Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons

Heather K. Decot, Vijay M.K. Namboodiri, Wei Gao, Jenna A. McHenry, Joshua H. Jennings, Sung Ho Lee, Pranish A. Kantak, Yu Chieh Jill Kao, Manasmita Das, Ilana B. Witten, Karl Deisseroth, Yen Yu Ian Shih, Garret D. Stuber

Research output: Research - peer-reviewArticle

  • 3 Citations

Abstract

Several neuropsychiatric conditions, such as addiction and schizophrenia, may arise in part from dysregulated activity of ventral tegmental area dopaminergic (TH VTA) neurons, as well as from more global maladaptation in neurocircuit function. However, whether TH VTA activity affects large-scale brain-wide function remains unknown. Here we selectively activated TH VTA neurons in transgenic rats and measured resulting changes in whole-brain activity using stimulus-evoked functional magnetic resonance imaging. Applying a standard generalized linear model analysis approach, our results indicate that selective optogenetic stimulation of TH VTA neurons enhanced cerebral blood volume signals in striatal target regions in a dopamine receptor-dependent manner. However, brain-wide voxel-based principal component analysis of the same data set revealed that dopaminergic modulation activates several additional anatomically distinct regions throughout the brain, not typically associated with dopamine release events. Furthermore, explicit pairing of TH VTA neuronal activation with a forepaw stimulus of a particular frequency expanded the sensory representation of that stimulus, not exclusively within the somatosensory cortices, but brain-wide. These data suggest that modulation of TH VTA neurons can impact brain dynamics across many distributed anatomically distinct regions, even those that receive little to no direct TH VTA input.

LanguageEnglish (US)
Pages615-627
Number of pages13
JournalNeuropsychopharmacology
Volume42
Issue number3
DOIs
StatePublished - Feb 1 2017

Fingerprint

Dopaminergic Neurons
Brain
Neurons
Optogenetics
Transgenic Rats
Corpus Striatum
Ventral Tegmental Area
Somatosensory Cortex
Dopamine Receptors
Principal Component Analysis
Linear Models
Dopamine
Schizophrenia
Magnetic Resonance Imaging
Cerebral Blood Volume
Datasets

ASJC Scopus subject areas

  • Pharmacology
  • Psychiatry and Mental health

Cite this

Decot, H. K., Namboodiri, V. M. K., Gao, W., McHenry, J. A., Jennings, J. H., Lee, S. H., ... Stuber, G. D. (2017). Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons. Neuropsychopharmacology, 42(3), 615-627. DOI: 10.1038/npp.2016.151

Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons. / Decot, Heather K.; Namboodiri, Vijay M.K.; Gao, Wei; McHenry, Jenna A.; Jennings, Joshua H.; Lee, Sung Ho; Kantak, Pranish A.; Jill Kao, Yu Chieh; Das, Manasmita; Witten, Ilana B.; Deisseroth, Karl; Shih, Yen Yu Ian; Stuber, Garret D.

In: Neuropsychopharmacology, Vol. 42, No. 3, 01.02.2017, p. 615-627.

Research output: Research - peer-reviewArticle

Decot, HK, Namboodiri, VMK, Gao, W, McHenry, JA, Jennings, JH, Lee, SH, Kantak, PA, Jill Kao, YC, Das, M, Witten, IB, Deisseroth, K, Shih, YYI & Stuber, GD 2017, 'Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons' Neuropsychopharmacology, vol 42, no. 3, pp. 615-627. DOI: 10.1038/npp.2016.151
Decot HK, Namboodiri VMK, Gao W, McHenry JA, Jennings JH, Lee SH et al. Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons. Neuropsychopharmacology. 2017 Feb 1;42(3):615-627. Available from, DOI: 10.1038/npp.2016.151
Decot, Heather K. ; Namboodiri, Vijay M.K. ; Gao, Wei ; McHenry, Jenna A. ; Jennings, Joshua H. ; Lee, Sung Ho ; Kantak, Pranish A. ; Jill Kao, Yu Chieh ; Das, Manasmita ; Witten, Ilana B. ; Deisseroth, Karl ; Shih, Yen Yu Ian ; Stuber, Garret D./ Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons. In: Neuropsychopharmacology. 2017 ; Vol. 42, No. 3. pp. 615-627
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