Reward-driven Changes in Striatal Pathway Competition Shape Evidence Evaluation in Decision-making

Overview

Journal PLoS Comput Biol

Specialty Biology

Date 2019 May 7

PMID 31060045

Citations 16

Authors

Kyle Dunovan

Catalina Vich

Matthew Clapp

Timothy Verstynen

Jonathan Rubin

Affiliations

Soon will be listed here.

Abstract

Cortico-basal-ganglia-thalamic (CBGT) networks are critical for adaptive decision-making, yet how changes to circuit-level properties impact cognitive algorithms remains unclear. Here we explore how dopaminergic plasticity at corticostriatal synapses alters competition between striatal pathways, impacting the evidence accumulation process during decision-making. Spike-timing dependent plasticity simulations showed that dopaminergic feedback based on rewards modified the ratio of direct and indirect corticostriatal weights within opposing action channels. Using the learned weight ratios in a full spiking CBGT network model, we simulated neural dynamics and decision outcomes in a reward-driven decision task and fit them with a drift diffusion model. Fits revealed that the rate of evidence accumulation varied with inter-channel differences in direct pathway activity while boundary height varied with overall indirect pathway activity. This multi-level modeling approach demonstrates how complementary learning and decision computations can emerge from corticostriatal plasticity.

Citing Articles

CBGTPy: An extensible cortico-basal ganglia-thalamic framework for modeling biological decision making.

Clapp M, Bahuguna J, Giossi C, Rubin J, Verstynen T, Vich C PLoS One. 2025; 20(1):e0310367.

PMID: 39808625 PMC: 11731724. DOI: 10.1371/journal.pone.0310367.

Arkypallidal neurons in the external globus pallidus can mediate inhibitory control by altering competition in the striatum.

Giossi C, Bahuguna J, Rubin J, Verstynen T, Vich C Proc Natl Acad Sci U S A. 2024; 121(47):e2408505121.

PMID: 39536079 PMC: 11588131. DOI: 10.1073/pnas.2408505121.

Distinct dopaminergic spike-timing-dependent plasticity rules are suited to different functional roles.

Sosis B, Rubin J bioRxiv. 2024; .

PMID: 38979377 PMC: 11230239. DOI: 10.1101/2024.06.24.600372.

How cortico-basal ganglia-thalamic subnetworks can shift decision policies to maximize reward rate.

Bahuguna J, Verstynen T, Rubin J bioRxiv. 2024; .

PMID: 38826315 PMC: 11142098. DOI: 10.1101/2024.05.21.595174.

Anti-Hebbian plasticity drives sequence learning in striatum.

Vignoud G, Venance L, Touboul J Commun Biol. 2024; 7(1):555.

PMID: 38724614 PMC: 11082161. DOI: 10.1038/s42003-024-06203-8.

References

Parker J, Marshall J, Ahanonu B, Wu Y, Kim T, Grewe B . Diametric neural ensemble dynamics in parkinsonian and dyskinetic states. Nature. 2018; 557(7704):177-182. PMC: 6526726. DOI: 10.1038/s41586-018-0090-6. View

Licata A, Kaufman M, Raposo D, Ryan M, Sheppard J, Churchland A . Posterior Parietal Cortex Guides Visual Decisions in Rats. J Neurosci. 2017; 37(19):4954-4966. PMC: 5426183. DOI: 10.1523/JNEUROSCI.0105-17.2017. View

Krakauer J, Ghazanfar A, Gomez-Marin A, MacIver M, Poeppel D . Neuroscience Needs Behavior: Correcting a Reductionist Bias. Neuron. 2017; 93(3):480-490. DOI: 10.1016/j.neuron.2016.12.041. View

Escande M, Taravini I, Zold C, Belforte J, Murer M . Loss of Homeostasis in the Direct Pathway in a Mouse Model of Asymptomatic Parkinson's Disease. J Neurosci. 2016; 36(21):5686-98. PMC: 6601837. DOI: 10.1523/JNEUROSCI.0492-15.2016. View

