Organization of monosynaptic inputs to the serotonin and dopamine neuromodulatory systems
Open accessAbstract
Serotonin and dopamine are major neuromodulators. Here, we used a modified rabies virus to identify monosynaptic inputs to serotonin neurons in the dorsal and median raphe (DR and MR). We found that inputs to DR and MR serotonin neurons are spatially shifted in the forebrain, and MR serotonin neurons receive inputs from more medial structures. Then, we compared these data with inputs to dopamine neurons in the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc). We found that DR serotonin neurons receive inputs from a remarkably similar set of areas as VTA dopamine neurons apart from the striatum, which preferentially targets dopamine neurons. Our results suggest three major input streams: a medial stream regulates MR serotonin neurons, an intermediate stream regulates DR serotonin and VTA dopamine neurons, and a lateral stream regulates SNc dopamine neurons. These results provide fundamental organizational principles of afferent control for serotonin and dopamine.
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DR serotonin neurons as a whole receive monosynaptic inputs from diverse brain regions.
“DR serotonin neurons as a whole receive monosynaptic inputs from diverse brain regions (Ogawa et al., 2014; Pollak Dorocic et al., 2014; Weissbourd et al., 2014).”
From Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems (2018) · cites this paper as Ogawa et al., 2014
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The mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
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 · see citing works
Structure and function of the brain serotonin system
Jacobs, B. L., & Azmitia, E. C. (1992) · Physiological Reviews · doi:10.1152/physrev.1992.72.1.165 · Cited by 2,574 · see citing works
Azmitia, E. C., & Segal, M. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901790311 · Cited by 1,908 · see citing works
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 · see citing works
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
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 · see citing works
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 · see citing works
Self-citationMidbrain dopamine neurons encode a quantitative reward prediction error signal
Bayer, H. M., & Glimcher, P. W. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.020 · Cited by 1,304 · see citing works
Input-specific control of reward and aversion in the ventral tegmental area
Lammel, S., Lim, B. K., Ran, C., Huang, K. W., Betley, M. J., Tye, K. M., Deisseroth, K., & Malenka, R. C. (2012) · Nature · doi:10.1038/nature11527 · Cited by 1,300 · see citing works
Phasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning
Tsai, H.-C., Zhang, F., Adamantidis, A., Stuber, G. D., Bonci, A., de Lecea, L., & Deisseroth, K. (2009) · Science · doi:10.1126/science.1168878 · Cited by 1,266 · see citing works
Whole-Brain Mapping of Direct Inputs to Midbrain Dopamine Neurons
Watabe‐Uchida, M., Zhu, L., Ogawa, S. K., Vamanrao, A., & Uchida, N. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.017 · Cited by 1,221 · see citing works
Self-citationModels of Information Processing in the Basal Ganglia
(1994) · doi:10.7551/mitpress/4708.001.0001 · Cited by 1,190 · see citing works
Monosynaptic Restriction of Transsynaptic Tracing from Single, Genetically Targeted Neurons
Wickersham, I. R., Lyon, D. C., Barnard, R. J. O., Mori, T., Finke, S., Conzelmann, K., Young, J. A. T., & Callaway, E. M. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.033 · Cited by 1,176 · see citing works
5-HT and mechanisms of defence
Deakin, J. F. W., & Graeff, F. G. (1991) · Journal of Psychopharmacology · doi:10.1177/026988119100500414 · Cited by 1,011 · see citing works
Reconciling the role of central serotonin neurons in human and animal behavior
Soubrié, P. (1986) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00022871 · Cited by 993 · see citing works
Dorsal raphe neurons: depression of firing during sleep in cats
McGinty, D., & Harper, R. M. (1976) · Brain Research · doi:10.1016/0006-8993(76)90480-7 · Cited by 900 · see citing works
A causal link between prediction errors, dopamine neurons and learning
Steinberg, E. E., Keiflin, R., Boivin, J. R., Witten, I. B., Deisseroth, K. A., & Janak, P. H. (2013) · Nature Neuroscience · doi:10.1038/nn.3413 · Cited by 879 · see citing works
Efferent connections of the habenular nuclei in the rat
Herkenham, M. A., & Nauta, W. J. H. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870103 · Cited by 855 · see citing works
Cerebral hemisphere regulation of motivated behavior
Swanson, L. W. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02905-x · Cited by 846 · see citing works
Opponent interactions between serotonin and dopamine
Daw, N. D., Kakade, S., & Dayan, P. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00052-7 · Cited by 844 · see citing works
Serotonin-dopamine interaction and its relevance to schizophrenia
Kapur, S., & Remington, G. (1996) · American Journal of Psychiatry · doi:10.1176/ajp.153.4.466 · Cited by 826 · see citing works
Reward and aversion in a heterogeneous midbrain dopamine system
Lammel, S., Lim, B. K., & Malenka, R. C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.019 · Cited by 804 · see citing works
What are the computations of the cerebellum, the basal ganglia and the cerebral cortex?
