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Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits
Open accessAbstract
Recent progress in understanding the diversity of midbrain dopamine neurons has highlighted the importance--and the challenges--of defining mammalian neuronal cell types. Although neurons may be best categorized using inclusive criteria spanning biophysical properties, wiring of inputs, wiring of outputs, and activity during behavior, linking all of these measurements to cell types within the intact brains of living mammals has been difficult. Here, using an array of intact-brain circuit interrogation tools, including CLARITY, COLM, optogenetics, viral tracing, and fiber photometry, we explore the diversity of dopamine neurons within the substantia nigra pars compacta (SNc). We identify two parallel nigrostriatal dopamine neuron subpopulations differing in biophysical properties, input wiring, output wiring to dorsomedial striatum (DMS) versus dorsolateral striatum (DLS), and natural activity patterns during free behavior. Our results reveal independently operating nigrostriatal information streams, with implications for understanding the logic of dopaminergic feedback circuits and the diversity of mammalian neuronal cell types.
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“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 Lerner et al., 2015
In the citing paper
“Thus, a strong activation in response to the physical impact of an aversive stimulus in particularly sensitive neurons may supersede a depression reflecting the negative value, and this might appear as a categorical difference in aversive and motivational salience coding15,23,24,134.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [134]
In the citing paper
“Dopamine neurons in the lateral midbrain display greater burst activity in vivo28 and higher excitability in vitro29,30 than those in the medial midbrain, such as the ventral tegmental area (VTA), where canonical reward-processing dopamine neurons reside.”
From Dopamine dynamics as a regulatory mechanism for shifting between defensive and reward-seeking behaviors (2026) · cites this paper as [30]
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Citations
Cites
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ResultUltrasensitive fluorescent proteins for imaging neuronal activity
Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., Schreiter, E. R., Kerr, R. A., Orger, M. B., Jayaraman, V., et al. (2013) · Nature · doi:10.1038/nature12354 · Cited by 6,474 · cited 1×
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MethodLearning to predict by the methods of temporal differences
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“…neurons suggested that a key function of DA is to transmit reward prediction error signals (Mirenowicz and Schultz, 1996; Schultz et al., 1997; Waelti et al., 2001), a hypothesis concordant with temporal difference learning models (Montague et al., 1996, 2004; Steinberg et al., 2013; Sutton, 1988).”
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BackgroundInfluentialA framework for mesencephalic dopamine systems based on predictive Hebbian learning
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Structural and molecular interrogation of intact biological systems
Chung, K., Wallace, J., Kim, S.-Y., Kalyanasundaram, S., Andalman, A. S., Davidson, T. J., Mirzabekov, J. J., Zalocusky, K. A., Mattis, J., Denisin, A. K., et al. (2013) · Nature · doi:10.1038/nature12107 · Cited by 2,008 · cited 6×
“We began by demonstrating that novel circuit-tracing and -recording methodologies can be effectively combined with whole-brain CLARITY/COLM imaging (Chung et al., 2013; Tomer et al., 2014) to provide a uniquely informative overview of richly defined cell types and their global connectivity motifs…”
BackgroundMethodInfluentialSelf-citationHaber, S. N., Fudge, J. L., & McFarland, N. R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-06-02369.2000 · Cited by 1,610 · cited 1×
“This information notably enriches the ascending spiral model proposed by Haber et al. (2000), which could not make definitive statements about striatal inputs onto DAergic versus non-DAergic midbrain cells.”
BackgroundNatural neural projection dynamics underlying social behavior
Gunaydin, L. A., Grosenick, L., Finkelstein, J. C., Kauvar, I. V., Fenno, L. E., Adhikari, A., Lammel, S., Mirzabekov, J. J., Airan, R. D., Zalocusky, K. A., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.017 · Cited by 1,389 · cited 1×
“…monitored activity from projection-defined SNc DA neurons during behavior using fiber photometry, a method for collecting population intracellular [Ca2+] fluorescent signals from a genetically encoded Ca2+ indicator such as GCaMP through a single chronic fiber optic implant (Gunaydin et al., 2014).”
MethodTwo types of dopamine neuron distinctly convey positive and negative motivational signals
Matsumoto, M., & Hikosaka, O. (2009) · Nature · doi:10.1038/nature08028 · Cited by 1,378 · cited 5×
“Another study used recordings in awake monkeys to demonstrate a correlation between the depth at which a DA neuron was recorded along the electrode (indicating a more ventromedial location in the midbrain) and the likelihood that it would decrease rather than increase its firing in response to an aversive cue (Matsumo…”
BackgroundResultInfluentialNeuron-type-specific signals for reward and punishment in the ventral tegmental area
Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B., & Uchida, N. (2012) · Nature · doi:10.1038/nature10754 · Cited by 1,318
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“Along with this consideration on parallel or sequential contributions of DMS and DLS, the participations of cortical and thalamic projections to the distinct striatal territories in these learning processes have to be addressed.”
