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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
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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“All known drugs of abuse cause DA release in the nucleus accumbens (NAC), preferentially in the nucleus accumbens shell region (NACs), and also more broadly throughout the mesolimbic DA pathway (Swanson 1982; Di Chiara and Imperato 1988; Koob and Bloom 1988; Pontieri et al 1995; Pontieri et al 1996; Tanda et al 1997; for a review, see Di Chiara et al 2004).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Swanson 1982
In the citing paper
“Consistent with previous reports, eYFP expression in DRN DA somata resulted in terminal expression in several regions including the medial prefrontal cortex (mPFC), bed nucleus of the stria terminalis (BNST), lateral hypothalamus, central amygdala (CeA), entorhinal cortex, and basolateral amygdala (Hasue and Shammah-Lagnado, 2002, Meloni et al., 2006, Swanson, 1982, Yoshida et al., 1989).”
From Dorsal raphe dopamine neurons represent the experience of social isolation (2016) · cites this paper as Swanson, 1982
In the citing paper
“The VTA has been defined in several different ways. There are two popular versions, differing in their inclusion or exclusion of the midline nuclei.”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Swanson, 1982
In the citing paper
“Interestingly, this midline structure contains both dopaminergic (Phillipson, 1979b; Swanson, 1982) and serotonergic (Steinbusch, 1981; Halliday and Tork, 1989) neurons.”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Swanson, 1982
In the citing paper
“These values of co-localization are slightly higher than the 85% value for the VTA TH neurons projecting to the nucleus provided by Swanson (1982), although within the same range with 95% or higher values for the dopaminergic cells projecting to the dorsal striatum (van der Kooy et al., 1981).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Swanson (1982)
In the citing paper
“First, the present experiment utilized small injections confined in small areas within the ventral striatum, while Swanson used large injections affecting the entire nucleus accumbens, which may have affected sites outside of the nucleus such as the diagonal band.”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Swanson (1982)
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“(A) Schematic drawing shows a flatmap adopted andmodified from the one by Swanson (2004). (B–F) Afferents to the”
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Bidirectional Regulation of DARPP-32 Phosphorylation by Dopamine
Nishi, A., Snyder, G. L., & Greengard, P. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08147.1997 · Cited by 420
“The nucleus accumbens is a target for mesolimbic dopaminergic projections (Swanson, 1982) that has been implicated in the genesis of psychotic symptoms (Davis et al.”
BackgroundDonoghue, J. P., & Herkenham, M. A. (1986) · Brain Research · doi:10.1016/0006-8993(86)91658-6 · Cited by 418
The ins and outs of the striatum: Role in drug addiction
Yager, L. M., Garcia, A. F., Wunsch, A. M., & Ferguson, S. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.06.033 · Cited by 467
“Both the NAc and the dorsal striatum receive dense innervation from midbrain dopamine neurons, and these inputs have long been implicated in addictive behaviors (Swanson, 1982; Robinson and Berridge, 1993; Berke and Hyman, 2000; Everitt and Robbins, 2005; Gerfen and Surmeier, 2011).”
Dorsal raphe dopamine neurons represent the experience of social isolation
Matthews, G. A., Nieh, E. H., Vander Weele, C. M., Halbert, S. A., Pradhan, R. V., Yosafat, A. S., Glober, G. F., Izadmehr, E. M., Thomas, R. E., Lacy, G. D., et al. (2016) · Cell · doi:10.1016/j.cell.2015.12.040 · Cited by 402
“…in several regions including the medial prefrontal cortex (mPFC), bed nucleus of the stria terminalis (BNST), lateral hypothalamus, central amygdala (CeA), entorhinal cortex, and basolateral amygdala (Hasue and Shammah-Lagnado, 2002; Meloni et al., 2006; Swanson, 1982; Yoshida et al., 1989).”
BackgroundResultNeuhoff, H., Neu, A. D., Liss, B., & Roeper, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-04-01290.2002 · Cited by 400
“associated with limbic and cognitive functions (Swanson, 1982; Oades and Halliday, 1987; Carr and Sesack, 2000b).”