Doya, K. (1999) · Neural Networks · doi:10.1016/s0893-6080(99)00046-5 · Cited by 739 · see citing works
Metalearning and neuromodulation
Doya, K. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00044-8 · Cited by 704 · see citing works
Jhou, T. C., Fields, H. L., Baxter, M. G., Saper, C. B., & Holland, P. C. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.001 · Cited by 696 · see citing works
GABA Neurons of the VTA Drive Conditioned Place Aversion
Tan, K. R., Yvon, C., Turiault, M., Mirzabekov, J. J., Doehner, J., Labouèbe, G., Deisseroth, K. A., Tye, K. M., & Lüscher, C. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.015 · Cited by 635 · see citing works
Activation of VTA GABA Neurons Disrupts Reward Consumption
van Zessen, R., Phillips, J. L., Budygin, E. A., & Stuber, G. D. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.016 · Cited by 609 · see citing works
A Model of How the Basal Ganglia Generate and Use Neural Signals That Predict Reinforcement
Houk, J. C., Adams, J. L., & Barto, A. G. (1994) · The MIT Press eBooks · doi:10.7551/mitpress/4708.003.0020 · Cited by 555 · see citing works
Peyron, C., Petit, J.-M., Rampon, C., Jouvet, M., & Luppi, P. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00268-6 · Cited by 509 · see citing works
Differential Innervation of Direct- and Indirect-Pathway Striatal Projection Neurons
Wall, N. R., De La Parra, M., Callaway, E. M., & Kreitzer, A. C. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.014 · Cited by 489 · see citing works
Bäckman, C. M., Malik, N., Zhang, Y., Shan, L., Grinberg, A., Hoffer, B. J., Westphal, H., & Tomac, A. C. (2006) · genesis · doi:10.1002/dvg.20228 · Cited by 463 · see citing works
Opponency revisited: competition and cooperation between dopamine and serotonin
Boureau, Y.-L., & Dayan, P. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.151 · Cited by 456 · see citing works
Fiber Connections of the Basal Ganglia
Graybiel, A. M., & Ragsdale, C. W. (1979) · Progress in brain research · doi:10.1016/s0079-6123(08)61309-6 · Cited by 388 · see citing works
Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique
Aghajanian, G. K., & Wang, R. Y. (1977) · Brain Research · doi:10.1016/0006-8993(77)90291-8 · Cited by 380 · see citing works
Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions
Geisler, S., & Zahm, D. S. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20668 · Cited by 379 · see citing works
Dissecting the diversity of midbrain dopamine neurons
Roeper, J. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.03.003 · Cited by 372 · see citing works
Targeted gene expression in dopamine and serotonin neurons of the mouse brain
Zhuang, X., Masson, J., Gingrich, J. A., Rayport, S., & Hen, R. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.09.020 · Cited by 316 · see citing works
Jacobs, B. L., & Fornal, C. A. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80141-9 · Cited by 311 · see citing works
Miyamichi, K., Shlomai, Y., Shu, M., Weissbourd, B., Luo, L., & Mizrahi, A. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.027 · Cited by 310 · see citing works
Role and Origin of the GABAergic Innervation of Dorsal Raphe Serotonergic Neurons
Gervasoni, D., Peyron, C., Rampon, C., Barbagli, B., Chouvet, G., Urbain, N., Fort, P., & Luppi, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04217.2000 · Cited by 298 · see citing works
Serotonin, inhibition, and negative mood
Dayan, P., & Huys, Q. J. M. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0040004 · Cited by 263 · see citing works
Dissociable Effects of Dopamine and Serotonin on Reversal Learning
den Ouden, H. E. M., Daw, N. D., Fernández, G., Elshout, J. A., Rijpkema, M., Hoogman, M., Franke, B., & Cools, R. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.030 · Cited by 259 · see citing works
Activation of Dorsal Raphe Serotonin Neurons Underlies Waiting for Delayed Rewards
Miyazaki, K., Miyazaki, K. W., & Doya, K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3714-10.2011 · Cited by 257 · see citing works
Serotonin Selectively Modulates Reward Value in Human Decision-Making
Seymour, B., Daw, N. D., Roiser, J. P., Dayan, P., & Dolan, R. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0053-12.2012 · Cited by 252 · see citing works
Hale, M. W., & Lowry, C. A. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2089-z · Cited by 243 · see citing works
