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Nigrostriatal dopamine pathway regulates auditory discrimination behavior

Author

Listed:
  • Allen P. F. Chen

    (Stony Brook University
    Renaissance School of Medicine at Stony Brook University)

  • Jeffrey M. Malgady

    (Stony Brook University)

  • Lu Chen

    (Stony Brook University)

  • Kaiyo W. Shi

    (Stony Brook University)

  • Eileen Cheng

    (Stony Brook University
    Stony Brook University)

  • Joshua L. Plotkin

    (Stony Brook University
    Stony Brook University)

  • Shaoyu Ge

    (Stony Brook University)

  • Qiaojie Xiong

    (Stony Brook University)

Abstract

The auditory striatum, the tail portion of dorsal striatum in basal ganglia, is implicated in perceptual decision-making, transforming auditory stimuli to action outcomes. Despite its known connections to diverse neurological conditions, the dopaminergic modulation of sensory striatal neuronal activity and its behavioral influences remain unknown. We demonstrated that the optogenetic inhibition of dopaminergic projections from the substantia nigra pars compacta to the auditory striatum specifically impairs mouse choice performance but not movement in an auditory frequency discrimination task. In vivo dopamine and calcium imaging in freely behaving mice revealed that this dopaminergic projection modulates striatal tone representations, and tone-evoked striatal dopamine release inversely correlated with the evidence strength of tones. Optogenetic inhibition of D1-receptor expressing neurons and pharmacological inhibition of D1 receptors in the auditory striatum dampened choice performance accuracy. Our study uncovers a phasic mechanism within the nigrostriatal system that regulates auditory decisions by modulating ongoing auditory perception.

Suggested Citation

  • Allen P. F. Chen & Jeffrey M. Malgady & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Joshua L. Plotkin & Shaoyu Ge & Qiaojie Xiong, 2022. "Nigrostriatal dopamine pathway regulates auditory discrimination behavior," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33747-2
    DOI: 10.1038/s41467-022-33747-2
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    as
    1. Ali Mohebi & Jeffrey R. Pettibone & Arif A. Hamid & Jenny-Marie T. Wong & Leah T. Vinson & Tommaso Patriarchi & Lin Tian & Robert T. Kennedy & Joshua D. Berke, 2019. "Dissociable dopamine dynamics for learning and motivation," Nature, Nature, vol. 570(7759), pages 65-70, June.
    2. Joaquim Alves da Silva & Fatuel Tecuapetla & Vitor Paixão & Rui M. Costa, 2018. "Dopamine neuron activity before action initiation gates and invigorates future movements," Nature, Nature, vol. 554(7691), pages 244-248, February.
    3. John N. J. Reynolds & Brian I. Hyland & Jeffery R. Wickens, 2001. "A cellular mechanism of reward-related learning," Nature, Nature, vol. 413(6851), pages 67-70, September.
    4. Lan Guo & William I. Walker & Nicholas D. Ponvert & Phoebe L. Penix & Santiago Jaramillo, 2018. "Stable representation of sounds in the posterior striatum during flexible auditory decisions," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    5. Christophe Micheyl & Paul R Schrater & Andrew J Oxenham, 2013. "Auditory Frequency and Intensity Discrimination Explained Using a Cortical Population Rate Code," PLOS Computational Biology, Public Library of Science, vol. 9(11), pages 1-7, November.
    6. Ben Engelhard & Joel Finkelstein & Julia Cox & Weston Fleming & Hee Jae Jang & Sharon Ornelas & Sue Ann Koay & Stephan Y. Thiberge & Nathaniel D. Daw & David W. Tank & Ilana B. Witten, 2019. "Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons," Nature, Nature, vol. 570(7762), pages 509-513, June.
    7. Ali Mohebi & Jeffrey R. Pettibone & Arif A. Hamid & Jenny-Marie T. Wong & Leah T. Vinson & Tommaso Patriarchi & Lin Tian & Robert T. Kennedy & Joshua D. Berke, 2019. "Publisher Correction: Dissociable dopamine dynamics for learning and motivation," Nature, Nature, vol. 571(7763), pages 3-3, July.
    8. Zhong Li & Jin-Xing Wei & Guang-Wei Zhang & Junxiang J. Huang & Brian Zingg & Xiyue Wang & Huizhong W. Tao & Li I. Zhang, 2021. "Corticostriatal control of defense behavior in mice induced by auditory looming cues," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    9. Yusuke Iino & Takeshi Sawada & Kenji Yamaguchi & Mio Tajiri & Shin Ishii & Haruo Kasai & Sho Yagishita, 2020. "Dopamine D2 receptors in discrimination learning and spine enlargement," Nature, Nature, vol. 579(7800), pages 555-560, March.
    10. Liang Chen & Xinxing Wang & Shaoyu Ge & Qiaojie Xiong, 2019. "Medial geniculate body and primary auditory cortex differentially contribute to striatal sound representations," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    11. Jeremiah Y. Cohen & Sebastian Haesler & Linh Vong & Bradford B. Lowell & Naoshige Uchida, 2012. "Neuron-type-specific signals for reward and punishment in the ventral tegmental area," Nature, Nature, vol. 482(7383), pages 85-88, February.
    12. Johannes J. Letzkus & Steffen B. E. Wolff & Elisabeth M. M. Meyer & Philip Tovote & Julien Courtin & Cyril Herry & Andreas Lüthi, 2011. "A disinhibitory microcircuit for associative fear learning in the auditory cortex," Nature, Nature, vol. 480(7377), pages 331-335, December.
    13. Mark W. Howe & Patrick L. Tierney & Stefan G. Sandberg & Paul E. M. Phillips & Ann M. Graybiel, 2013. "Prolonged dopamine signalling in striatum signals proximity and value of distant rewards," Nature, Nature, vol. 500(7464), pages 575-579, August.
    14. Petr Znamenskiy & Anthony M. Zador, 2013. "Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination," Nature, Nature, vol. 497(7450), pages 482-485, May.
    15. Bianca J. Marlin & Mariela Mitre & James A. D’amour & Moses V. Chao & Robert C. Froemke, 2015. "Oxytocin enables maternal behaviour by balancing cortical inhibition," Nature, Nature, vol. 520(7548), pages 499-504, April.
    16. Qiaojie Xiong & Petr Znamenskiy & Anthony M. Zador, 2015. "Selective corticostriatal plasticity during acquisition of an auditory discrimination task," Nature, Nature, vol. 521(7552), pages 348-351, May.
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    1. Allen P. F. Chen & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Shaoyu Ge & Qiaojie Xiong, 2023. "Nigrostriatal dopamine modulates the striatal-amygdala pathway in auditory fear conditioning," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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