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Striatal indirect pathway mediates exploration via collicular competition

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  • Jaeeon Lee

    (Harvard Medical School)

  • Bernardo L. Sabatini

    (Harvard Medical School)

Abstract

The ability to suppress actions that lead to a negative outcome and explore alternative actions is necessary for optimal decision making. Although the basal ganglia have been implicated in these processes1–5, the circuit mechanisms underlying action selection and exploration remain unclear. Here, using a simple lateralized licking task, we show that indirect striatal projection neurons (iSPN) in the basal ganglia contribute to these processes through modulation of the superior colliculus (SC). Optogenetic activation of iSPNs suppresses contraversive licking and promotes ipsiversive licking. Activity in lateral superior colliculus (lSC), a region downstream of the basal ganglia, is necessary for task performance and predicts lick direction. Furthermore, iSPN activation suppresses ipsilateral lSC, but surprisingly excites contralateral lSC, explaining the emergence of ipsiversive licking. Optogenetic inactivation reveals inter-collicular competition whereby each hemisphere of the superior colliculus inhibits the other, thus allowing the indirect pathway to disinhibit the contralateral lSC and trigger licking. Finally, inactivating iSPNs impairs suppression of devalued but previously rewarded licking and reduces exploratory licking. Our results reveal that iSPNs engage the competitive interaction between lSC hemispheres to trigger a motor action and suggest a general circuit mechanism for exploration during action selection.

Suggested Citation

  • Jaeeon Lee & Bernardo L. Sabatini, 2021. "Striatal indirect pathway mediates exploration via collicular competition," Nature, Nature, vol. 599(7886), pages 645-649, November.
  • Handle: RePEc:nat:nature:v:599:y:2021:i:7886:d:10.1038_s41586-021-04055-4
    DOI: 10.1038/s41586-021-04055-4
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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. Suma Chinta & Scott R. Pluta, 2023. "Neural mechanisms for the localization of unexpected external motion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Alyse Thomas & Weiguo Yang & Catherine Wang & Sri Laasya Tipparaju & Guang Chen & Brennan Sullivan & Kylie Swiekatowski & Mahima Tatam & Charles Gerfen & Nuo Li, 2023. "Superior colliculus bidirectionally modulates choice activity in frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    4. Akshay Markanday & Sungho Hong & Junya Inoue & Erik Schutter & Peter Thier, 2023. "Multidimensional cerebellar computations for flexible kinematic control of movements," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Daigo Takeuchi & Dheeraj Roy & Shruti Muralidhar & Takashi Kawai & Andrea Bari & Chanel Lovett & Heather A. Sullivan & Ian R. Wickersham & Susumu Tonegawa, 2022. "Cingulate-motor circuits update rule representations for sequential choice decisions," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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