Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches
Open accessAbstract
Midbrain dopamine (DA) neurons have diverse functions that can in part be explained by their heterogeneity. Although molecularly distinct subtypes of DA neurons have been identified by single-cell gene expression profiling, fundamental features such as their projection patterns have not been elucidated. Progress in this regard has been hindered by the lack of genetic tools for studying DA neuron subtypes. Here we develop intersectional genetic labeling strategies, based on combinatorial gene expression, to map the projections of molecularly defined DA neuron subtypes. We reveal distinct genetically defined dopaminergic pathways arising from the substantia nigra pars compacta and from the ventral tegmental area that innervate specific regions of the caudate putamen, nucleus accumbens and amygdala. Together, the genetic toolbox and DA neuron subtype projections presented here constitute a resource that will accelerate the investigation of this clinically significant neurotransmitter system.
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ALDH1A1+ dopamine neurons of the substantia nigra pars compacta project prominently to the dorsal caudate putamen, with fibers being denser in rostral sections and less dense caudally.
“Prominent projections of ALDH1A1+ DA neurons of the SNc have been observed in the dorsal caudate putamen (CP; [20–22]), with fibers being more dense in rostral sections and less so in caudal regions.”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [20]
In the dorsal caudate putamen, ALDH1A1+ dopamine neurons preferentially innervate some mu-opioid receptor-positive patches, known as striosomes, although this preference is not exclusive.
“In the dorsal CP, these neurons preferentially innervate some μ-opioid receptor+ (MOR) patches (commonly known as striosomes), although this is not exclusive [20–22].”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [20]
Otx2+, Aldh1a1+ dopamine neurons direct major projections to the medial shell of the nucleus accumbens and minor projections to the lateral septum.
“This population has been accessed using Aldh1a1 and NeuroD6 based drivers, and it appears to direct major projections to the medial shell of the ACB, and minor projections to the lateral septum [17,20,22,36].”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [20]
Intersectional genetic methods have been created to target DA neuron subtypes specified by combinations of genes.
“Towards this end, selective intersectional genetic approaches have been developed to target DA neuron subtypes that are defined by a combination of genes [20] (Box 3)”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [20]
Projections of Vip+ dopamine neurons are focal, mapped to the bed nucleus of the stria terminalis and central nucleus of the amygdala, and innervate a smaller target volume than other dopamine neurons.
“The projections of these neurons are peculiar in that they are particularly focal – they have been mapped to the bed nucleus of the stria terminals (BST) and central nucleus of the amygdala [13,20], and appear to innervate a much smaller target volume than other DA neurons (e.g. [49] and [50]).”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [20]
Initial studies suggested that DA neuron subtypes marked by particular genes project differently even inside the same target area.
“and initial studies have suggested that indeed DA neuron subtypes expressing given markers have distinctive projection patterns even within a given target region.”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [20]
Comparing projections of Vglut2+, Aldh1a1- and Vglut2+, Aldh1a1+ ventral tegmental area cohorts shows significant overlap in the nucleus accumbens, olfactory tubercle, and lateral septum; projections in the basolateral amygdala, entorhinal cortex, and prefrontal cortex are exclusively from Aldh1a1-, Vglut2+ projections.
“Comparing the projections of Vglut2+, Aldh1a1- and Vglut2+, Aldh1a1+ VTA cohorts, we observed significant overlap in the ACB, olfactory tubercle (OT), and lateral septum (LS). In comparison, we observed projections in the BLA, entorhinal and prefrontal cortex, exclusively from Aldh1a1-, Vglut2+ projections [20].”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [20]
Vip was found in all 3 DA neuron subtypes, as previously reported for DRN and CLi DA neurons, but Vip expression varied between the 3 subtypes.
“Although Vip was found in all 3 DA neuron subtypes, as previously reported for DRN and CLi DA neurons (Dougalis et al., 2012; Poulin et al., 2018; Poulin et al., 2014), Vip expression varied between the 3 subtypes.”
From Molecular and anatomical organization of the dorsal raphe nucleus (2019) · cites this paper as Poulin et al., 2018
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Inhibitory co-transmission from midbrain dopamine neurons relies on presynaptic GABA uptake
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“, 2021), both of which project to the lateral NAc (Beier et al., 2015; Poulin et al., 2018).”
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- Authors
- Poulin, J.-F., Caronia, G., Hofer, C., Cui, Q., Helm, B., Ramakrishnan, C., Chan, C. S., Dombeck, D. A., Deisseroth, K., & Awatramani, R.
- Affiliations
- Northwestern University (US)
- Stanford University (US)
- Corresponding author
- Awatramani, Rajeshwar
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2018-08-13
- Volume
- 21
- Issue
- 9
- Pages
- 1260-1271
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC6342021
- OpenAlex
- W2887114149
- Cited by
- 423
- References
- 64
- Citations by year
- 2026: 50 · 2025: 63 · 2024: 52 · 2023: 63 · 2022: 49 · 2021: 54 · 2020: 48 · 2019: 38 · 2018: 5
- FWCI
- 16.62
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Nature
- National Institutes of Health
- National Institute of Mental Health (R01MH110556)
- National Institute on Drug Abuse (P50DA042012)
- National Institute of Neurological Disorders and Stroke (R01NS069777, P50NS047085, R01NS096240, R21NS072703)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- combinatorial gene expression, substantia nigra pars compacta, ventral tegmental area, caudate-putamen, nucleus accumbens, amygdala, dopaminergic pathways
- MeSH terms
- Animals, Brain Mapping, Caudate Nucleus, Cell Line, Mice, Inbred C57BL, Neural Pathways, Nucleus Accumbens, Olfactory Bulb, Substantia Nigra, Gene Expression Profiling, Mice, Dopaminergic Neurons
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