Multiscale single-cell analysis reveals unique phenotypes of raphe 5-HT neurons projecting to the forebrain
Abstract
Serotonergic neurons of the raphe nuclei exhibit anatomical, neurochemical and elecrophysiological heterogeneity that likely underpins their specific role in multiple behaviors. However, the precise organization of serotonin (5-HT) neurons to orchestrate 5-HT release patterns throughout the brain is not well understood. We compared the electrophysiological and neurochemical properties of dorsal and median raphe 5-HT neurons projecting to the medial prefrontal cortex (mPFC), amygdala (BLA) and dorsal hippocampus (dHP), combining retrograde tract tracing with brain slice electrophysiology and single-cell RT-PCR in Pet1-EGFP mice. Our results show that 5-HT neurons projecting to the dHP and the mPFC and the BLA form largely non-overlapping populations and that BLA-projecting neurons have characteristic excitability and membrane properties. In addition, using an unbiased clustering method that correlates anatomical, molecular and electrophysiological phenotypes, we find that 5-HT neurons with projections to the mPFC and the dHP segregate from those projecting to the BLA. Single-cell gene profiling showed a restricted expression of the peptide galanin in the population of 5-HT neurons projecting to the mPFC. Finally, cluster analysis allowed identifying an atypical subtype of 5-HT neuron with low excitability, long firing delays and preferential expression of the vesicular glutamate transporter type 3. Overall, these findings allow to define correlated anatomical and physiological identities of serotonin raphe neurons that help understanding how discrete raphe cells subpopulations account for the heterogeneous activities of the midbrain serotonergic system.
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Accumulating evidence points to physiological and molecular heterogeneity within the DR serotonin system.
“Accumulating evidence points to physiological and molecular heterogeneity within the DR serotonin system (Calizo et al., 2011; Cohen et al., 2015; Fernandez et al., 2016; Okaty et al., 2015).”
From Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems (2018) · cites this paper as Fernandez et al., 2016
The electrophysiological properties of DR serotonin neurons vary according to the projection patterns.
“The electrophysiological properties of DR serotonin neurons vary according to the projection patterns (Fernandez et al., 2016).”
From Single-cell transcriptomes and whole-brain projections of serotonin neurons in the mouse dorsal and median raphe nuclei (2019) · cites this paper as Fernandez et al., 2016
Serotonin neurons in the MR and DR have different electrophysiological characteristics, such as resting potential, membrane resistance, and reaction to serotonin receptor-1A agonist.
“Slice physiology recording showed that the serotonin neurons in the MR and DR have different electrophysiological characteristics, such as resting potential, membrane resistance, and reaction to serotonin receptor-1A agonist (Calizo et al., 2011; Fernandez et al., 2016).”
From Single-cell transcriptomes and whole-brain projections of serotonin neurons in the mouse dorsal and median raphe nuclei (2019) · cites this paper as Fernandez et al., 2016
Even bona fide DRN 5-HT neurons are molecularly, anatomically, and physiologically heterogeneous.
“Even bona fide DRN 5-HT neurons are molecularly, anatomically, and physiologically heterogeneous.”
From Molecular and anatomical organization of the dorsal raphe nucleus (2019) · cites this paper as Fernandez et al., 2016
DRN 5-HT neurons in different subregions express different G protein-coupled receptors and vesicular transporters.
“Although DRN 5-HT neurons share a common developmental lineage (Deneris and Gaspar, 2018; Jensen et al., 2008), DRN 5-HT neurons in different subregions express different G protein-coupled receptors and vesicular transporters, suggesting spatial clustering of functionally specialized neurons (Calizo et al., 2011; Fernandez et al., 2016; Lowry et al., 2000; Templin et al., 2012).”
From Molecular and anatomical organization of the dorsal raphe nucleus (2019) · cites this paper as Fernandez et al., 2016
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Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems
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Self-citation
- Authors
- Fernandez, S. P., Cauli, B., Cabezas, C., Muzerelle, A., Poncer, J.-C., & Gaspar, P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- Venue
- Brain Structure and Function
- Published
- 2015-11-25
- Volume
- 221
- Issue
- 8
- Pages
- 4007-4025
- ISSN
- 1863-2653 (ISSN-L)
- 1863-2661
- OpenAlex
- W2173903421
- Cited by
- 100
- References
- 77
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 3 · 2023: 6 · 2022: 3 · 2021: 13 · 2020: 12 · 2019: 17 · 2018: 11 · 2017: 14 · 2016: 10
- FWCI
- 5.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Brain Structure and Function (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- European Research Council (BE) (FP7-health-2007-A-201714)
- Fondation pour la Recherche Médicale (FR) (equipe FRM, Fellowship)
- ANR (France) (ANR605-neur-046)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- serotonergic neurons, dorsal raphe nucleus, median raphe, medial prefrontal cortex, amygdala, dorsal hippocampus, neuronal heterogeneity, galanin, VGLUT3, neuronal excitability, single-cell transcriptomics, neuronal cell types
- MeSH terms
- Action Potentials, Amygdala, Animals, Hippocampus, Mice, Transgenic, Neural Pathways, Phenotype, Raphe Nuclei, Prosencephalon, Prefrontal Cortex, Mice, Neuroanatomical Tract-Tracing Techniques, Single-Cell Analysis, Serotonergic Neurons
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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