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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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Bunney, B. S., Chiodo, L. A., & Grace, A. A. (1991) · Synapse · doi:10.1002/syn.890090202 · Cited by 159
“In some cases, one neuron projects only to one area, such as those DA neurons that project to the prefrontal cortex, while in other cases the same DA neuron may project to two or more structures (Swanson, 1982).”
Background
Oxytocin receptors are expressed on dopamine and glutamate neurons in the mouse ventral tegmental area that project to nucleus accumbens and other mesolimbic targets
Peris, J., MacFadyen, K. A., Smith, J. A., de Kloet, A. D., Wang, L. A., & Krause, E. G. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24116 · Cited by 158
“The staining observed in the present study was identical to the example labeling provided by the manufacturer and matches The Journal of Comparative Neurology | Research in Systems Neuroscience 1097 published reports of TH staining in the VTA and substantia nigra (Swanson, 1982).”
Result
Brain-derived neurotrophic factor expression is increased in the rat amygdala, piriform cortex and hypothalamus following repeated amphetamine administration
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“The adult SVZ and dentate gyrus are innervated by dopaminergic fibers from the substantia nigra and ventral tegmental area in the midbrain, respectively (Swanson, 1982).”
Background
Ultrastructural features of dopamine axon terminals in the anteromedial and the suprarhinal cortex of adult rat
Séguéla, P., Watkins, K. C., & Descarries, L. (1988) · Brain Research · doi:10.1016/0006-8993(88)91427-8 · Cited by 155
Dopaminergic modulation of incentive motivation in adolescence: age-related changes in signaling, individual differences, and implications for the development of self-regulation
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“The VTA-to-NAcc (mesoaccumbens) projection is particularly relevant to this review given that the latter structure represents a core node for behavioral activation associated with incentive-reward motivation; it has been estimated that 75% of this projection is dopaminergic (Swanson, 1982).”
Background
The effects of 6-OHDA-induced dopamine depletions in the ventral or dorsal striatum on maternal and sexual behavior in the female rat
Hansen, S., Harthon, C., Wallin, E., Löfberg, L., & Svensson, K. A. (1991) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(91)90399-m · Cited by 156
The ability of the mesocortical dopamine system to operate in distinct temporal modes
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“The percentage was as high as 52.7% in the rostral linear nucleus (RLi) of the VTA which is a rostral midline nuclei projecting preferentially to PFC and limbic regions (Swanson 1982).”
BackgroundInfluential
Reward Modulation of Hippocampal Subfield Activation during Successful Associative Encoding and Retrieval
Wolosin, S. M., Zeithamová, D., & Preston, A. R. (2012) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00237 · Cited by 162
“Emerging evidence suggests that interactions between MTL regions and reward-sensitive dopaminergic midbrain (Luo, Tahsili-Fahadan, Wise, Lupica, & Aston-Jones, 2011; Gasbarri, Packard, Campana, & Pacitti, 1994b; Akil & Lewis, 1993; Swanson, 1982) play an important role in episodic memory formation.”
Background
Orexin axons in the rat ventral tegmental area synapse infrequently onto dopamine and γ‐aminobutyric acid neurons
Balcita‐Pedicino, J. J., & Sesack, S. R. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21420 · Cited by 150
“The smaller number of VTA neurons with cortical vs. striatal targets (Swanson, 1982) would be consistent with the low number of synapses observed in the present study.”
BackgroundResultInfluential
Exposure to nicotine and sensitization of nicotine-induced behaviors
Vezina, P., McGehee, D. S., & Green, W. N. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2007.08.038 · Cited by 153
Endocannabinoid Regulation of Reward and Reinforcement through Interaction with Dopamine and Endogenous Opioid Signaling
Wenzel, J. M., & Cheer, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.126 · Cited by 161
Structural basis of large-scale functional connectivity in the mouse
Grandjean, J., Zerbi, V., Balsters, J. H., Wenderoth, N., & Rudin, M. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.0438-17.2017 · Cited by 151
“Anterograde/retrograde neuronal viral tracer studies in animal models are not hindered by crossing fibers and are currently considered the gold standard for determining monosynaptic axonal pathways (Swanson, 1982; Oh et al., 2014; Zingg et al., 2014; Hintiryan et al., 2016).”
