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: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Several neuropsychiatric conditions, such as addiction and schizophrenia, may arise in part from dysregulated activity of ventral tegmental area dopaminergic (THVTA) neurons, as well as from more global maladaptation in neurocircuit function. However, whether THVTA activity affects large-scale brain-wide function remains unknown. Here we selectively activated THVTA 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 THVTA 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 THVTA 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 THVTA neurons can impact brain dynamics across many distributed anatomically distinct regions, even those that receive little to no direct THVTA input.

Original languageEnglish
Pages (from-to)615-627
Number of pages13
JournalNeuropsychopharmacology
Volume42
Issue number3
DOIs
Publication statusPublished - Feb 2017
Externally publishedYes

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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

Keywords

  • Journal Article

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. https://doi.org/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, 02.2017, p. 615-627.

Research output: Contribution to journalArticle

Decot, HK, Namboodiri, VMK, Gao, W, McHenry, JA, Jennings, JH, Lee, S-H, Kantak, PA, Jill Kao, Y-C, Das, M, Witten, IB, Deisseroth, K, Shih, Y-YI & Stuber, GD 2017, 'Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons', Neuropsychopharmacology, vol. 42, no. 3, pp. 615-627. https://doi.org/10.1038/npp.2016.151
Decot HK, Namboodiri VMK, Gao W, McHenry JA, Jennings JH, Lee S-H et al. Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons. Neuropsychopharmacology. 2017 Feb;42(3):615-627. https://doi.org/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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