Cited by 795Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchDeep Brain Stimulation and Movement Disorders

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Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits

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Lerner, Talia N., Shilyansky, Carrie, Davidson, Thomas J., Evans, Kathryn E., Beier, Kevin T., Zalocusky, Kelly A., Crow, Ailey K., Malenka, Robert C., Luo, Liqun, Tomer, Raju, Deisseroth, Karl·2015·Cell

DOI 10.1016/j.cell.2015.07.014PMC PMC4790813

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Abstract

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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A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · cited 2×
“Seminal early studies into the information encoded by midbrain DA 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.”
Result
Ultrasensitive 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×
“We expressed GCaMP6f (Chen et al., 2013) in DMS- or DLS-projecting SNc DA neurons by injecting CAV-cre into the DMS or the DLS, followed by injection of a cre-dependent GCaMP6f construct into the SNc.”
Method
Learning to predict by the methods of temporal differences
Sutton, R. S. (1988) · Machine Learning · doi:10.1007/bf00115009 · Cited by 5,148 · cited 2×
“…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).”
Background
Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396 · cited 4×
“…that the DA neurons, which increase their firing in response to these stimuli, may signal salience rather than value (Brischoux et al., 2009; Bromberg-Martin et al., 2010; Matsumoto and Hikosaka, 2009), though controversy on this point remains (Cohen et al., 2012; Fiorillo et al., 2013,…”
BackgroundInfluential
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Montague, P., Dayan, P., & Sejnowski, T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01936.1996 · Cited by 2,066 · cited 1×
“…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).”
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-citation
Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum
Haber, 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.”
Background
Natural 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).”
Method
Two 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…”
BackgroundResultInfluential
Neuron-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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“In fact, it has been shown that SNc DA neurons, including ALDH1A1 + DA neurons, receive strong monosynaptic inputs from direct MSNs originating from the DMS and VMS (37, 74, 81), and that direct MSNs (dMSNs) negatively influence DA release in the DLS and firing of ALDH1A1 + DA neurons (82, 83).”
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“Furthermore, previous studies have associated the SNc with processing negative emotion [11] and promoting REM sleep [12].”
Background
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“Fluorescence was excited by 405 nm and 465 nm sinusoidally modulated light at ~200 Hz and ~500 Hz respectively, and bandpass-filtered 500 – 550 nm emitted light was collected and demodulated [41].”
Method
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“To control for motion artifacts, we excited GCaMP6s with its calcium-dependent excitation wavelength of 470 nm and at its calcium-independent isosbestic excitation wavelength of 405 nm (Lerner et al., 2015).”
Method
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“To assess the activity of VTA neurons during the consumption of differently-flavored macronutrient solutions, the ‘bulk’ fluorescence signal generated by GCaMP6s expressing cells was recorded using fiber photometry (Gunaydin et al., 2014; Lerner et al., 2015).”
Method
G-protein coupled receptor 88 knock-down in the associative striatum reduces the psychiatric symptoms in a translational model of Parkinson’s diseasePreprint
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“21 pathways may provide a system for such lateral transfer of information (71).”
Background
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“F/F0 was calculated as (465nm-405nm)/fitted(405nm) [37].”
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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: Lerner, Talia N.
Davidson, Thomas J.
Evans, Kathryn E.
Beier, Kevin T.
Zalocusky, Kelly A.
Malenka, Robert C.
Luo, Liqun
Tomer, Raju
Deisseroth, Karl
Venue: Cell
Publisher: Elsevier BV
Published: 2015-07
Volume: 162
Issue: 3
Pages: 635-647
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2015.07.014
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 395 d)
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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Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits

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