BackgroundElectrophysiological Characterization of GABAergic Neurons in the Ventral Tegmental Area
Steffensen, S. C., Svingos, A. L., Pickel, V. M., & Henriksen, S. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-19-08003.1998 · Cited by 388
“The anatomical projections of DA neurons in the substantia nigra pars compacta (SNc; nucleus A9) and adjacent VTA (nucleus A10) have been carefully examined (Fallon and Moore, 1978; Beckstead et al., 1979; Swanson, 1982).”
BackgroundRosenkranz, J., & Grace, A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00324.2002 · Cited by 422
“In addition, the BLA has a large number of highly collateralizing inhibitory interneurons (McDonald, 1982, 1985; McDonald and Betette, 2001) that respond potently to mPFC stimulation (Rosenkranz and Grace, 2001), and these intrinsic GABAergic inputs would presumably overwhelm a much more sparse GABAergic input from th…”
BackgroundInfluentialEstrogen Shapes Dopamine-Dependent Cognitive Processes: Implications for Women's Health
Jacobs, E., & D'Esposito, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.6394-10.2011 · Cited by 342
“socortical pathway were dopaminergic (TH-immunoreactive) (Swanson, 1982).”
Dopamine Prediction Errors in Reward Learning and Addiction: From Theory to Neural Circuitry
Keiflin, R., & Janak, P. H. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.037 · Cited by 401
“Midbrain DA neurons send efferent projections to many brain regions including the striatum, globus pallidus/ ventral pallidum, subthalamic nucleus, thalamus, amygdala, BNST, prefrontal cortex, amygdala, and hippocampus (Beckstead et al., 1979; Gerfen et al., 1987; Swanson, 1982).”
BackgroundBaskerville, T. A., & Douglas, A. J. (2010) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00154.x · Cited by 377
“In addition to the NA [84], the VTA also supplies dopaminergic fibers to the hippocampus and amygdala [85] suggesting that dopamine–oxytocin interactions within these nuclei may also have a bi-directional role.”
BackgroundAfferents 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
“Furthermore, the VTA consists of -aminobutyric acid (GABA)ergic and dopaminergic projection neurons (Swanson, 1982), some of which contain the peptidergic cotransmitters neurotensin and cholecystokinin (Seroogy et al., 1988).”
BackgroundDopaminergic Projections from Midbrain to Primary Motor Cortex Mediate Motor Skill Learning
Hosp, J. A., Pekanovic, A., Rioult-Pedotti, M. S., & Luft, A. R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5411-10.2011 · Cited by 354
“VTA dopaminergic neurons project to many areas of cortex (Lindvall et al., 1974; Albanese and Bentivoglio, 1982; Swanson, 1982; Descarries et al., 1987; Pirot et al., 1992; Ikemoto, 2007).”
BackgroundDopamine neurons create Pavlovian conditioned stimuli with circuit-defined motivational properties
Saunders, B. T., Richard, J. M., Margolis, E. B., & Janak, P. H. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0191-4 · Cited by 393
Hervé, D., Pickel, V. M., JOH, T. H., & Beaudet, A. (1987) · Brain Research · doi:10.1016/0006-8993(87)91588-5 · Cited by 372
Jones, B. E., & Cuello, A. C. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90029-8 · Cited by 369
Glutamatergic neurons are present in the rat ventral tegmental area
Yamaguchi, T., Sheen, W., & Morales, M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05263.x · Cited by 367
“VTA glutamatergic neurons as projection neurons A detailed anatomical study by Swanson (1982) establishes that a large number of nondopaminergic VTA cells usually project to the same terminal fields as DAergic neurons.”
BackgroundAnatomical Substrates for Glutamate‐Dopamine Interactions
Sesack, S. R., CARR, D. B., Omelchenko, N., & Pinto, A. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.066 · Cited by 372
Stamatakis, A. M., Jennings, J. H., Ung, R. L., Blair, G. A., Weinberg, R. J., Neve, R. L., Boyce, F., Mattis, J., Ramakrishnan, C., Deisseroth, K., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.023 · Cited by 364
“Previous studies have demonstrated that separate popula- tions of VTA dopaminergic neurons project to nonoverlapping target structures such as the NAc, BLA, and mPFC (Ford et al., 2006; Lammel et al., 2008; Swanson, 1982).”