Reward-Dependent Modulation of Neuronal Activity in the Primate Dorsal Raphe Nucleus
Nakamura, K., Matsumoto, M., & Hikosaka, O. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0021-08.2008 · Cited by 243 · see citing works
Giovanni, G. D., Deurwaerdère, P. D., Mascio, M. D., Matteo, V. D., Esposito, E., & Spampinato, U. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00655-1 · Cited by 219 · see citing works
Hioki, H., Nakamura, H., Ma, Y., Konno, M., Hayakawa, T., Nakamura, K., Fujiyama, F., & Kaneko, T. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22237 · Cited by 218 · see citing works
Groenewegen, H. J., Ahlenius, S., Haber, S. N., Kowall, N. W., & Nauta, W. J. H. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902490107 · Cited by 202 · see citing works
Allers, K. A., & Sharp, T. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00518-9 · Cited by 188 · see citing works
Ranade, S., & Mainen, Z. F. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00507.2009 · Cited by 174 · see citing works
Kocsis, B., Varga, V., Dahan, L., & Attila Gabor, S. I. K. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508360103 · Cited by 158 · see citing works
Behzadi, G., Kalén, P., Parvopassu, F., & Wiklund, L. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90194-9 · Cited by 140 · see citing works
Role of Serotonin in Central Dopamine Dysfunction
Giovanni, G. D., Esposito, E., & Matteo, V. D. (2010) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00135.x · Cited by 139 · see citing works
Marcinkiewicz, M., Morcos, R., & Chrétien, M. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890103 · Cited by 134 · see citing works
Smith, Y., Kieval, J. Z., Couceyro, P. R., & Kuhar, M. J. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990517)407:4 · Cited by 122 · see citing works
Lydic, R., McCarley, R. W., & Hobson, J. A. (1983) · Brain Research · doi:10.1016/0006-8993(83)90720-5 · Cited by 110 · see citing works
Phasic responses in dorsal raphe serotonin neurons to noxious stimuli
Schweimer, J. V., & Ungless, M. A. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.09.058 · Cited by 102 · see citing works
Ferreira, J. G. P., Del-Fava, F., Hasue, R. H., & Shammah‐Lagnado, S. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.003 · Cited by 101 · see citing works
Glutamatergic drive of the dorsal raphe nucleus
Soiza‐Reilly, M., & Commons, K. G. (2011) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2011.04.004 · Cited by 95 · see citing works
Hervé, D., Simon, H., Blanc, G., Lisoprawski, A., Moal, M. L., Glowinski, J., & Tassin, J. (1979) · Neuroscience Letters · doi:10.1016/0304-3940(79)96101-9 · Cited by 89 · see citing works
Hypothalamic neuron involvement in integration of reward, aversion, and cue signals
Ono, T., Nakamura, K., Nishijo, H., & Fukuda, M. (1986) · Journal of Neurophysiology · doi:10.1152/jn.1986.56.1.63 · Cited by 87 · see citing works
Kal�n, P., Skagerberg, G., & Lindvall, O. (1988) · Experimental Brain Research · doi:10.1007/bf00279662 · Cited by 81 · see citing works
Serotonin and Sleep: Molecular, Functional and Clinical Aspects
Jellinger, K. A. (2009) · European Journal of Neurology · doi:10.1111/j.1468-1331.2008.02470.x · Cited by 70 · see citing works
Efferent and afferent connections of the dorsal and median raphe nuclei in the rat
Vertes, R. P., & Linley, S. B. (2008) · Birkhäuser Basel eBooks · doi:10.1007/978-3-7643-8561-3_3 · Cited by 63 · see citing works
Groenewegen, H. J., & Steinbusch, H. W. M. (1984) · Neuroscience Letters · doi:10.1016/0304-3940(84)90256-8 · Cited by 37 · see citing works
Montagne-Clavel, J., Oliveras, J. L., & Martin, G. E. (1995) · Pain · doi:10.1016/0304-3959(94)00129-3 · Cited by 34 · see citing works
Flagged first, then by citations
1 of the 70 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The brain on drugs: from reward to addiction
Volkow, N. D., & Morales, M. (2015) · Cell · doi:10.1016/j.cell.2015.07.046 · Cited by 1,306 · see citing works
Selective neuronal vulnerability in Parkinson disease
Surmeier, D. J., Obeso, J. A., & Halliday, G. M. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.178 · Cited by 1,120 · see citing works
Ventral tegmental area: cellular heterogeneity, connectivity and behaviour