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“, 2018) or genetically (Lerner et al., 2015) identified mouse nigral DA neurons, but notches were reported in identified mouse ventral tegmental area DA neurons (Schweimer et al.”
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“Significant differences between the inputs to several projectionspecific subpopulations of dopaminergic neurons in the ventral tegmental area (VTA) and substantia nigra have recently been reported (Beier et al., 2015; Lerner et al., 2015; Ogawa & Watabe- Uchida, 2018).”
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What Role Does Striatal Dopamine Play in Goal-directed Action?
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Pavlovian-instrumental interactions in active avoidance: The bark of neutral trials
Lloyd, K., & Dayan, P. (2018) · Brain Research · doi:10.1016/j.brainres.2018.10.011 · Cited by 9
Jhou, T. C., & Vento, P. J. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.11.001 · Cited by 10
Knock-in rats expressing Cre and Flp recombinases at the Parvalbumin locusPreprint
Yu, J. Y., Pettibone, J. R., Guo, C., Zhang, S., Saunders, T. L., Hughes, E. D., Filipiak, W. E., Zeidler, M. G., Bender, K. J., Hopf, F. W., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/386474 · Cited by 13
Fronto-striatal projections regulate approach-avoidance conflictPreprint
Loewke, A. C., Minerva, A. R., Nelson, A. B., Kreitzer, A., & Gunaydin, L. A. (2020) · bioRxiv · doi:10.1101/2020.03.05.979708 · Cited by 7
“In vivo calcium data were acquired using a custom-built rig based on a previously described setup (51).”
MethodA review of cell-type specific circuit mechanisms underlying epilepsy
Zhao, P., Ding, X., Li, L., & Jiang, G. (2024) · Acta Epileptologica · doi:10.1186/s42494-024-00159-2 · Cited by 13
GnRH pulse generator activity in mouse models of polycystic ovary syndromePreprint
Zhou, Z., Han, S. Y., Pardo-Navarro, M., Wall, E. G., Desai, R., Vas, S., Handelsman, D. J., & Herbison, A. E. (2024) · eLife · doi:10.7554/elife.97179.3 · Cited by 15
“Photometry systems were built using Doric components (Doric Lenses, QC, Canada) and National Instrument data acquisition board (TX, USA) based on a previous design ( Lerner et al., 2015 ).”
Kelly, E. A., Contreras, J., Duan, A., Vassell, R., & Fudge, J. L. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.018 · Cited by 9
Brain-wide connectivity map of mouse thermosensory cortices
Bokiniec, P., Whitmire, C. J., Leva, T. M., & Poulet, J. F. A. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac386 · Cited by 9
Gyawali, U., Martin, D. A., Sun, F., Li, Y., & Calu, D. J. (2023) · eLife · doi:10.7554/elife.81980 · Cited by 9
“We calculated ΔF/F (z score) by smoothing signals from the isosbestic control channel (Lerner et al., 2015; Root et al., 2020).”
MethodPrediction error in dopamine neurons during associative learning
Amo, R. (2023) · Neuroscience Research · doi:10.1016/j.neures.2023.07.003 · Cited by 11
“…activity patterns are derived from anatomically distinct subpopulations of dopamine neurons, namely those that project to the dorsolateral striatum (Lerner et al., 2015), the ventromedial nucleus accumbens (NAc) (de Jong et al., 2019), and the tail of striatum (TS) (Menegas et al., 2017).”
