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External globus pallidus input to the dorsal striatum regulates habitual seeking behavior in male mice

Author

Listed:
  • Matthew Baker

    (Mayo Clinic)

  • Seungwoo Kang

    (Mayo Clinic
    Augusta University)

  • Sa-Ik Hong

    (Mayo Clinic)

  • Minryung Song

    (Korea Advanced Institute of Science and Technology (KAIST))

  • Minsu Abel Yang

    (Korea Advanced Institute of Science and Technology (KAIST))

  • Lee Peyton

    (Mayo Clinic)

  • Hesham Essa

    (Mayo Clinic)

  • Sang Wan Lee

    (Korea Advanced Institute of Science and Technology (KAIST)
    Korea Advanced Institute of Science and Technology (KAIST))

  • Doo-Sup Choi

    (Mayo Clinic
    Mayo Clinic College of Medicine and Science
    Mayo Clinic College of Medicine and Science)

Abstract

The external globus pallidus (GPe) coordinates action-selection through GABAergic projections throughout the basal ganglia. GPe arkypallidal (arky) neurons project exclusively to the dorsal striatum, which regulates goal-directed and habitual seeking. However, the role of GPe arky neurons in reward-seeking remains unknown. Here, we identified that a majority of arky neurons target the dorsolateral striatum (DLS). Using fiber photometry, we found that arky activities were higher during random interval (RI; habit) compared to random ratio (RR; goal) operant conditioning. Support vector machine analysis demonstrated that arky neuron activities have sufficient information to distinguish between RR and RI behavior. Genetic ablation of this arkyGPe→DLS circuit facilitated a shift from goal-directed to habitual behavior. Conversely, chemogenetic activation globally reduced seeking behaviors, which was blocked by systemic D1R agonism. Our findings reveal a role of this arkyGPe→DLS circuit in constraining habitual seeking in male mice, which is relevant to addictive behaviors and other compulsive disorders.

Suggested Citation

  • Matthew Baker & Seungwoo Kang & Sa-Ik Hong & Minryung Song & Minsu Abel Yang & Lee Peyton & Hesham Essa & Sang Wan Lee & Doo-Sup Choi, 2023. "External globus pallidus input to the dorsal striatum regulates habitual seeking behavior in male mice," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39545-8
    DOI: 10.1038/s41467-023-39545-8
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    References listed on IDEAS

    as
    1. Rafael Renteria & Emily T. Baltz & Christina M. Gremel, 2018. "Chronic alcohol exposure disrupts top-down control over basal ganglia action selection to produce habits," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    2. Ming-Dao Mu & Hong-Yan Geng & Kang-Lin Rong & Rong-Chao Peng & Shu-Ting Wang & Lin-Ting Geng & Zhong-Ming Qian & Wing-Ho Yung & Ya Ke, 2020. "A limbic circuitry involved in emotional stress-induced grooming," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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    Cited by:

    1. Marie A. Labouesse & Arturo Torres-Herraez & Muhammad O. Chohan & Joseph M. Villarin & Julia Greenwald & Xiaoxiao Sun & Mysarah Zahran & Alice Tang & Sherry Lam & Jeremy Veenstra-VanderWeele & Clay O., 2023. "A non-canonical striatopallidal Go pathway that supports motor control," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    2. Terra A. Schall & King-Lun Li & Xiguang Qi & Brian T. Lee & William J. Wright & Erin E. Alpaugh & Rachel J. Zhao & Jianwei Liu & Qize Li & Bo Zeng & Lirong Wang & Yanhua H. Huang & Oliver M. Schlüter , 2024. "Temporal dynamics of nucleus accumbens neurons in male mice during reward seeking," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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