Differential activation of monkey striatal neurons in the early and late stages of procedural learning
Abstract
The basal ganglia is a key structure for procedural learning. To examine in what aspects of procedural learning the basal ganglia participate, we recorded from striatal neurons (phasically active neurons) in monkeys while the animals were performing a sequential button press task (the 2 x 5 task) and compared the neuronal activity between two conditions: (1) while learning new sequences and (2) while executing overlearned sequences. Among 147 neurons recorded in two monkeys, 45 neurons were activated preferentially for new sequences (new-preferring neurons), 34 for overlearned sequences (learned-preferring neurons), and 68 were activated non-selectively (non-selective neurons). New-preferring neurons were more abundant in the "association" region [association striatum (AS); caudate nucleus and rostral putamen anterior to the anterior commissure], while the learned-preferring neurons were more abundant in the "sensorimotor" region [sensorimotor striatum (SM); putamen posterior to the anterior commissure]. In addition to the learning dependency, the AS and SM neurons were activated in different task periods: many AS neurons were activated during the delay period, while the SM neurons were more activated with reaching and button presses. These data, together with the data from our previous blockade study, suggest that the "association" and "sensorimotor" regions of the basal ganglia contribute preferentially to the early and late stages of procedural learning, respectively.
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Most striatal neurons that responded more strongly during early learning were in the associative striatum.
“Most of the striatal neurons that responded more strongly during early learning were in the associative striatum (Figure 1).”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [14]
The associative striatum is active during initial skill acquisition.
“Several studies have reported that the associative striatum is active during initial skill acquisition and that its activity decreases with extended training.”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [14]
Most striatal neurons that responded more strongly after over-learning a motor sequence were in the sensorimotor striatum.
“For example, Miyachi et al. [14] found that most striatal neurons that responded more strongly after over-learning a motor sequence were in the sensorimotor striatum (see Figure 1).”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [14]
Neurophysiological studies in non-human primates and rodents have found dissociable contributions of the DMS and DLS to early versus late stages of training.
“neuro-physiological studies in non-human primates [9], as well as in rodents [10], have also found dissociable contributions of the DMS and DLS to early versus late stages of training.”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [9]
A large body of research implicates the dorsal striatum in the implementation of already learned instrumental motor behaviors, with dissociations between the DLS and DMS.
“A large body of research has also implicated the dorsal striatum in the implementation of already learned instrumental motor behaviors, often with dissociations emerging between the DLS and DMS [7–10].”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [9]
There is overwhelming evidence for a role of the dorsolateral striatum in performance of well-learned motor programs.
“there is overwhelming evidence for a role of the DLS in performance of well-learned motor programs [5,7–10,18]”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [9]
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References 20 · Cited by 262
- Authors
- Miyachi, S., Hikosaka, O., & Lu, X.
- Affiliations
- Juntendo University (JP)
- Corresponding author
- Miyachi, Shigehiro
- Venue
- Experimental Brain Research
- Published
- 2002-07-26
- Volume
- 146
- Issue
- 1
- Pages
- 122-126
- ISSN
- 0014-4819 (ISSN-L)
- 1432-1106
- OpenAlex
- W2017487333
- Cited by
- 262
- References
- 20
- Citations by year
- 2025: 11 · 2024: 12 · 2023: 7 · 2022: 9 · 2021: 10 · 2020: 12 · 2019: 17 · 2018: 16 · 2017: 15 · 2016: 11 · 2015: 22 · 2014: 14 · 2013: 15 · 2012: 16
- FWCI
- 3.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Experimental Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Keywords
- procedural learning, basal ganglia, striatum, phasic neuronal activity, sensorimotor striatum, caudate nucleus, putamen, overlearning, delay period
- MeSH terms
- Animals, Extracellular Space, Learning, Macaca, Male, Neurons, Overlearning, Psychomotor Performance, Neostriatum
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