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Dopamine D2 receptors modulate the cholinergic pause and inhibitory learning

Molecular Psychiatry volume 27, pages 1502–1514 (2022)Cite this article

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Abstract

Cholinergic interneurons (CINs) in the striatum respond to salient stimuli with a multiphasic response, including a pause, in neuronal activity. Slice-physiology experiments have shown the importance of dopamine D2 receptors (D2Rs) in regulating CIN pausing, yet the behavioral significance of the CIN pause and its regulation by dopamine in vivo is still unclear. Here, we show that D2R upregulation in CINs of the nucleus accumbens (NAc) lengthens the pause in CIN activity ex vivo and enlarges a stimulus-evoked decrease in acetylcholine (ACh) levels during behavior. This enhanced dip in ACh levels is associated with a selective deficit in the learning to inhibit responding in a Go/No-Go task. Our data demonstrate, therefore, the importance of CIN D2Rs in modulating the CIN response induced by salient stimuli and point to a role of this response in inhibitory learning. This work has important implications for brain disorders with altered striatal dopamine and ACh function, including schizophrenia and attention-deficit hyperactivity disorder (ADHD).

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Fig. 1: D2R upregulation does not alter intrinsic properties or firing in NAc CINs.
Fig. 2: D2R upregulation in NAc CINs increases pause duration.
Fig. 3: D2R upregulation in NAc CINs alters ACh levels in a continuous-reinforcement (CRF) task.
Fig. 4: D2R upregulation in NAc CINs impairs No-Go responding.
Fig. 5: CIN D2R upregulation reduces contrast in cue-evoked phasic ACh signaling in Go/No-Go task.

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Acknowledgements

We would like to thank Dr. Lin Tian for providing dLight1.2, and Christine Lim, Julianna Cavallaro, Daphne Baker, and Natalie Zarrelli for assistance with histology. Also, many thanks to Dr. Nao Chuhma and Dr. Steven Rayport for advice on slice physiology, and Joseph Floeder, Dr. Marie Labouesse, and Dr. Mark Ansorge for assistance with fiber photometry.

Funding

C.K., J.G., K.M.M., J.A.J., and P.D.B. were supported by R01 MH093672 and R01 MH124858. P.D.B and J.A.J. were also supported by MH068073 and MH054137, respectively. E.F.G, J.Y., and E.T. were supported by K01 MH107648 and a Faculty Research Grant (Fordham University). J.M.V was supported by the Leon Levy Fellowship in Neuroscience.

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Authors and Affiliations

  1. Department of Biological Sciences, Fordham University, Bronx, NY, USA

    Eduardo F. Gallo & Jenna Yeisley

  2. Department of Psychiatry, Columbia University, New York, NY, USA

    Julia Greenwald, Eric Teboul, Joseph M. Villarin, Jonathan A. Javitch, Peter D. Balsam & Christoph Kellendonk

  3. Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, USA

    Julia Greenwald, Eric Teboul, Kelly M. Martyniuk, Joseph M. Villarin, Jonathan A. Javitch, Peter D. Balsam & Christoph Kellendonk

  4. Department of Neuroscience, Columbia University, New York, NY, USA

    Kelly M. Martyniuk

  5. State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, Beijing, China

    Yulong Li

  6. Department of Molecular Pharmacology and Therapeutics, Columbia University, New York, NY, USA

    Jonathan A. Javitch & Christoph Kellendonk

  7. Department of Psychology, Columbia University, New York, NY, USA

    Peter D. Balsam

  8. Division of Developmental Neuroscience, New York State Psychiatric Institute, New York, NY, USA

    Peter D. Balsam

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Contributions

E.F.G., J.G., J.Y., E.T., and K.M.M. performed the experiments. E.F.G., J.G., C.K., and P.D.B. analyzed the data. E.G. and C.K. designed the experiments and supervised the project, with input from P.D.B. and J.A.J.; E.F.G. and C.K. wrote the paper with input from J.G., J.A.J., Y.L., and P.D.B.

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Gallo, E.F., Greenwald, J., Yeisley, J. et al. Dopamine D2 receptors modulate the cholinergic pause and inhibitory learning. Mol Psychiatry 27, 1502–1514 (2022). https://doi.org/10.1038/s41380-021-01364-y

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