Morales, M., & Margolis, E. B. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.165 · Cited by 1,108 · see citing works
Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems
Ren, J., Friedmann, D., Xiong, J., Liu, C. D., Ferguson, B. R., Weerakkody, T., DeLoach, K. E., Ran, C., Pun, A., Sun, Y., et al. (2018) · Cell · doi:10.1016/j.cell.2018.07.043 · Cited by 498 · see citing works
Serotonin neurons in the dorsal raphe nucleus encode reward signals
Li, Y., Zhong, W., Wang, D., Feng, Q., Liu, Z., Zhou, J., Jia, C., Hu, F., Zeng, J., Guo, Q., et al. (2016) · Nature Communications · doi:10.1038/ncomms10503 · Cited by 420 · see citing works
Monosynaptic Circuit Tracing with Glycoprotein-Deleted Rabies Viruses
Callaway, E. M., & Luo, L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0409-15.2015 · Cited by 418 · see citing works
Overlapping Brain Circuits for Homeostatic and Hedonic Feeding
Rossi, M. A., & Stuber, G. D. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2017.09.021 · Cited by 415 · see citing works
Serotonergic neurons signal reward and punishment on multiple timescales
Cohen, J. Y., Amoroso, M. W., & Uchida, N. (2015) · eLife · doi:10.7554/elife.06346 · Cited by 388 · see citing works
Self-citationThe ventral pallidum: Subregion-specific functional anatomy and roles in motivated behaviors
Root, D. H., Meléndez, R. I., Záborszky, L., & Napier, T. C. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.005 · Cited by 343 · see citing works
Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass
Menegas, W., Bergan, J. F., Ogawa, S. K., Isogai, Y., Venkataraju, K. U., Osten, P., Uchida, N., & Watabe‐Uchida, M. (2015) · eLife · doi:10.7554/elife.10032 · Cited by 324 · see citing works
Self-citationEmbracing diversity in the 5-HT neuronal system
Okaty, B. W., Commons, K. G., & Dymecki, S. M. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0151-3 · Cited by 319 · see citing works
Rabies Virus CVS-N2c ΔG Strain Enhances Retrograde Synaptic Transfer and Neuronal Viability
Reardon, T. R., Murray, A., Turi, G. F., Wirblich, C., Croce, K. R., Schnell, M. J., Jessell, T. M., & Losonczy, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.004 · Cited by 311 · see citing works
Ren, J., Isakova, A., Friedmann, D., Zeng, J., Grutzner, S. M., Pun, A., Zhao, G. Q., Kolluru, S. S., Wang, R., Lin, R., et al. (2019) · eLife · doi:10.7554/elife.49424 · Cited by 304 · see citing works
Whole-brain mapping of the direct inputs and axonal projections of POMC and AgRP neurons
Wang, D., He, X., Zhao, Z., Feng, Q., Lin, R., Sun, Y., Ding, T., Xu, F., Luo, M., & Zhan, C. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00040 · Cited by 298 · see citing works
Hu, H. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-014106 · Cited by 253 · see citing works
The Input-Output Relationship of the Cholinergic Basal Forebrain
Gielow, M. R., & Záborszky, L. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.060 · Cited by 230 · see citing works
Parkinson's Disease Is Not Simply a Prion Disorder
Surmeier, D. J., Obeso, J. A., & Halliday, G. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1787-16.2017 · Cited by 186 · see citing works
Synaptic Specificity and Application of Anterograde Transsynaptic AAV for Probing Neural Circuitry
Zingg, B., Peng, B., Huang, J., Tao, H. W., & Zhang, L. I. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2158-19.2020 · Cited by 189 · see citing works
The concept of alpha-synuclein as a prion-like protein: ten years after
Steiner, J. A., Quansah, E., & Brundin, P. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2814-1 · Cited by 183 · see citing works
Afferent Inputs to Neurotransmitter-Defined Cell Types in the Ventral Tegmental Area
Faget, L. C., Osakada, F., Duan, J., Ressler, R. L., Johnson, A. B., Proudfoot, J., Yoo, J. H., Callaway, E. M., & Hnasko, T. S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.05.057 · Cited by 180 · see citing works
An Update on the Role of Serotonin and its Interplay with Dopamine for Reward
Fischer, A. G., & Ullsperger, M. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00484 · Cited by 176 · see citing works
Stable representations of decision variables for flexible behavior
Bari, B. A., Grossman, C. D., Lubin, E. E., Rajagopalan, A. E., Cressy, J. I., & Cohen, J. Y. (2019) · Neuron · doi:10.1016/j.neuron.2019.06.001 · Cited by 173 · see citing works
