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

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

Robert Wood Johnson Medical School (RWJMS), Psychiatry

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

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.

Original language	English (US)
Pages (from-to)	1253-1259
Number of pages	7
Journal	Nature Neuroscience
Volume	27
Issue number	7
DOIs	https://doi.org/10.1038/s41593-024-01643-1
State	Published - Jul 2024

All Science Journal Classification (ASJC) codes

General Neuroscience

Access to Document

10.1038/s41593-024-01643-1

Cite this

@article{5aee4ade2b674db09c96ca0474cdcff1,

title = "Cognitive representations of intracranial self-stimulation of midbrain dopamine neurons depend on stimulation frequency",

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.",

author = "Millard, {Samuel J.} and Hoang, {Ivy B.} and Savannah Sherwood and Masakazu Taira and Vanessa Reyes and Zara Greer and O{\textquoteright}Connor, {Shayna L.} and Wassum, {Kate M.} and James, {Morgan H.} and Barker, {David J.} and Sharpe, {Melissa J.}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = jul,

doi = "10.1038/s41593-024-01643-1",

language = "English (US)",

volume = "27",

pages = "1253--1259",

journal = "Nature Neuroscience",

issn = "1097-6256",

publisher = "Nature Research",

number = "7",

}

TY - JOUR

T1 - Cognitive representations of intracranial self-stimulation of midbrain dopamine neurons depend on stimulation frequency

AU - Millard, Samuel J.

AU - Hoang, Ivy B.

AU - Sherwood, Savannah

AU - Taira, Masakazu

AU - Reyes, Vanessa

AU - Greer, Zara

AU - O’Connor, Shayna L.

AU - Wassum, Kate M.

AU - James, Morgan H.

AU - Barker, David J.

AU - Sharpe, Melissa J.

PY - 2024/7

Y1 - 2024/7

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85192853430&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85192853430&partnerID=8YFLogxK

U2 - 10.1038/s41593-024-01643-1

DO - 10.1038/s41593-024-01643-1

M3 - Article

C2 - 38741021

AN - SCOPUS:85192853430

SN - 1097-6256

VL - 27

SP - 1253

EP - 1259

JO - Nature Neuroscience

JF - Nature Neuroscience

IS - 7

ER -

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

Abstract

All Science Journal Classification (ASJC) codes

Access to Document

Other files and links

Fingerprint

Cite this