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The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat

Swanson, L.W.·1982·Brain Research Bulletin

DOI 10.1016/0361-9230(82)90145-9

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Abstract

The organization of projection neurons in the ventral tegmental area (VTA), and in adjacent parts of the raphe nuclei medial to it (the central and rostral linear, and interfascicular nuclei), the mammillary body (the supramammillary region and the tuberomammillary nucleus), and the substantia nigra have been examined in the rat with Kuypers' retrograde double labeling method, and with a combined retrograde labeling (with true blue)-immunohistochemical method for the demonstration of dopaminergic neurons. First, the distribution, within the VTA and adjacent regions, of dopaminergic and non-dopaminergic cells that project to terminal fields in the telencephalon (nucleus accumbens, lateral septum, pre- and supragenual fields of the anterior limbic cortex, amygdala, dorsal hippocampus, and entorhinal area), in the diencephalon (lateral habenula), and in the brainstem (locus coeruleus, and parabrachial nucleus) was determined. Then, 15 different combinations of injections of the tracers bisbenzimide and true blue into different terminal fields were made to determine whether individual cells in the region of the VTA send collaterals to more than one site. Taken together, the results indicate that essentially separate groups of cells in the VTA and adjacent regions of the raphe project to each terminal field. In addition, each group can be further divided into dopaminergic and non-dopaminergic components, although the proportion of dopaminergic cells in each group can vary from over 80% (e.g., to the nucleus accumbens) to less than 1% (to the lateral habenula and to the locus coeruleus). In addition, it was found that the supramammillary region, which contains a dense extension of the A10 cell group in its medial part, and the tuberomammillary nucleus, project to, or through, most of the regions injected with retrograde tracers. Virtually all of the projections from the VTA and adjacent regions are partially crossed, the percentage of cells on the uninjected side ranging from over 40% (e.g., for locus coeruleus injections) to only about 2% (e.g., for amygdalar injections). Most of the groups of projection neurons in the region of the VTA are considerably intermixed with the exception of those that project to the lateral septum, to the lateral habenula, and to the hippocampal formation, which are concentrated in ventral and medial parts of the VTA, and in the raphe nuclei medial to the VTA. It was concluded that in the ventral part of the midbrain, essentially separate groups of aminergic and non-aminergic neurons in both the reticular formation (VTA) and in the adjacent nuclei of the raphe project bilaterally to a variety of similar terminal fields in the telencephalon, diencephalon, and brainstem. Further work at the single cell level is needed to determine whether these cell groups are differentially innervated by known inputs to the VTA and adjacent regions, most of which appear to descend through the medial forebrain bundle from sites in the limbic system and hypothalamus.