Self-citationHabenula Lesions Reveal that Multiple Mechanisms Underlie Dopamine Prediction Errors
Tian, J., & Uchida, N. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.028 · Cited by 165 · see citing works
Self-citationModulating the Neuromodulators: Dopamine, Serotonin, and the Endocannabinoid System
Peters, K. Z., Cheer, J. F., & Tonini, R. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.02.001 · Cited by 171 · see citing works
Cell type-specific long-range connections of basal forebrain circuit
Do, J. P. H., Xu, M., Lee, S., Chang, W.-C., Zhang, S., Chung, S., Yung, T. J., Fan, J. L., Miyamichi, K., Luo, L., et al. (2016) · eLife · doi:10.7554/elife.13214 · Cited by 167 · see citing works
Serotonin neurons modulate learning rate through uncertainty
Grossman, C. D., Bari, B. A., & Cohen, J. Y. (2022) · Current Biology · doi:10.1016/j.cub.2021.12.006 · Cited by 164 · see citing works
Self-citationNucleus Accumbens Modulation in Reward and Aversion
Klawonn, A. M., & Malenka, R. C. (2018) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2018.83.037457 · Cited by 163 · see citing works
Communication in Neural Circuits: Tools, Opportunities, and Challenges
Lerner, T. N., Ye, L., & Deisseroth, K. (2016) · Cell · doi:10.1016/j.cell.2016.02.027 · Cited by 159 · see citing works
Nassi, J. J., Cepko, C. L., Born, R. T., & Beier, K. T. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00080 · Cited by 156 · see citing works
Cell-Type-Specific Afferent Innervation of the Nucleus Accumbens Core and Shell
Li, Z., Chen, Z., Fan, G., Li, A., Yuan, J., & Xu, T. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00084 · Cited by 155 · see citing works
The external globus pallidus: progress and perspectives
Hegeman, D. J., Hong, E. S., Hernández, V. M., & Chan, C. S. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13196 · Cited by 149 · see citing works
Chemistry of the Adaptive Mind: Lessons from Dopamine
Cools, R. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.035 · Cited by 143 · see citing works
A common hub for sleep and motor control in the substantia nigra
Liu, D., Li, W., Ma, C., Zheng, W., Yao, Y., Tso, C. F., Zhong, P., Chen, X., Song, J. H., Choi, W., et al. (2020) · Science · doi:10.1126/science.aaz0956 · Cited by 147 · see citing works
Intense threat switches dorsal raphe serotonin neurons to a paradoxical operational mode
Seo, C., Guru, A., Jin, M., Ito, B. S., Sleezer, B. J., Ho, Y.-Y., Wang, E., Boada, C. M., Krupa, N. A., Kullakanda, D. S., et al. (2019) · Science · doi:10.1126/science.aau8722 · Cited by 146 · see citing works
The integrated brain network that controls respiration
Krohn, F., Novello, M., van der Giessen, R. S., Zeeuw, C. I. D., Pel, J. J. M., & Bosman, L. W. J. (2023) · eLife · doi:10.7554/elife.83654 · Cited by 155 · see citing works
Architectural Representation of Valence in the Limbic System
Namburi, P., Al‐Hasani, R., Calhoon, G. G., Bruchas, M. R., & Tye, K. M. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.358 · Cited by 133 · see citing works
A single-cell transcriptomic and anatomic atlas of mouse dorsal raphe Pet1 neurons
Okaty, B. W., Sturrock, N., Lozoya, Y. E., Chang, Y., Senft, R. A., Lyon, K. A., Alekseyenko, O. V., & Dymecki, S. M. (2020) · eLife · doi:10.7554/elife.55523 · Cited by 117 · see citing works
Zhou, L., Liu, M., Li, Q., Deng, J., Mu, D., & Sun, Y.-G. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.077 · Cited by 116 · see citing works
Reward processing by the dorsal raphe nucleus: 5-HT and beyondPreprint
Luo, M., Zhou, J., & Liu, Z. (2015) · Learning & Memory · doi:10.1101/lm.037317.114 · Cited by 117 · see citing works
A Discrete Dorsal Raphe to Basal Amygdala 5-HT Circuit Calibrates Aversive Memory
Sengupta, A., & Holmes, A. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.029 · Cited by 112 · see citing works
Evans, R. C., Zhu, M., & Khaliq, Z. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0117-17.2017 · Cited by 101 · see citing works
Dopamine and Acetylcholine, a Circuit Point of View in Parkinson’s Disease
Rizzi, G., & Tan, K. R. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00110 · Cited by 101 · see citing works
A deep learning algorithm for 3D cell detection in whole mouse brain image datasets
Tyson, A. L., Rousseau, C. V., Niedworok, C. J., Keshavarzi, S., Tsitoura, C., Cossell, L., Strom, M., & Margrie, T. W. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009074 · Cited by 101 · see citing works