Dreyer J, Herrik K, Berg R, Hounsgaard J . Influence of phasic and tonic dopamine release on receptor activation. J Neurosci. 2010; 30(42):14273-83. PMC: 6634758. DOI: 10.1523/JNEUROSCI.1894-10.2010. View

Afacan-Seref K, Steinemann N, Blangero A, Kelly S . Dynamic Interplay of Value and Sensory Information in High-Speed Decision Making. Curr Biol. 2018; 28(5):795-802.e6. PMC: 5841252. DOI: 10.1016/j.cub.2018.01.071. View

Ratcliff R, Frank M . Reinforcement-based decision making in corticostriatal circuits: mutual constraints by neurocomputational and diffusion models. Neural Comput. 2012; 24(5):1186-229. DOI: 10.1162/NECO_a_00270. View

Gurney K, Humphries M, Redgrave P . A new framework for cortico-striatal plasticity: behavioural theory meets in vitro data at the reinforcement-action interface. PLoS Biol. 2015; 13(1):e1002034. PMC: 4285402. DOI: 10.1371/journal.pbio.1002034. View

Bogacz R, Gurney K . The basal ganglia and cortex implement optimal decision making between alternative actions. Neural Comput. 2007; 19(2):442-77. DOI: 10.1162/neco.2007.19.2.442. View

10.

Jahfari S, Ridderinkhof K, Collins A, Knapen T, Waldorp L, Frank M . Cross-Task Contributions of Frontobasal Ganglia Circuitry in Response Inhibition and Conflict-Induced Slowing. Cereb Cortex. 2018; 29(5):1969-1983. DOI: 10.1093/cercor/bhy076. View

11.

Richfield E, Penney J, Young A . Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system. Neuroscience. 1989; 30(3):767-77. DOI: 10.1016/0306-4522(89)90168-1. View

12.

Herz D, Zavala B, Bogacz R, Brown P . Neural Correlates of Decision Thresholds in the Human Subthalamic Nucleus. Curr Biol. 2016; 26(7):916-20. PMC: 4826434. DOI: 10.1016/j.cub.2016.01.051. View

13.

Forstmann B, Anwander A, Schafer A, Neumann J, Brown S, Wagenmakers E . Cortico-striatal connections predict control over speed and accuracy in perceptual decision making. Proc Natl Acad Sci U S A. 2010; 107(36):15916-20. PMC: 2936628. DOI: 10.1073/pnas.1004932107. View

14.

Steiner L, Barreda Tomas F, Planert H, Alle H, Vida I, Geiger J . Connectivity and Dynamics Underlying Synaptic Control of the Subthalamic Nucleus. J Neurosci. 2019; 39(13):2470-2481. PMC: 6435833. DOI: 10.1523/JNEUROSCI.1642-18.2019. View

15.

Mallet N, Ballion B, Le Moine C, Gonon F . Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci. 2006; 26(14):3875-84. PMC: 6674115. DOI: 10.1523/JNEUROSCI.4439-05.2006. View

16.

Herz D, Tan H, Brittain J, Fischer P, Cheeran B, Green A . Distinct mechanisms mediate speed-accuracy adjustments in cortico-subthalamic networks. Elife. 2017; 6. PMC: 5287713. DOI: 10.7554/eLife.21481. View

17.

Collins A, Frank M . Opponent actor learning (OpAL): modeling interactive effects of striatal dopamine on reinforcement learning and choice incentive. Psychol Rev. 2014; 121(3):337-66. DOI: 10.1037/a0037015. View

18.

Ding L, Gold J . Caudate encodes multiple computations for perceptual decisions. J Neurosci. 2010; 30(47):15747-59. PMC: 3005761. DOI: 10.1523/JNEUROSCI.2894-10.2010. View

19.

Gonon F . Prolonged and extrasynaptic excitatory action of dopamine mediated by D1 receptors in the rat striatum in vivo. J Neurosci. 1997; 17(15):5972-8. PMC: 6573191. View

20.

Fourcaud-Trocme N, Hansel D, van Vreeswijk C, Brunel N . How spike generation mechanisms determine the neuronal response to fluctuating inputs. J Neurosci. 2003; 23(37):11628-40. PMC: 6740955. View