» Articles » PMID: 29958111

Optogenetic Editing Reveals the Hierarchical Organization of Learned Action Sequences

Overview
Journal Cell
Publisher Cell Press
Specialty Cell Biology
Date 2018 Jun 30
PMID 29958111
Citations 58
Authors
Affiliations
Soon will be listed here.
Abstract

The organization of action into sequences underlies complex behaviors that are essential for organismal survival and reproduction. Despite extensive studies of innate sequences in relation to central pattern generators, how learned action sequences are controlled and whether they are organized as a chain or a hierarchy remain largely unknown. By training mice to perform heterogeneous action sequences, we demonstrate that striatal direct and indirect pathways preferentially encode different behavioral levels of sequence structure. State-dependent closed-loop optogenetic stimulation of the striatal direct pathway can selectively insert a single action element into the sequence without disrupting the overall sequence length. Optogenetic manipulation of the striatal indirect pathway completely removes the ongoing subsequence while leaving the following subsequence to be executed with the appropriate timing and length. These results suggest that learned action sequences are not organized in a serial but rather a hierarchical structure that is distinctly controlled by basal ganglia pathways.

Citing Articles

Distinct role of primate DLPFC and LIP in hierarchical control of learned saccade sequences.

Wang Q, Shi B, Jia J, Hu J, Li H, Jin X iScience. 2025; 28(1):111694.

PMID: 39877070 PMC: 11773476. DOI: 10.1016/j.isci.2024.111694.


Striosomes control dopamine via dual pathways paralleling canonical basal ganglia circuits.

Lazaridis I, Crittenden J, Ahn G, Hirokane K, Wickersham I, Yoshida T Curr Biol. 2024; 34(22):5263-5283.e8.

PMID: 39447573 PMC: 11702862. DOI: 10.1016/j.cub.2024.09.070.


Hand-Jaw Coordination as Mice Handle Food Is Organized around Intrinsic Structure-Function Relationships.

Barrett J, Martin M, Gao M, Druzinsky R, Miri A, Shepherd G J Neurosci. 2024; 44(42).

PMID: 39251351 PMC: 11484547. DOI: 10.1523/JNEUROSCI.0856-24.2024.


Striatal projection neurons coexpressing dopamine D1 and D2 receptors modulate the motor function of D1- and D2-SPNs.

Bonnavion P, Varin C, Fakhfouri G, Martinez Olondo P, De Groote A, Cornil A Nat Neurosci. 2024; 27(9):1783-1793.

PMID: 38965445 DOI: 10.1038/s41593-024-01694-4.


Striosomes Target Nigral Dopamine-Containing Neurons via Direct-D1 and Indirect-D2 Pathways Paralleling Classic Direct-Indirect Basal Ganglia Systems.

Lazaridis I, Crittenden J, Ahn G, Hirokane K, Yoshida T, Wickersham I bioRxiv. 2024; .

PMID: 38915684 PMC: 11195572. DOI: 10.1101/2024.06.01.596922.


References
1.
Tecuapetla F, Jin X, Lima S, Costa R . Complementary Contributions of Striatal Projection Pathways to Action Initiation and Execution. Cell. 2016; 166(3):703-715. DOI: 10.1016/j.cell.2016.06.032. View

2.
Lai C, Fisher S, Hurst J, Vargha-Khadem F, Monaco A . A forkhead-domain gene is mutated in a severe speech and language disorder. Nature. 2001; 413(6855):519-23. DOI: 10.1038/35097076. View

3.
Jin X, Costa R . Shaping action sequences in basal ganglia circuits. Curr Opin Neurobiol. 2015; 33:188-96. PMC: 4523429. DOI: 10.1016/j.conb.2015.06.011. View

4.
Kravitz A, Freeze B, Parker P, Kay K, Thwin M, Deisseroth K . Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature. 2010; 466(7306):622-6. PMC: 3552484. DOI: 10.1038/nature09159. View

5.
Saito M, Iwawaki T, Taya C, Yonekawa H, Noda M, Inui Y . Diphtheria toxin receptor-mediated conditional and targeted cell ablation in transgenic mice. Nat Biotechnol. 2001; 19(8):746-50. DOI: 10.1038/90795. View