BackgroundInfluentialBurkert, N., Roy, S., Häusler, M., Wuttke, D., Müller, S., Wiemer, J., Hollmann, H., Oldrati, M., Ramírez‐Franco, J., Benkert, J., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05441-6 · Cited by 11
Mongrédien, R., Anésio, A., Fernandes, G. J. D., Eagle, A. L., Maldera, S., Pham, C., Robert, S., Bezerra, F. R., Vilette, A., Bianchi, P. C., et al. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.02.904 · Cited by 11
Viral vector strategies for investigating midbrain dopamine circuits underlying motivated behaviors
Pinto, D. F. C., & Lammel, S. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.02.006 · Cited by 12
“Conversely, using classical retrograde tracing techniques, several studies have correlated a DA neuron's projection targetwith different features at the molecular, anatomical, and electrophysiological level (Beckley et al., 2013; Beier et al., 2015; Ford et al., 2006; Ikemoto, 2007; Lammel et al., 2008, 2011, 2012; Le…”
Wireless Optoelectronic Fiber Photometry Headstage for Deep Brain Structures Monitoring
Khiarak, M. N., Martel, S., Koninck, Y. D., et al. (2018) · IEEE Life Sciences Conference (LSC) · doi:10.1109/lsc.2018.8572276 · Cited by 9
“Conventional fiber photometry apparatus utilizes high performance microscopy systems with a tethered implanted fiber to deliver excitation light and retrieve the fluorescence from deep brain structures [7].”
BackgroundKrolewski, D. M., Kumar, V., Martin, B., Tomer, R., Deisseroth, K. A., Myers, R., Schatzberg, A. F., Lee, F. S., Barchas, J. D., Bunney, W. E., et al. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1583-z · Cited by 9
“Changing the ratio of acrylamide monomer to bis-acrylamide (Costantini et al. 2015, Epp et al. 2015; Lerner et al. 2015; Liu et al. 2016; Miller and Rothstein 2016; Phillips et al. 2016; Tomer et al. 2014; Treweek et al. 2015; Woo et al. 2016; Yang et al. 2014; Yu et al. 2017; Zheng and Rinaman 2016) has also been ins…”
Multi-dimensional oscillatory activity of mouse GnRH neurons in vivoPreprint
Han, S. Y., Yeo, S., Kim, J.-C., Zhou, Z., & Herbison, A. E. (2024) · eLife · doi:10.7554/elife.100856 · Cited by 9
Mantas, I., Contestabile, A., Skara, V., Loiseau, C., Santos, I., Cramb, K. M. L., Filograna, R., Wade‐Martins, R., Magill, P. J., & Meletis, K. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.22.629963 · Cited by 12
Neurexin 3α in the Central Amygdala has a Role in Orofacial Varicella Zoster Pain
Kramer, P. R., Umorin, M., Hornung, R. S., & Kinchington, P. R. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.003 · Cited by 8
Link Brain-Wide Projectome to Neuronal Dynamics in the Mouse Brain
Li, X., Du, Y., Huang, J., Li, W.-W., Song, W., Fan, R.-N., Zhou, H. K., Jiang, T., Lu, C., Guan, Z., et al. (2024) · Neuroscience Bulletin · doi:10.1007/s12264-024-01232-z · Cited by 8
“To avoid the photobleaching and phototoxicity caused by long-term imaging, we imaged the neuronal responses to foot-shock in a trial-by-trial manner, which is known to activate dopaminergic neurons [31, 32].”
Cui, L., Tang, S., Pan, J., Deng, L., Zhang, Z., Zhao, K., Si, B., & Xu, N.-L. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.115084 · Cited by 8
Superior Colliculus Projections Drive Dopamine Neuron Activity and Movement But Not Value
Poisson, C. L., Green, I. K., Stemmler, G. M., Wolff, A. R., Prohofsky, J., Herubin, C., Blake, M., & Saunders, B. T. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0291-25.2025 · Cited by 9
Doran, P. R., Fomin-Thunemann, N., Tang, R. P., Balog, D., Zimmerman, B., Kılıç, K., Martin, E. A., Kura, S., Fisher, H. P., Chabbott, G., et al. (2024) · Neurophotonics · doi:10.1117/1.nph.11.3.034310 · Cited by 8
Galet, B., Ingallinesi, M., Pegon, J., Thi, A. N. D., Ravassard, P., Biguet, N. F., & Meloni, R. (2021) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.190171 · Cited by 10
Nascimento, G. C., Bortolanza, M., Bribián, A., Leal-Luiz, G., Raisman‐Vozari, R., López‐Mascaraque, L., & Bel, E. A. D. (2023) · ASN NEURO · doi:10.1177/17590914231155976 · Cited by 7
Kahan, A., Mahe, K., Dutta, S., Kassraian, P., Wang, A. Z., & Gradinaru, V. (2023) · iScience · doi:10.1016/j.isci.2023.107865 · Cited by 9
Towards a connectome of descending commands controlling locomotion
Sharma, S., Kim, L. H., & Whelan, P. J. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2018.12.005 · Cited by 8
Nakamura, T., Rios, L. C., Yagi, T., Sasaoka, T., & Kitsukawa, T. (2019) · Neuroscience Research · doi:10.1016/j.neures.2019.12.001 · Cited by 7
Applications of tissue clearing in the spinal cord
Tian, T., & Li, X. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14938 · Cited by 9
“Combination of these engineered viruses and tissue clearing facilitates to reveal circuit organization of neurons with different biophysical properties (Lerner et al., 2015).”