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Synaptic and extrasynaptic location of the receptor tyrosine kinase met during postnatal development in the mouse neocortex and hippocampus
Eagleson, K. L., Milner, T. A., Xie, Z., & Levitt, P. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23343 · Cited by 32
“…collaterals of CA3 pyramidal cells, local GABAergic interneurons, as well as projections from the medial septum, ventral tegmental area, raphe, and locus ceruleus (Moore and Halaris, 1975; Jones and Moore, 1977; Swanson, 1982; Amaral and Witter, 1989; Colom et al., 2005; Klausberger, 2009).”
Background
Adenosine A1 and Dopamine D1 Receptor Regulation of AMPA Receptor Phosphorylation and Cocaine-Seeking Behavior
Hobson, B. D., O’Neill, C. E., Levis, S. C., Monteggia, L. M., Neve, R. L., Self, D. W., & Bachtell, R. K. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.96 · Cited by 36
“The mesolimbic dopamine system consists of dopamine cells in the ventral tegmental area that project to medium spiny neurons in the nucleus accumbens (Swanson, 1982).”
Background
The role of the mesolimbic dopamine system in the formation of blood-oxygen-level dependent responses in the medial prefrontal/anterior cingulate cortex during high-frequency stimulation of the rat perforant pathway
Helbing, C., Brocka, M., Scherf, T., Lippert, M., & Angenstein, F. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x15615535 · Cited by 34
Cerebellar Modulation of Mesolimbic Dopamine Transmission Is Functionally Asymmetrical
Holloway, Z. R., Paige, N. B., Comstock, J. F., Nolen, H. G., Sable, H. J. K., & Lester, D. B. (2019) · The Cerebellum · doi:10.1007/s12311-019-01074-w · Cited by 35
Noradrenaline activation of hippocampal dopamine D 1 receptors promotes antidepressant effects
Kobayashi, K., Shikano, K., Kuroiwa, M., Horikawa, M., Ito, W., Nishi, A., Segi-Nishida, E., & Suzuki, H. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2117903119 · Cited by 34
Organization of the sleep‐related neural systems in the brain of the river hippopotamus (Hippopotamus amphibius): A most unusual cetartiodactyl species
Dell, L., Patzke, N., Spocter, M. A., Bertelsen, M. F., Siegel, J. M., & Manger, P. R. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23930 · Cited by 34
“Although the ventral tegmental area is synonymous with reward circuitry, it is also involved in locomotion, aggression, and appetitive behavior (Proshansky et al., 1974; Iversen and Koob, 1977; Swanson et al., 1981; Swanson, 1982).”
Background
The Novel Modafinil Analog, JJC8-016, as a Potential Cocaine Abuse Pharmacotherapeutic
Zhang, H., Bi, G., Yang, H.-J., He, Y., Xue, G., Cao, J., Tanda, G., Gardner, E. L., Newman, A. H., & Xi, Z. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.41 · Cited by 35
“…(DA) pathway, which originates in the midbrain ventral tegmental area (VTA) and projects to the nucleus accumbens (NAc) and prefrontal cortex (PFC), is believed to be essential for both drug reward and relapse to drug-seeking behavior (Luscher and Malenka, 2011; Swanson, 1982; Wise et al, 1996).”
Background
Fluctuations in neural activity during cocaine self-administration: clues provided by brain thermorecording
Kiyatkin, E. A., & Brown, P. L. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00711-x · Cited by 34
A catecholaminergic projection from the ventral tegmental area to the diagonal band of broca: Modulation by neurotensin
Kalivas, P. W., Jennes, L., & Miller, J. S. (1985) · Brain Research · doi:10.1016/0006-8993(85)90032-0 · Cited by 34
Neurotensin terminals form synapses primarily with neurons lacking detectable tyrosine hydroxylase immunoreactivity in the rat substantia nigra and ventral tegmental area
Woulfe, J., & Beaudet, A. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903210114 · Cited by 34
Opioid receptors in midbrain dopaminergic regions of the rat I. MU receptor autoradiography
German, D. C., Speciale, S. G., Manaye, K. F., & Sadeq, M. (1993) · Journal of Neural Transmission · doi:10.1007/bf01244917 · Cited by 34
The influence of Val158Met COMT on physiological stress responsivity
Serrano, J. M., Banks, J. B., Fagan, T. J., & Tartar, J. L. (2019) · Stress · doi:10.1080/10253890.2018.1553949 · Cited by 33
“Finally, since women have significantly more DA cells within the mesocortical pathway (Kritzer & Creutz, 2008; Swanson, 1982) we tested an equal number of men and women in order to detect possible sex differences in our results.”
A Subpopulation of Neurochemically-Identified Ventral Tegmental Area Dopamine Neurons Is Excited by Intravenous Cocaine
Mejías-Aponte, C. A., Ye, C.-Q., Bonci, A., Kiyatkin, E. A., & Morales, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3422-13.2015 · Cited by 37
“In addition, we determined the effects of cocaine on neurons within different subdivisions of the dopaminergic area A10, because subdivisions of this area have different cellular composition and connectivity (Dahlstroem and Fuxe, 1964; Swanson, 1982; Deutch et al., 1991; Yamaguchi et al., 2011).”
