Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories
Abstract
Learning to perform a behavioural procedure as a well-ingrained habit requires extensive repetition of the behavioural sequence, and learning not to perform such behaviours is notoriously difficult. Yet regaining a habit can occur quickly, with even one or a few exposures to cues previously triggering the behaviour. To identify neural mechanisms that might underlie such learning dynamics, we made long-term recordings from multiple neurons in the sensorimotor striatum, a basal ganglia structure implicated in habit formation, in rats successively trained on a reward-based procedural task, given extinction training and then given reacquisition training. The spike activity of striatal output neurons, nodal points in cortico-basal ganglia circuits, changed markedly across multiple dimensions during each of these phases of learning. First, new patterns of task-related ensemble firing successively formed, reversed and then re-emerged. Second, task-irrelevant firing was suppressed, then rebounded, and then was suppressed again. These changing spike activity patterns were highly correlated with changes in behavioural performance. We propose that these changes in task representation in cortico-basal ganglia circuits represent neural equivalents of the explore-exploit behaviour characteristic of habit learning.
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There is a modulation in the firing rate of putamen neurons during the acquisition, extinction, and re-emergence of procedural learning.
“and there is a modulation in the firing rate of its neurons during the acquisition, extinction, and re-emergence of procedural learning (Barnes et al., 2005).”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Barnes et al., 2005
Other studies reported a decrease in the number of sensorimotor striatal neurons showing task-relevant phasic activations over the course of training.
“Other studies also reported a decrease in the number of sensorimotor striatal neurons showing task-relevant phasic activations over the course of training, but in addition, reported that a small group of neurons within the sensorimotor striatum continued to show task-related activations and that the magnitude of the phasic neuronal responses in this restricted population of neurons increased over”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [23]
In tasks with a single motor response, extended training leads to a decrease in the number of neurons within the sensorimotor striatum showing task-related activation.
“These studies have reported that extended training leads to a decrease in the number of neurons within the sensorimotor striatum showing task-related activation.”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [23]
The response of the sensorimotor striatum to extended training depends on the type of task used.
“On the other hand, there is evidence that the response of the sensorimotor striatum to extended training may depend on the type of task that is used.”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [23]
The magnitude of phasic neuronal responses in this restricted population of sensorimotor striatal neurons increased over the course of extended training.
“Other studies also reported a decrease in the number of sensorimotor striatal neurons showing task-relevant phasic activations over the course of training, but in addition, reported that a small group of neurons within the sensorimotor striatum continued to show task-related activations and that the magnitude of the phasic neuronal responses in this restricted population of neurons increased over”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [23]
A small group of neurons within the sensorimotor striatum continued to show task-related activations over extended training.
“Other studies also reported a decrease in the number of sensorimotor striatal neurons showing task-relevant phasic activations over the course of training, but in addition, reported that a small group of neurons within the sensorimotor striatum continued to show task-related activations and that the magnitude of the phasic neuronal responses in this restricted population of neurons increased over”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [23]
The number of striatal cells showing task-related activations decreases dramatically over the course of operant stimulus-response learning, as focused activity time-locked to task-related events emerges in a select group of striatal cells.
“As noted above, the number of striatal cells showing task-related activations decreases dramatically over the course of operant S-R learning, as focused activity time-locked to task-related events emerges in a select group of striatal cells [23–24].”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [23]
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“, 1986), and there is a modulation in the firing rate of its neurons during the acquisition, extinction, and re-emergence of procedural learning (Barnes et al., 2005).”
BackgroundHabit learning shapes activity dynamics in the central nucleus of the amygdala
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- Authors
- Barnes, T. D., Kubota, Y., Hu, D., Jin, D. Z., & Graybiel, A. M.
- Affiliations
- McGovern Institute for Brain Research (US)
- Pennsylvania State University (US)
- Corresponding author
- Graybiel, Ann M.
- Venue
- Nature
- Published
- 2005-10
- Volume
- 437
- Issue
- 7062
- Pages
- 1158-1161
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1979441832
- Cited by
- 595
- References
- 35
- Citations by year
- 2026: 13 · 2025: 17 · 2024: 25 · 2023: 22 · 2022: 17 · 2021: 30 · 2020: 29 · 2019: 24 · 2018: 37 · 2017: 35 · 2016: 33 · 2015: 33 · 2014: 33 · 2013: 32 · 2012: 38
- FWCI
- 14.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health (5p50ns038372-10)
- National Institute of Neurological Disorders and Stroke (P50-NS-038372)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Keywords
- habit formation, procedural memory, basal ganglia, sensorimotor striatum, memory reconsolidation, cortico-basal ganglia circuits, reward learning
- MeSH terms
- Acoustic Stimulation, Action Potentials, Animals, Basal Ganglia, Behavior, Animal, Cues, Extinction, Psychological, Habits, Memory, Neuronal Plasticity, Neurons, Reward, Maze Learning, Rats
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