Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping
Open accessAbstract
Dopamine (DA) neurons in the midbrain ventral tegmental area (VTA) integrate complex inputs to encode multiple signals that influence motivated behaviors via diverse projections. Here, we combine axon-initiated viral transduction with rabies-mediated trans-synaptic tracing and Cre-based cell-type-specific targeting to systematically map input-output relationships of VTA-DA neurons. We found that VTA-DA (and VTA-GABA) neurons receive excitatory, inhibitory, and modulatory input from diverse sources. VTA-DA neurons projecting to different forebrain regions exhibit specific biases in their input selection. VTA-DA neurons projecting to lateral and medial nucleus accumbens innervate largely non-overlapping striatal targets, with the latter also sending extensive extra-striatal axon collaterals. Using electrophysiology and behavior, we validated new circuits identified in our tracing studies, including a previously unappreciated top-down reinforcing circuit from anterior cortex to lateral nucleus accumbens via VTA-DA neurons. This study highlights the utility of our viral-genetic tracing strategies to elucidate the complex neural substrates that underlie motivated behaviors.
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The input-output architecture of the DR serotonin system differs from the locus coeruleus norepinephrine system with more homogeneous input and output, and resembles midbrain dopamine systems with biased input and segregated output.
“Thus, the input-output architecture of the DR serotonin system differs from that of the locus coeruleus norepinephrine system with more homogeneous input and output (Schwarz et al., 2015), and resembles more closely those of the midbrain dopamine systems (Beier et al., 2015; Lerner et al., 2015), with biased input and segregated output.”
From Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems (2018) · cites this paper as Beier et al., 2015
NAc, dRph, and VTA receive direct or indirect projections from hypothalamic OT neurons.
“the nucleus accumbens (NAc), dorsal raphe nucleus (dRph), and ventral tegmental area (VTA) receive direct or indirect projections from hypothalamic OT neurons (Beier et al., 2015; Dölen et al., 2013; Hung et al., 2017; Nardou et al., 2019)”
From Parallel social information processing circuits are differentially impacted in autism (2020) · cites this paper as Beier et al., 2015
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Oxytocin functions as a spatiotemporal filter for excitatory synaptic inputs to VTA dopamine neurons
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“We labeled glutamatergic neurons in LHb and PPN using a Slc17a6 probe, observing extensive overlap between GRB signal and Slc17a6 puncta in both of these regions.”
BackgroundInfluentialHypocretin as a Hub for Arousal and Motivation
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- Authors
- Beier, K. T., Steinberg, E. E., DeLoach, K. E., Xie, S., Miyamichi, K., Schwarz, L., Gao, X. J., Kremer, E. J., Malenka, R. C., & Luo, L.
- Affiliations
- Howard Hughes Medical Institute (US)
- Stanford Medicine (US)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Malenka, Robert C.
- Luo, Liqun
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2015-07
- Volume
- 162
- Issue
- 3
- Pages
- 622-634
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4522312
- OpenAlex
- W1870304014
- Cited by
- 1,068
- References
- 49
- Citations by year
- 2026: 82 · 2025: 122 · 2024: 101 · 2023: 127 · 2022: 111 · 2021: 93 · 2020: 105 · 2019: 98 · 2018: 92 · 2017: 63 · 2016: 58 · 2015: 14
- FWCI
- 35.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH099647, TR01MH099647, P50MH086403)
- National Institute on Drug Abuse (F32DA038913, P01DA008227)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- ventral tegmental area, dopaminergic neurons, input-output mapping, transsynaptic tracing, rabies virus tracing, nucleus accumbens, striatum, axon collaterals, anterior cortex, motivated behavior, neural circuits
- MeSH terms
- Animals, Brain Mapping, Dopamine, gamma-Aminobutyric Acid, Mice, Inbred C57BL, Neural Pathways, Neurons, Nucleus Accumbens, Rabies virus, Ventral Tegmental Area, Mice
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