Cognitive representations of intracranial self-stimulation of midbrain dopamine neurons depend on stimulation frequency

Samuel J Millard; Ivy B Hoang; Savannah Sherwood; Masakazu Taira; Vanessa Reyes; Zara Greer; Shayna L O'Connor; Kate M Wassum; Morgan H James; David J Barker; Melissa J Sharpe

doi:10.1038/s41593-024-01643-1

Cognitive representations of intracranial self-stimulation of midbrain dopamine neurons depend on stimulation frequency

Nat Neurosci. 2024 May 13. doi: 10.1038/s41593-024-01643-1. Online ahead of print.

Authors

Samuel J Millard^#¹, Ivy B Hoang^#¹, Savannah Sherwood¹, Masakazu Taira^{1

2}, Vanessa Reyes¹, Zara Greer¹, Shayna L O'Connor^{3

4

5}, Kate M Wassum¹, Morgan H James^{3

4}, David J Barker^{4

5}, Melissa J Sharpe^{6

7}

Affiliations

¹ Department of Psychology, University of California, Los Angeles, Los Angeles, CA, USA.
² Department of Psychology, University of Sydney, Camperdown, New South Wales, Australia.
³ Department of Psychiatry, Robert Wood Johnson Medical School, Rutgers, The State University of New Jersey, Piscataway, NJ, USA.
⁴ Brain Health Institute, Rutgers Biomedical Health Sciences, Rutgers, The State University of New Jersey, Piscataway, NJ, USA.
⁵ Department of Psychology, Rutgers, The State University of New Jersey, Piscataway, NJ, USA.
⁶ Department of Psychology, University of California, Los Angeles, Los Angeles, CA, USA. melissa.sharpe@sydney.edu.au.
⁷ Department of Psychology, University of Sydney, Camperdown, New South Wales, Australia. melissa.sharpe@sydney.edu.au.

^# Contributed equally.

PMID: 38741021
DOI: 10.1038/s41593-024-01643-1

Abstract

Dopamine neurons in the ventral tegmental area support intracranial self-stimulation (ICSS), yet the cognitive representations underlying this phenomenon remain unclear. Here, 20-Hz stimulation of dopamine neurons, which approximates a physiologically relevant prediction error, was not sufficient to support ICSS beyond a continuously reinforced schedule and did not endow cues with a general or specific value. However, 50-Hz stimulation of dopamine neurons was sufficient to drive robust ICSS and was represented as a specific reward to motivate behavior. The frequency dependence of this effect is due to the rate (not the number) of action potentials produced by dopamine neurons, which differently modulates dopamine release downstream.

Abstract

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