Fernandez, S. P., Cauli, B., Cabezas, C., Muzerelle, A., Poncer, J.-C., & Gaspar, P. (2016) · Brain Structure and Function · doi:10.1007/s00429-015-1142-4 · Cited by 100 · see citing works
Yoshida, J., Oñate, M., Khatami, L., Vera, J. R., Farzan Nadim, A., & Khodakhah, K. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1535-22.2022 · Cited by 96 · see citing works
In vivo functional diversity of midbrain dopamine neurons within identified axonal projections
Farassat, N., Costa, K. M., Stojanovic, S., Albert, S., Kovacheva, L., Shin, J., Egger, R., Somayaji, M., Duvarci, S., Schneider, G., et al. (2019) · eLife · doi:10.7554/elife.48408 · Cited by 94 · see citing works
Review of the cytology and connections of the lateral habenula, an avatar of adaptive behaving
Zahm, D. S., & Root, D. H. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.004 · Cited by 91 · see citing works
Miyazaki, K., Miyazaki, K. W., Yamanaka, A., Tokuda, T., Tanaka, K. F., & Doya, K. (2018) · Nature Communications · doi:10.1038/s41467-018-04496-y · Cited by 79 · see citing works
The lateral habenula and the serotonergic system
Metzger, M., Bueno, D., & Lima, L. B. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.05.007 · Cited by 81 · see citing works
Sargin, D., Oliver, D. K., & Lambe, E. K. (2016) · eLife · doi:10.7554/elife.21416 · Cited by 81 · see citing works
Pinto, D. F. C., Yang, H., Dorocic, I. P., de Jong, J. W., Han, V. J., Peck, J. R., Zhu, Y., Liu, C. J., Beier, K. T., Smidt, M. P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12392-2 · Cited by 76 · see citing works
Reward Contributions to Serotonergic Functions
Liu, Z., Lin, R., & Luo, M. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-093019-112252 · Cited by 78 · see citing works
Lima, L. B., Bueno, D., Leite, F., Souza, S., Gonçalves, L., Furigo, I. C., Donato, J., & Metzger, M. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24217 · Cited by 80 · see citing works
Do dorsal raphe 5-HT neurons encode “beneficialness”?
Luo, M., Li, Y., & Zhong, W. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.008 · Cited by 76 · see citing works
Metzger, M., Souza, R., Lima, L. B., Bueno, D., Gonçalves, L., Sego, C., Donato, J., & Shammah‐Lagnado, S. J. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14647 · Cited by 77 · see citing works
Glutamate Input in the Dorsal Raphe Nucleus As a Determinant of Escalated Aggression in Male Mice
Takahashi, A., Lee, R. X., Iwasato, T., Itohara, S., Arima, H., Bettler, B., Miczek, K. A., & Koide, T. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2450-14.2015 · Cited by 75 · see citing works
Plastic and stimulus-specific coding of salient events in the central amygdala
Yang, T., Yu, K., Zhang, X., Xiao, X., Chen, X., Fu, Y., & Li, B. (2023) · Nature · doi:10.1038/s41586-023-05910-2 · Cited by 70 · see citing works
Niederkofler, V., Asher, T. E., & Dymecki, S. M. (2015) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00021 · Cited by 75 · see citing works
Azizi, S. A. (2020) · The Neuroscientist · doi:10.1177/1073858420974336 · Cited by 76 · see citing works
Ascending serotonin neuron diversity under two umbrellas
Commons, K. G. (2016) · Brain Structure and Function · doi:10.1007/s00429-015-1176-7 · Cited by 72 · see citing works
Li, Y., Li, C., Wang, X., Jin, S., Wu, Z.-H., Jiang, P., Dong, P., He, X., Xu, F., Duan, S., et al. (2019) · Neuron · doi:10.1016/j.neuron.2018.12.012 · Cited by 72 · see citing works
GABAergic modulation of serotonergic neurons in the dorsal raphe nucleus
Hernández-Vázquez, F., Garduño, J., & Hernández‐López, S. (2018) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0014 · Cited by 71 · see citing works
Zhang, L., Wang, J., Niu, C., Zhang, Y., Zhu, T., Huang, D., Ma, J., Sun, H., Gamper, N. L., Du, X., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109936 · Cited by 65 · see citing works
Transient and sustained effects of dopamine and serotonin signaling in motivation‐related behavior
Yagishita, S. (2019) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12942 · Cited by 64 · see citing works
Pilotto, A., Blau, N., Leks, E., Schulte, C., Deuschl, C., Zipser, C. M., Piel, D., Freisinger, P., Gramer, G., Kölker, S., et al. (2019) · Journal of Inherited Metabolic Disease · doi:10.1002/jimd.12049 · Cited by 62 · see citing works