Background
Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area
Ikemoto, S., Qin, M., & Liu, Z.-H. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4542-05.2006 · Cited by 151
“The central linear nucleus raphé [or caudal linear nucleus of the raphé according to Paxinos and Watson (1997)] lies in the midline, at the posterior end of the A10 dopamine nucleus, and contains dopaminergic neurons projecting to the nucleus accumbens (Swanson, 1982).”
BackgroundMethodInfluential
A functional neuroanatomical investigation of the role of the medial preoptic area in neural circuits regulating maternal behavior
Stack, E. C., Balakrishnan, R., Numan, M. J., & Numan, M. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00370-9 · Cited by 151
Estrogen receptor‐β immunoreactivity in the midbrain of adult rats: Regional, subregional, and cellular localization in the A10, A9, and A8 dopamine cell groups
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“Within brain areas where the neurons projecting to anatomically and functionally distinct targets are notoriously intermingled (Fallon et al., 1978; Fallon and Moore, 1978; Swanson, 1982), the associations between ER immunoreactivity and cells of a particular appearance and/or neurochemistry established here may be co…”
BackgroundMethodInfluential
Segregated cholinergic transmission modulates dopamine neurons integrated in distinct functional circuits
Dautan, D., de Souza, A. S., Huerta-Ocampo, I., Valencia, M., Assous, M., Witten, I. B., Deisseroth, K. A., Tepper, J. M., Bolam, J. P., Gerdjikov, T. V., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4335 · Cited by 160
Localization of NADPH diaphorase activity in monoaminergic neurons of the rat brain
Johnson, M. D., & Ma, P. M. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903320402 · Cited by 149
Single dose of l -dopa makes extinction memories context-independent and prevents the return of fear
Haaker, J., Gaburro, S., Sah, A., Gartmann, N., Lonsdorf, T. B., Meier, K., Singewald, N., Pape, H.-C., Morellini, F., & Kalisch, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303061110 · Cited by 166
“Dopamine in the vmPFC probably derives from neurons originating in the ventral tegmental area (VTA) (41), and L-dopa enhances dopamine, but not noradrenaline, release in the frontal cortex (42).”
BackgroundInfluential
Anatomical Substrates of Hypothalamic Integration
Simerly, R. B. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50015-8 · Cited by 148
Connections of the parahippocampal cortex in the cat. II. Subcortical afferents
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Evaluation of reward from pain relief
Navratilova, E., Xie, J. Y., King, T. E., & Porreca, F. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12095 · Cited by 152
Retrograde degeneration of nigrostriatal neurons induced by intrastriatal 6-hydroxydopamine injection in rats
Berger, K., Przedborski, S., & Cadet, J. L. (1991) · Brain Research Bulletin · doi:10.1016/0361-9230(91)90242-c · Cited by 147
Comparative anatomy of the ventromedial mesencephalic tegmentum in the rat, cat, monkey and human
Halliday, G. M., & Törk, I. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902520402 · Cited by 147
Relevance of Norepinephrine–Dopamine Interactions in the Treatment of Major Depressive Disorder
Mansari, M. E., Guiard, B. P., Chernoloz, O., Ghanbari, R., Katz, N., & Blier, P. (2010) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00146.x · Cited by 153
“Although retrograde tracer studies showed few projections from ventral tegmental area (VTA) neurons to the locus coeruleus (LC) [14,15], dense expression of D2/3 mRNA and high density of binding sites using [(125)I]iodosulpiride have been documented [16–19].”
