hallermann, S.; Kaeser, P.S. An action potential initiation mechanism in distal axons for the control of dopamine release. Science, 2022, 375(6587), 1378-1385.
[http://dx.doi.org/10.1126/science.abn0532] [PMID: 35324301]
[16]
Becchi, S.; Chieng, B.; Bradfield, L.A.; Capellán, R.; Leung, B.K.; Balleine, B.W. Cognitive effects of thalamostriatal degeneration are ameliorated by normalizing striatal cholinergic activity. BioRxiv, 2022.
[http://dx.doi.org/10.1101/2022.08.25.505358]
[17]
Lange, F.; Seer, C.; Loens, S.; Wegner, F.; Schrader, C.; Dressler, D.; Dengler, R.; Kopp, B. Neural mechanisms underlying cognitive inflexibility in Parkinson’s disease. Neuropsychologia, 2016, 93(Pt A), 142-150.
[http://dx.doi.org/10.1016/j.neuropsychologia.2016.09.021] [PMID: 27693667]
[18]
Malcolm, B.R.; Foxe, J.J.; Butler, J.S.; De Sanctis, P. The aging brain shows less flexible reallocation of cognitive resources during dual-task walking: A mobile brain/body imaging (MoBI) study. Neuroimage, 2015, 117, 230-242.
[http://dx.doi.org/10.1016/j.neuroimage.2015.05.028] [PMID: 25988225]
[19]
de Lores Arnaiz, G.R.; Ordieres, M.G.L. Brain Na(+), K(+)-ATPase activity in aging and disease. Int. J. Biomed. Sci., 2014, 10(2), 85-102.
[PMID: 25018677]
[20]
Chantranupong, L.; Beron, C.C.; Zimmer, J.A.; Wen, M.J.; Wang, W.; Sabatini, B.L. Dopamine and glutamate regulate striatal acetylcholine in decision-making. Nature, 2023, 621(7979), 577-585.
[http://dx.doi.org/10.1038/s41586-023-06492-9]
[21]
Krok, A.C.; Maltese, M.; Mistry, P.; Miao, X.; Li, Y.; Tritsch, N.X. Intrinsic dopamine and acetylcholine dynamics in the striatum of mice. Nature, 2023, 621(7979), 543-548.
[http://dx.doi.org/10.1038/s41586-023-05995-9]
[22]
Bradfield, L.A.; Hart, G.; Balleine, B.W. The role of the anterior, mediodorsal, and parafascicular thalamus in instrumental conditioning. Front. Syst. Neurosci., 2013, 7, 51.
[http://dx.doi.org/10.3389/fnsys.2013.00051] [PMID: 24130522]
[23]
Prado, V.F.; Janickova, H.; Al-Onaizi, M.A.; Prado, M.A.M. Cholinergic circuits in cognitive flexibility. Neuroscience, 2017, 345, 130-141.
[http://dx.doi.org/10.1016/j.neuroscience.2016.09.013] [PMID: 27641830]
[24]
Ragozzino, M.E.; Artis, S.; Singh, A.; Twose, T.M.; Beck, J.E.; Messer, W.S., Jr The selective M1 muscarinic cholinergic agonist CDD-0102A enhances working memory and cognitive flexibility. J. Pharmacol. Exp. Ther., 2012, 340(3), 588-594.
[http://dx.doi.org/10.1124/jpet.111.187625] [PMID: 22135384]
[25]
Townsend, E.S.; Amaya, K.A.; Smedley, E.B.; Smith, K.S. Nucleus accumbens acetylcholine receptors modulate the balance of flexible and inflexible cue-directed motivation. Neuroscience, 2022.
[http://dx.doi.org/10.1101/2022.12.22.521615]
[26]
Mamaligas, A.A.; Barcomb, K.; Ford, C.P. Cholinergic transmission at muscarinic synapses in the striatum is driven equally by cortical and thalamic inputs. Cell Rep., 2019, 28(4), 1003-1014.e3.
[http://dx.doi.org/10.1016/j.celrep.2019.06.077] [PMID: 31340139]
[27]
Matamales, M.; Götz, J.; Bertran-Gonzalez, J. Quantitative imaging of cholinergic interneurons reveals a distinctive spatial organization and a functional gradient across the mouse striatum. PLoS One, 2016, 11(6), e0157682.
[http://dx.doi.org/10.1371/journal.pone.0157682]
[28]
Holly, E.N.; Davatolhagh, M.F.; Choi, K.; Alabi, O.O.; Vargas Cifuentes, L.; Fuccillo, M.V. Striatal low-threshold spiking interneurons regulate goal-directed learning. Neuron, 2019, 103(1), 92-101.e6.
[http://dx.doi.org/10.1016/j.neuron.2019.04.016] [PMID: 31097361]
[29]
Kaminer, J.; Espinoza, D.; Bhimani, S.; Tepper, J.M.; Koos, T.; Shiflett, M.W. Loss of striatal tyrosine‐hydroxylase interneurons impairs instrumental goal‐directed behavior. Eur. J. Neurosci., 2019, 50(4), 2653-2662.
[http://dx.doi.org/10.1111/ejn.14412] [PMID: 30941837]

Rights & Permissions Print Cite
Article Metrics
14
1
© 2024 Bentham Science Publishers | Privacy Policy