Takahashi, A., Cuttoli, R. D.-D., Flanigan, M. E., Hasegawa, E., Tsunematsu, T., Aleyasin, H., Chérasse, Y., Miya, K., Okada, T., Keino‐Masu, K., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31728-z · Cited by 61 · see citing works
Self-citationA discrete serotonergic circuit regulates vulnerability to social stress
Zou, W.-J., Song, Y., Wu, M., Chen, X.-T., You, Q.-L., Yang, Q., Luo, Z.-Y., Huang, L., Kong, Y., Feng, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18010-w · Cited by 57 · see citing works
A D2 to D1 shift in dopaminergic inputs to midbrain 5-HT neurons causes anorexia in mice
Cai, X., Liu, H., Feng, B. C., Yu, M., He, Y., Liu, H., Liang, C., Yang, Y., Tu, L., Zhang, N., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01062-0 · Cited by 56 · see citing works
Xu, Z., Feng, Z., Zhao, M., Sun, Q., Deng, L., Jia, X., Jiang, T., Luo, P., Chen, W., Tudi, A., et al. (2021) · eLife · doi:10.7554/elife.65502 · Cited by 51 · see citing works
COVID-19, Oxidative Stress, and Neuroinflammation in the Depression Route
Mingoti, M. E. D., Bertollo, A. G., Simões, J. L. B., Francisco, G. R., Bagatini, M. D., & Ignácio, Z. M. (2022) · Journal of Molecular Neuroscience · doi:10.1007/s12031-022-02004-y · Cited by 56 · see citing works
Pomeranz, L. E., Ekstrand, M. I., Latcha, K. N., Smith, G. A., Enquist, L. W., & Friedman, J. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3193-16.2017 · Cited by 54 · see citing works
Autism: Oxytocin, serotonin, and social reward
Dölen, G. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1087875 · Cited by 51 · see citing works
Separable gain control of ongoing and evoked activity in the visual cortex by serotonergic input
Azimi, Z., Barzan, R., Spoida, K., Surdin, T., Wollenweber, P., Mark, M. D., Herlitze, S., & Jancke, D. (2020) · eLife · doi:10.7554/elife.53552 · Cited by 58 · see citing works
Xiao, X., Yeghiazaryan, G., Heß, S., Klemm, P., Sieben, A., Kleinridders, A., Morgan, D. A., Wunderlich, F. T., Rahmouni, K., Kong, D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25380-2 · Cited by 55 · see citing works
Demireva, E. Y., Suri, D., Morelli, E., Mahadevia, D., Chuhma, N., Teixeira, C. M., Ziolkowski-Blake, A., Hersh, M. A., Fifer, J. E., Bagchi, S., et al. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0227-x · Cited by 52 · see citing works
Synthetic consciousness: the distributed adaptive control perspective
Verschure, P. F. M. J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0448 · Cited by 51 · see citing works
Merging the Pathophysiology and Pharmacotherapy of Tics
Augustine, F., & Singer, H. S. (2018) · Europe PMC (PubMed Central) · doi:10.7916/d8h14jtx · Cited by 49 · see citing works
Prospective Coding of Dorsal Raphe Reward Signals by the Orbitofrontal Cortex
Zhou, J., Jia, C., Feng, Q., Bao, J., & Luo, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4017-14.2015 · Cited by 49 · see citing works
Two major network domains in the dorsal raphe nucleus
Commons, K. G. (2015) · Journal of Comparative Neurology · doi:10.1002/cne.23748 · Cited by 46 · see citing works
Serotonergic regulation of the dopaminergic system: Implications for reward-related functions
Courtiol, E., Menezes, E. D. C., & Teixeira, C. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.022 · Cited by 47 · see citing works
Whole-Brain Monosynaptic Afferent Inputs to Basal Forebrain Cholinergic System
Hu, R. K., Jin, S., He, X., Xu, F., & Hu, J. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00098 · Cited by 46 · see citing works
Zhu, X., Lin, K., Liu, Q., Yue, X., Mi, H., Huang, X., He, X., Wu, R., Zheng, D., Wei, D., et al. (2019) · Neuroscience Bulletin · doi:10.1007/s12264-019-00423-3 · Cited by 46 · see citing works
Selective activation of serotoninergic dorsal raphe neurons facilitates sleep through anxiolysis
Venner, A., Broadhurst, R. Y., Sohn, L. T., Todd, W. D., & Fuller, P. M. (2019) · SLEEP · doi:10.1093/sleep/zsz231 · Cited by 54 · see citing works
Curiosity: primate neural circuits for novelty and information seeking
Monosov, I. E. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00784-9 · Cited by 44 · see citing works
Shah, T., Dunning, J. L., & Contet, C. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108906 · Cited by 42 · see citing works