Background
BDNF Overexpression in the Ventral Tegmental Area Prolongs Social Defeat Stress-induced Cross-Sensitization to Amphetamine and Increases ΔFosB Expression in Mesocorticolimbic Regions of Rats
Wang, J., Fanous, S., Terwilliger, E. F., Bass, C. E., Hammer, R. P., & Nikulina, E. M. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.130 · Cited by 36
“The mesocorticolimbic circuitry is comprised of the ventral tegmental area (VTA), where dopamine neurons are located, and its projection areas: the prefrontal cortex (PFC), nucleus accumbens (NAc), hippocampus, and amygdala (Swanson, 1982).”
Background
Apo-Ghrelin Receptor (apo-GHSR1a) Regulates Dopamine Signaling in the Brain
Kern, A., Grande, C., & Smith, R. G. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00129 · Cited by 33
Spatial memory, plasticity and nucleus accumbens
Rinaldi, A., Oliverio, A., & Mele, A. (2012) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0070 · Cited by 32
“Another very important source of inputs is the ventral tegmental area (VTA), which sends to the NAc dopaminergic projections (Fallon and Moore, 1978; Swanson, 1982) that have a critical role in the mechanisms of action of natural rewards and addictive drugs (Robbins et al., 2008).”
Background
Nucleus accumbens neuronal activity in freely behaving rats is modulated following acute and chronic methylphenidate administration
Chong, S. L., Claussen, C. M., & Dafny, N. (2012) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2012.01.004 · Cited by 34
Anabolic-androgenic steroids decrease dendritic spine density in the nucleus accumbens of male rats
Wallin-Miller, K. G., Li, G., Kelishani, D., & Wood, R. I. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.045 · Cited by 33
“For instance, the VTA contains classic androgen receptors and projects to Acb (Swanson, 1982; Simerly et al., 1990).”
Background
Postnatal sequential development of dopaminergic and enkephalinergic perineuronal formations in the lateral septal nucleus of the rat correlated with local neuronal maturation
Verney, C., Gaspar, P., Alvarez, C., & Berger, B. (1987) · Anatomy and Embryology · doi:10.1007/bf00310087 · Cited by 32
Dopamine depresses melanin concentrating hormone neuronal activity through multiple effects on α2-noradrenergic, D1 and D2-like dopaminergic receptors
Conductier, G., Nahon, J., & Guyon, A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.01.030 · Cited by 33
Dopamine D3 agonists into the substantia nigra aggravate cataplexy but do not modify sleep
Honda, K., Riehl, J., Mignot, E. J.-M., & Nishino, S. (1999) · Neuroreport · doi:10.1097/00001756-199911260-00046 · Cited by 33
Substantia Nigra, Ventral Tegmental Area, and Retrorubral Fields
Halliday, G. M., Reyes, S., & Double, K. L. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374236-0.10013-6 · Cited by 34
Ultrastructural localization of enkephalin and μ-opioid receptors in the rat ventral tegmental area
Garzón, M., & Pickel, V. M. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00249-x · Cited by 33
Neurotransmitter characteristics of neurons projecting to the supramammillary nucleus of the rat
Gonzalo‐Ruiz, A., Morte, L., Flecha, J. M., & Sanz, J. M. (1999) · Anatomy and Embryology · doi:10.1007/s004290050287 · Cited by 33
Neuroanatomical and Neurochemical Substrates of Drug-Seeking Behavior: Overview and Future Directions
Watson, S. J., Trujillo, K. A., Herman, J. P., & Akil, H. (1989) · Springer eBooks · doi:10.1007/978-1-4613-8817-3_2 · Cited by 33
Opiate actions on mesocortical dopamine metabolism in the rat
Kim, H. S., Iyengar, S., & Wood, P. L. (1986) · Life Sciences · doi:10.1016/0024-3205(86)90327-9 · Cited by 33
Action of habenular efferents on ventral tegmental area neurons studied in vitro
Matsuda, Y., & Fujimura, K. (1992) · Brain Research Bulletin · doi:10.1016/0361-9230(92)90254-u · Cited by 33
Effects of inducible glial fibrillary acidic protein on glioma cell motility and proliferation
El‐Obeid, A., Bongcam‐Rudloff, E., Westermark, B., & Nist�r, M. (2000) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(20000415)60:2 · Cited by 46
Dopaminergic activation anticipates daily nursing in the rabbit
Aguirre, J. M., Meza, E., & Caba, M. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13571 · Cited by 31
“Additionally, we found an increase of FOS in the POA, which is part of the MB neural circuit that involves the VTA (Numan et al., 1990) and in the LS, which receives DAergic input from A10 and A10vr neurons (Carter & Fibiger, 1977; Swanson, 1982).”
BackgroundInfluential
Changes in reward-related signals in the rat nucleus accumbens measured by in vivo oxygen amperometry are consistent with fMRI BOLD responses in man