Method
Colocalization of calbindin D-28k, calretinin, and GABA immunoreactivities in neurons of the human temporal cortex
del R�o, M. R., & DeFelipe, J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960603)369:3 · Cited by 97
Light and electron microscopic immunocytochemical analysis of the noradrenaline innervation of the rat visual cortex
Papadopoulos, G. C., Parnavelas, J. G., & Buijs, R. M. (1989) · Journal of Neurocytology · doi:10.1007/bf01188418 · Cited by 146
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Long-range projection neurons of the mouse ventral tegmental area: a single-cell axon tracing analysis
Aransay, A., Rodríguez-López, C., García‐Amado, M., Clascá, F., & Prensa, L. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00059 · Cited by 153
“…et al., 1977; Fallon and Moore, 1978; Beckstead et al., 1979; Fallon, 1981; Albanese and Bentivoglio, 1982; Porrino and Goldman-Rakic, 1982; Swanson, 1982; Oades and Halliday, 1987; Le Moal and Simon, 1991; Gaykema and Zaborszky, 1996, 1997; Carr and Sesack, 2000; Yamaguchi et al., 2011;…”
Background
Functional Mapping of the Neural Circuitry of Rat Maternal Motivation: Effects of Site‐Specific Transient Neural Inactivation
Pereira, M., & Morrell, J. I. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02200.x · Cited by 146
New perspectives on catecholaminergic regulation of executive circuits: evidence for independent modulation of prefrontal functions by midbrain dopaminergic and noradrenergic neurons
Chandler, D. J., Waterhouse, B. D., & Gao, W. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00053 · Cited by 143
Dopamine and glutamate regulate striatal acetylcholine in decision-making
Chantranupong, L., Beron, C. C., Zimmer, J. A., Wen, M. J., Wang, W., & Sabatini, B. L. (2023) · Nature · doi:10.1038/s41586-023-06492-9 · Cited by 153
Interactions between neuropeptides and dopamine neurons in the ventromedial mesencephalon
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Music therapy for posttraumatic stress in adults: A theoretical review.
Landis-Shack, N., Heinz, A. J., & Bonn-Miller, M. O. (2017) · Psychomusicology: Music, Mind, and Brain · doi:10.1037/pmu0000192 · Cited by 144
“…fMRI neuroimaging studies have found that music increases the cerebral blood flow to areas of the brain associated with reward and reinforcement of pleasurable behaviors (e.g., the nucleus accumbens and ventral tegmental area; Goldstein, 1980; Menon & Levitin, 2005; Swanson, 1982; Wise, 2004).”
BackgroundInfluential
Glutamatergic synaptic plasticity in the mesocorticolimbic system in addiction
van Huijstee, A. N., & Mansvelder, H. D. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00466 · Cited by 158
“The mesocorticolimbic system consists of the ventral tegmental area (VTA) and the brain regions that are innervated by projections from the VTA, such as the nucleus accumbens (NAc), the prefrontal cortex (PFC), the amygdala, and the hippocampus (Swanson, 1982).”
BackgroundInfluential
The dopaminergic innervation of the avian telencephalon
Durstewitz, D., Kröner, S., & Güntürkün, O. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00100-2 · Cited by 152
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Autoradiographic localization of μ-opioid and neurotensin receptors within the mesolimbic dopamine system
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“The DA neurons giving rise to the mesocorticolimbic system reside in the A10 region of the ventral midbrain, which comprises two major nuclei of the VTA, the parabrachial pigmented (PBP) nucleus and paranigral nucleus (PN), and three midline nuclei, the caudal linear nucleus (CLi), interfascicular nucleus (IF), and ro…”
Prelimbic to Accumbens Core Pathway Is Recruited in a Dopamine-Dependent Manner to Drive Cued Reinstatement of Cocaine Seeking
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“However, VTA is likely a major source of dopamine in PL, as PL receives dopaminergic input from fibers originating from the A10 group (Swanson, 1982), and VTA dopamine neurons are activated by food or drug-related Pavlovian cues (Yun et al.”
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Glutamatergic and dopaminergic neurons in the mouse ventral tegmental area
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“Because the TH neurons located within the anteromedial VTA provide TH-containing fibers to the LHb in the rat (Swanson, 1982), and because the TH mRNA (+)/TH-IR ( ) neurons in the mouse are in the anteromedial VTA, we determined whether mesohabenular fibers expressing mCherry under the TH promoter…”
BackgroundMethodInfluential
α-Adrenoceptor modulation hypothesis of antipsychotic atypicality
Svensson, T. H. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2003.09.009 · Cited by 143

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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