Serotonergic modulation across sensory modalities
Sizemore, T. R., Hurley, L. M., & Dacks, A. M. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00034.2020 · Cited by 40 · see citing works
Coates, K. E., Majot, A. T., Zhang, X., Michael, C. T., Spitzer, S. L., Gaudry, Q., & Dacks, A. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0192-17.2017 · Cited by 39 · see citing works
Ogawa, S. K., & Watabe‐Uchida, M. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.05.001 · Cited by 40 · see citing works
Self-citationMesoscale microscopy and image analysis tools for understanding the brain
Tyson, A. L., & Margrie, T. W. (2021) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2021.06.013 · Cited by 38 · see citing works
Melancholy, anhedonia, apathy: the search for separable behaviors and neural circuits in depression
Post, R. J., & Warden, M. R. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.018 · Cited by 35 · see citing works
Connections of the laterodorsal tegmental nucleus with the habenular‐interpeduncular‐raphe system
Bueno, D., Lima, L. B., Souza, R., Gonçalves, L., Leite, F., Souza, S., Furigo, I. C., Donato, J., & Metzger, M. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24729 · Cited by 38 · see citing works
The Wiring Logic of an Identified Serotonergic Neuron That Spans Sensory Networks
Coates, K. E., Calle-Schuler, S. A., Helmick, L. M., Knotts, V. L., Martik, B. N., Salman, F., Warner, L. T., Valla, S. V., Bock, D. D., & Dacks, A. M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0552-20.2020 · Cited by 36 · see citing works
de Git, K. C. G., Hazelhoff, E. M., Nota, M. H. C., Schéle, E., Luijendijk, M. C. M., Dickson, S. L., van der Plasse, G., & Adan, R. A. H. (2020) · The Journal of Physiology · doi:10.1113/jp276513 · Cited by 34 · see citing works
Multiple Mechanisms for Processing Reward Uncertainty in the Primate Basal Forebrain
Ledbetter, N. M., Chen, C. D., & Monosov, I. E. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1123-16.2016 · Cited by 33 · see citing works
Zhukovskaya, A., Zimmerman, C. A., Willmore, L., Pan-Vazquez, A., Janarthanan, S. R., Lynch, L. A., Falkner, A. L., & Witten, I. B. (2024) · Neuron · doi:10.1016/j.neuron.2024.09.009 · Cited by 32 · see citing works
Adjimann, T. S., Argañaraz, C., & Soiza‐Reilly, M. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01388-6 · Cited by 32 · see citing works
Alterations and interactions of subcortical modulatory systems in Alzheimer's disease
Leko, M. B., Hof, P. R., & Šimić, G. (2021) · Progress in brain research · doi:10.1016/bs.pbr.2020.07.016 · Cited by 31 · see citing works
Conde, K., Fang, S., & Xu, Y. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-01091-7 · Cited by 32 · see citing works
Serotonergic Modulation of Olfaction in Rodents and Insects.
Gaudry, Q. (2018) · PubMed Central · Cited by 30 · see citing works
Serotonergic modulation of cognitive computations
Doya, K., Miyazaki, K. W., & Miyazaki, K. (2021) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2021.02.003 · Cited by 28 · see citing works
- Authors
- Ogawa, S. K., Cohen, J. Y., Hwang, D., Uchida, N., & Watabe-Uchida, M.
- Affiliations
- Harvard University (US)
- Corresponding author
- Cohen, Jeremiah Y.
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 8
- Issue
- 4
- Pages
- 1105-1118
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC4142108
- OpenAlex
- W1975379532
- Cited by
- 249
- References
- 70
- Citations by year
- 2026: 13 · 2025: 14 · 2024: 20 · 2023: 23 · 2022: 12 · 2021: 26 · 2020: 19 · 2019: 33 · 2018: 17 · 2017: 23 · 2016: 22 · 2015: 25 · 2014: 2
- FWCI
- 10.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Helen Hay Whitney Foundation
- National Institutes of Health
- National Institute of Mental Health (R01MH101207, R01MH095953)
- 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
- serotonin, dopamine, monosynaptic input, dorsal raphe nucleus, median raphe, ventral tegmental area, substantia nigra pars compacta, neuromodulatory systems, afferent projections, forebrain, striatum, rabies virus tracing
- MeSH terms
- Animals, Cerebral Cortex, Dopamine, Female, Mice, Inbred C57BL, Mice, Transgenic, Neural Pathways, Synaptic Transmission, Serotonin, Synapses, Neurotransmitter Agents, Habenula, Dopaminergic Neurons, Serotonergic Neurons
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