François, J., Conway, M. W., Lowry, J. P., Tricklebank, M. D., & Gilmour, G. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.02.024 · Cited by 32
“A neuronal projection known to be fundamental for processing reward-related signals involves dopaminergic innervations of the nucleus accumbens core and shell from the ventral tegmental area (VTA) (Dahlström and Fuxe, 1964; Fallon and Moore, 1978; Swanson, 1982).”
Gastrodin Ameliorates Memory Deficits in 3,3′-Iminodipropionitrile-Induced Rats: Possible Involvement of Dopaminergic System
Wang, X., Yan, S., Wang, A., Li, Y., & Zhang, F. (2014) · Neurochemical Research · doi:10.1007/s11064-014-1335-x · Cited by 32
The Mesoaccumbens Pathway: A Retrograde Labeling and Single-Cell Axon Tracing Analysis in the Mouse
Rodríguez-López, C., Clascá, F., & Prensa, L. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00025 · Cited by 31
“Most retrograde studies, however, were based on large tracer injections in the rat, and these injections involved both Acb subdivisions (Swanson, 1982; Albanese and Minciacchi, 1983; Phillipson and Griffiths, 1985; Brog et al., 1993; Hasue and Shammah-Lagnado, 2002; Yamaguchi et al., 2011).”
BackgroundMethodResultInfluential
Anticipatory feelings: Neural correlates and linguistic markers
Stefanova, E. D., Dubljević, O., Herbert, C., Fairfield, B., Schroeter, M. L., Stern, E. R., Urben, S., Derntl, B., Wiebking, C., Brown, C. S., et al. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.015 · Cited by 33
The ventral tegmental area as a putative target for tachykinins in cardiovascular regulation
Deschamps, K., & Couture, R. (2005) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706249 · Cited by 32
“The main neuronal dopaminergic projections of the mesocortical–mesolimbic system from the VTA are to the prefrontal cortex, the nucleus accumbens of the striatum and the amygdala (Swanson, 1982; Oades & Halliday, 1987).”
Background
The neuroanatomic complexity of the CRF and DA systems and their interface: What we still don’t know
Kelly, E. A., & Fudge, J. L. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.04.014 · Cited by 31
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Ventromedial mesencephalic tegmental (VMT) projections to ten functionally different cortical areas in the cat: Topography and quantitative analysis
Scheibner, T., & Törk, I. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902590206 · Cited by 32
Reduced prepulse inhibition in rats with entorhinal cortex lesions
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Amygdala Central Nucleus Function Is Necessary for Learning, but Not Expression, of Conditioned Auditory Orienting.
Groshek, F., Kerfoot, E. C., McKenna, V., Polackwich, A. S., Gallagher, M., & Holland, P. C. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.202 · Cited by 31
Influence of the Mesocortical/Prefrontal Dopamine Neurons on Their Target Cellsa
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The roles of midbrain and diencephalic dopamine cell groups in the regulation of cataplexy in narcoleptic Dobermans
Okura, M., Fujiki, N., Kita, I., Honda, K., Yoshida, Y., Mignot, E. J.-M., & Nishino, S. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.02.008 · Cited by 32
A lectin horseradish peroxidase study of the origin of ascending fibers in the medial forebrain bundle of the rat. The upper brainstem
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Authors: Swanson, L. W.
Affiliations: Salk Institute for Biological Studies (US)
Corresponding author: Swanson, L.W.
ORCID: Swanson, L.W.
Venue: Brain Research Bulletin
Publisher: Elsevier BV
Published: 1982-07
Volume: 9
Issue: 1-6
Pages: 321-353
ISSN: 0361-9230 (ISSN-L)
DOI: 10.1016/0361-9230(82)90145-9
OpenAlex: W1997065612
Cited by: 1,718
References: 114
Citations by year: 2026: 17 · 2025: 16 · 2024: 37 · 2023: 34 · 2022: 39 · 2021: 27 · 2020: 50 · 2019: 49 · 2018: 72 · 2017: 55 · 2016: 70 · 2015: 82 · 2014: 67 · 2013: 62 · 2012: 55
FWCI: 8.14
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Research Bulletin (publishedVersion)
PubMed (publishedVersion)
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 › Parkinson's Disease Mechanisms and Treatments
Keywords: ventral tegmental area, dopaminergic neurons, projection neurons, raphe nuclei, tuberomammillary nucleus, substantia nigra, nucleus accumbens, lateral habenula, locus coeruleus, parabrachial nucleus, lateral septum, amygdala, dorsal hippocampus, entorhinal area, A10 cells, collateral projections
MeSH terms: Animals, Axons, Brain Mapping, Dopamine, Efferent Pathways, Fluorescent Antibody Technique, Limbic System, Locus Coeruleus, Mammillary Bodies, Microscopy, Fluorescence, Neurons, Nucleus Accumbens, Periaqueductal Gray, Red Nucleus, Reticular Formation, Substantia Nigra, Tegmentum Mesencephali, Rats

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The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat

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