BackgroundNeural basis of learning guided by sensory confidence and reward valuePreprint
Lak, A., Okun, M., Moss, M. M., Gurnani, H., Farrell, K., Wells, M. J., Reddy, C. B., Kepecs, Á., Harris, K. D., & Carandini, M. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/411413 · Cited by 9
Rappleye, M., Gordon-Fennell, A., Castro, D. C., Matarasso, A. K., Zamorano, C. A., Stine, C., Wait, S. J., Lee, J. D., Siebart, J. C., Suko, A. V., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.01.494241 · Cited by 8
“The transient increase in dMASS fluorescence in the DMS coincides with the onset of licking behavior, implying that dopamine release in the DMS may initiate but not sustain motor actions of consumption [15], [16].”
BackgroundMountoufaris, G., Nair, A., Yang, B., Kim, D., & Anderson, D. J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.01.565073 · Cited by 8
Separable dorsal raphe dopamine projections mimic the facets of a loneliness-like statePreprint
Lee, C. R., Matthews, G. A., Lemieux, M., Wasserlein, E. M., Borio, M., Miranda, R. L., Keyes, L. R., Schneider, G. P., Jia, C., Tran, A., et al. (2025) · eLife · doi:10.7554/elife.105955 · Cited by 9
Striatal Dopamine Represents Valence on Dynamic Regional Scales
Bornhoft, K. N., Prohofsky, J., O’Neal, T. J., Wolff, A. R., & Saunders, B. T. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1551-24.2025 · Cited by 11
Synapsin III Regulates Dopaminergic Neuron Development in Vertebrates
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Balsam, P. D., Simpson, E. H., Taylor, K. M., Kalmbach, A., & Gallistel, C. R. (2024) · Science Advances · doi:10.1126/sciadv.adi7137 · Cited by 7
Identification of the subventricular tegmental nucleus as brainstem reward center
Zichó, K., Balog, B. Z., Sebestény, R. Z., Brunner, J., Takács, V. T., Barth, A. M., Seng, C., Orosz, Á., Aliczki, M., Sebők, H., et al. (2025) · Science · doi:10.1126/science.adr2191 · Cited by 8
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Cai, Q., Xu, N., He, Y., Zhu, J., Ye, F., Luo, Z., Lu, R., Huang, L., Zhang, F.-Y., Chen, J.-F., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021365 · Cited by 7
“The DLS also receives DA signal inputs from the SNc, which is crucial for fine movement regulations [37].”
Background
Metadata
- Authors
- Lerner, T. N., Shilyansky, C., Davidson, T. J., Evans, K. E., Beier, K. T., Zalocusky, K. A., Crow, A. K., Malenka, R. C., Luo, L., Tomer, R., & Deisseroth, K.
- Affiliations
- Stanford University (US)
- Stanford Medicine (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Deisseroth, Karl
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2015-07
- Volume
- 162
- Issue
- 3
- Pages
- 635-647
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4790813
- OpenAlex
- W1875506666
- Cited by
- 794
- References
- 55
- Citations by year
- 2026: 52 · 2025: 90 · 2024: 87 · 2023: 77 · 2022: 85 · 2021: 77 · 2020: 70 · 2019: 71 · 2018: 70 · 2017: 51 · 2016: 51 · 2015: 13
- FWCI
- 28.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- H. L. Snyder Medical Foundation
- National Institutes of Health (5f31mh105151-02, 1f32mh105053-01)
- Defense Advanced Research Projects Agency
- National Institute of Mental Health (1F31MH105151-01, F32 MH105053, 1F32MH105053-01, P50MH086403, F31 MH105151)
- National Institute on Drug Abuse (F32DA038913, R37DA035377)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Keywords
- substantia nigra pars compacta, dopaminergic neurons, neuronal cell types, nigrostriatal pathway, dorsomedial striatum, dorsolateral striatum, striatal output, neuronal heterogeneity, clarity, optogenetics, viral tracing, fiber photometry
- MeSH terms
- Animals, Brain Mapping, Dopamine, Mice, Inbred C57BL, Neural Pathways, Neurons, Reward, Shock, Substantia Nigra, Mice
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