Shaping action sequences in basal ganglia circuits

doi:10.1016/j.conb.2015.06.011

Current Opinion in Neurobiology

Volume 33, August 2015, Pages 188-196

https://doi.org/10.1016/j.conb.2015.06.011 Get rights and content

Highlights

•
The basal ganglia are critical for chunking motor elements into action sequences.
•
Consolidation of motor sequences is paralleled by decreases in neural variability.
•
Neural activity related to action sequences emerges in basal ganglia circuits.
•
Sequence-related activity is differentially expressed in basal ganglia subcircuits.
•
Corticostriatal plasticity is critical for neural and behavioral crystallization.

Many behaviors necessary for organism survival are learned anew and become organized as complex sequences of actions. Recent studies suggest that cortico-basal ganglia circuits are important for chunking isolated movements into precise and robust action sequences that permit the achievement of particular goals. During sequence learning many neurons in the basal ganglia develop sequence-related activity — related to the initiation, execution, and termination of sequences — suggesting that action sequences are processed as action units. Corticostriatal plasticity is critical for the crystallization of action sequences, and for the development of sequence-related neural activity. Furthermore, this sequence-related activity is differentially expressed in direct and indirect basal ganglia pathways. These findings have implications for understanding the symptoms associated with movement and psychiatric disorders.

Section snippets

Taming variability and shaping action sequences

Learning new actions often starts from trying. Selection from variability has been proposed as a general feature contributing to a wide range of biological phenomena, from evolution to gene expression, to development, and behavior and learning [25, 26, 27, 28]. Although generation of action variability is essential for new learning, the selection of movements and improvement of motor accuracy, speed, and efficiency as actions are repeated is critical for survival. There are plenty examples of

Sequence learning and corticostriatal plasticity

What mechanisms could mediate the selection of particular activity patterns in specific neuronal ensembles? A somewhat obvious answer would be that synaptic plasticity in cortico-basal ganglia circuits could select some subcircuits/patterns and dismiss others. There is increasing evidence of synaptic plasticity in cortico-basal ganglia circuits during skill or sequence learning [37, 38, 39, 40••].

In the striatum, learning an operant task where rodents pressed a lever for intracranial

Sequence-related neural activity in basal ganglia circuits

How are learned sequences encoded and executed? Identifying the first and the last elements within a sequence is critical not only in the sensory domain for perceptual recognition [61], but also in the motor domain for behavioral execution. Consolidated or crystallized sequences of movements can be reliably reproduced once activated, much like reflexes or stimulus-response type circuits producing innate actions, but how are these learned action sequences initiated and terminated? Previous

Distinct sequence-related activity in direct/indirect pathways

Basal ganglia circuitry comprises two major pathways linking input (striatum) and output (SNr and GPi): a monosynaptic GABAergic projection from dopamine D1 receptor-expressing striatal projection neurons (dSPNs) to the output nuclei including substantia nigra pars reticulata (SNr), called ‘direct pathway’; and a polysynaptic projection from dopamine D2 receptor-expressing striatal projection neurons (iSPNs) to the output nuclei through external globus pallidus (GP) via subthalamic nucleus

Organization of action sequences

Early psychologists proposed that behavioral sequences were governed by reflex chains, where the activation of the first movement elicits the second, which triggers the third, and so on, based on a stimulation-response type principle [2]. This reflex chain theory predicts that action sequences are organized in a serial manner (Figure 4a). This theory has been called into question by the fact that the neural activity before the first movement of a sequence could sometimes correlate with the

Conclusions

We presented evidence that basal ganglia circuits are involved in the shaping of newly acquired action sequences. The basal ganglia circuits are important for the ‘chunking’ of isolated motor elements into action sequences, and the shaping of behavioral variability which leads to the emergence of complex action sequences as consolidated modules or units of behavior. This behavioral ‘crystallization’ is accompanied by a decrease in trial-to-trial variability of corticostriatal activity, most

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Conflict of interest statement

Nothing declared.

Acknowledgements

This work was supported by the US National Institutes of Health Grant NS083815 to X.J and European Research Council Grant 617142 to R.M.C.

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View full text

Shaping action sequences in basal ganglia circuits

Highlights

Section snippets

Taming variability and shaping action sequences

Sequence learning and corticostriatal plasticity

Sequence-related neural activity in basal ganglia circuits

Distinct sequence-related activity in direct/indirect pathways

Organization of action sequences

Conclusions

References and recommended reading

Conflict of interest statement

Acknowledgements

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Neurobiol Learn Mem

Exp Brain Res

Science

Curr Opin Neurobiol

Psychobiology

Nature

Science

Proc Natl Acad Sci U S A

Neuron

Brain Res

Mol Psychiatry

J Neurosci

Nature

Nature

Physiol Rev

Arch Neurol

Evolution and Modification of Behavior

The Integrative Action of the Nervous System

The Behavioural Physiology of Animals and Man: The Collected Papers of Erich von Holst

Parkinson's disease. Second of two parts

N Engl J Med

Sequential organization of multiple movements: involvement of cortical motor areas

Annu Rev Neurosci

What songbirds teach us about learning

Nature

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Ann N Y Acad Sci

Start/stop signals emerge in nigrostriatal circuits during sequence learning

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Nat Neurosci

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Psychol Rev

Cerebral Mechanisms in Behavior; The Hixon Symposium

The Organization of Action: A New Synthesis

Chunking during human visuomotor sequence learning

Exp Brain Res

Learning of sequential movements in the monkey: process of learning and retention of memory

J Neurophysiol

Chunking and Serially Organized Behavior in Pigeons, Monkeys and Humans

Differential recruitment of the sensorimotor putamen and frontoparietal cortex during motor chunking in humans

Neuron

Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection

Curr Biol

Neural Darwinism: selection and reentrant signaling in higher brain function

Neuron

Motor development. A new synthesis

Am Psychol

Dynamics of the vocal imitation process: how a zebra finch learns its song

Science

A novel reinforcement model of birdsong vocalization learning

Adv Neural Inf Process Syst

Visuomotor skill learning on serial reaction time task in patients with early Parkinson's disease

Mov Disord