A cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learning

Convergent evidence suggests that the basal ganglia support reinforcement learning by adjusting action values according to reward prediction errors. However, adaptive behavior in stochastic environments requires the consideration of uncertainty to dynamically adjust the learning rate. We consider ho...

Full description

Bibliographic Details
Main Authors: Nicholas T Franklin, Michael J Frank
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/12029
_version_ 1811236817856364544
author Nicholas T Franklin
Michael J Frank
author_facet Nicholas T Franklin
Michael J Frank
author_sort Nicholas T Franklin
collection DOAJ
description Convergent evidence suggests that the basal ganglia support reinforcement learning by adjusting action values according to reward prediction errors. However, adaptive behavior in stochastic environments requires the consideration of uncertainty to dynamically adjust the learning rate. We consider how cholinergic tonically active interneurons (TANs) may endow the striatum with such a mechanism in computational models spanning three Marr's levels of analysis. In the neural model, TANs modulate the excitability of spiny neurons, their population response to reinforcement, and hence the effective learning rate. Long TAN pauses facilitated robustness to spurious outcomes by increasing divergence in synaptic weights between neurons coding for alternative action values, whereas short TAN pauses facilitated stochastic behavior but increased responsiveness to change-points in outcome contingencies. A feedback control system allowed TAN pauses to be dynamically modulated by uncertainty across the spiny neuron population, allowing the system to self-tune and optimize performance across stochastic environments.
first_indexed 2024-04-12T12:15:51Z
format Article
id doaj.art-7e47009f5c4f418790f435dba9c82188
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T12:15:51Z
publishDate 2015-12-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-7e47009f5c4f418790f435dba9c821882022-12-22T03:33:26ZengeLife Sciences Publications LtdeLife2050-084X2015-12-01410.7554/eLife.12029A cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learningNicholas T Franklin0Michael J Frank1https://orcid.org/0000-0001-8451-0523Department of Cognitive, Linguistic and Psychological Sciences, Brown Institute for Brain Science, Brown University, Providence, United StatesDepartment of Cognitive, Linguistic and Psychological Sciences, Brown Institute for Brain Science, Brown University, Providence, United StatesConvergent evidence suggests that the basal ganglia support reinforcement learning by adjusting action values according to reward prediction errors. However, adaptive behavior in stochastic environments requires the consideration of uncertainty to dynamically adjust the learning rate. We consider how cholinergic tonically active interneurons (TANs) may endow the striatum with such a mechanism in computational models spanning three Marr's levels of analysis. In the neural model, TANs modulate the excitability of spiny neurons, their population response to reinforcement, and hence the effective learning rate. Long TAN pauses facilitated robustness to spurious outcomes by increasing divergence in synaptic weights between neurons coding for alternative action values, whereas short TAN pauses facilitated stochastic behavior but increased responsiveness to change-points in outcome contingencies. A feedback control system allowed TAN pauses to be dynamically modulated by uncertainty across the spiny neuron population, allowing the system to self-tune and optimize performance across stochastic environments.https://elifesciences.org/articles/12029reinforcement learningbasal gangliastriatumcholinergic interneuron
spellingShingle Nicholas T Franklin
Michael J Frank
A cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learning
eLife
reinforcement learning
basal ganglia
striatum
cholinergic interneuron
title A cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learning
title_full A cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learning
title_fullStr A cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learning
title_full_unstemmed A cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learning
title_short A cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learning
title_sort cholinergic feedback circuit to regulate striatal population uncertainty and optimize reinforcement learning
topic reinforcement learning
basal ganglia
striatum
cholinergic interneuron
url https://elifesciences.org/articles/12029
work_keys_str_mv AT nicholastfranklin acholinergicfeedbackcircuittoregulatestriatalpopulationuncertaintyandoptimizereinforcementlearning
AT michaeljfrank acholinergicfeedbackcircuittoregulatestriatalpopulationuncertaintyandoptimizereinforcementlearning
AT nicholastfranklin cholinergicfeedbackcircuittoregulatestriatalpopulationuncertaintyandoptimizereinforcementlearning
AT michaeljfrank cholinergicfeedbackcircuittoregulatestriatalpopulationuncertaintyandoptimizereinforcementlearning