BackgroundInfluentialModel-based and model-free Pavlovian reward learning: Revaluation, revision, and revelation
Dayan, P., & Berridge, K. C. (2014) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-014-0277-8 · Cited by 357
“…to the ventral pallidum and to them from the amygdala, as well as with other subcortical nuclei, such as the lateral habenula and rostromedial tegmental nucleus (RMTg) and the serotonergic raphe nucleus, and also pathways linking them to the hypothalamus (Moore & Bloom, 1978; Swanson, 1982).”
BackgroundNuman, M., & Stolzenberg, D. S. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.10.002 · Cited by 361
Diversity of Transgenic Mouse Models for Selective Targeting of Midbrain Dopamine Neurons
Lammel, S., Steinberg, E. E., Földy, C., Wall, N. R., Beier, K. T., Luo, L., & Malenka, R. C. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.036 · Cited by 359
“Consistent with previous reports (Gruber et al., 2007; Skagerberg et al., 1984; Stamatakis et al., 2013; Swanson, 1982), retrogradely labeled neurons were predominately located in midline VTA nuclei of the anterior and posterior midbrain.”
Bouthenet, M.-L., Martres, M., Salès, N., & Schwartz, J. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90008-x · Cited by 356
Afferents to the GABAergic tail of the ventral tegmental area in the rat
Kaufling, J., Veinante, P., Pawlowski, S. A., Freund‐Mercier, M., & Barrot, M. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21983 · Cited by 347
“The dopaminergic projection from the VTA to the nucleus accumbens (Acb) and prefrontal cortex (PFC), known as the mesolimbic projection, is widely studied in the context of drug abuse and other motivated behaviors (Robbins and Everitt, 1996; Chao and Nestler, 2004).”
BackgroundInfluentialDeutch, A. Y., Tam, S., & Roth, R. H. (1985) · Brain Research · doi:10.1016/0006-8993(85)90134-9 · Cited by 354
Kalivas, P. W., Churchill, L., & Klitenick, M. A. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90048-k · Cited by 353
Single rodent mesohabenular axons release glutamate and GABA
Root, D. H., Mejias-Aponte, C. A., Zhang, S., Wang, H.-L., Hoffman, A. F., Lupica, C. R., & Morales, M. (2014) · Nature Neuroscience · doi:10.1038/nn.3823 · Cited by 349
Chou, Y.-H., Halldin, C., & Farde, L. (2000) · Synapse · doi:10.1002/1098-2396(200011)38:2 · Cited by 57
Phenotypical characterization of neurons expressing the dopamine D3 receptor in the rat brain
Díaz, J., Lévesque, D., Lammers, C.-H., Griffon, N., Martres, M., Schwartz, J., & Sokoloff, P. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00527-c · Cited by 352
Ford, B., Holmes, C. J., Mainville, L., & Jones, B. E. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903630203 · Cited by 344
Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location
Ford, C. P., Mark, G. P., & Williams, J. T. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4331-05.2006 · Cited by 339
“This contrasts with previous anatomical studies in the rat, which identified a substantial proportion of non-DAergic cells that send projections to these target areas (Swanson, 1982).”
ResultWitter, M. P., & Amaral, D. G. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50022-5 · Cited by 361
Regional and laminar density of the dopamine innervation in adult rat cerebral cortex
Descarries, L., Lemay, B., Doucet, G., & Berger, B. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90038-8 · Cited by 341
Swanson, L. W., & Köhler, C. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-10-03010.1986 · Cited by 340
“…inputs from the medial forebrain bundle, it seems likely that cells in these regions may also relay a broad variety of information to the lateral entorhinal area that is perhaps related to attention or arousal (see Haglund et al., 1984; Kijhler et al., 1984; Swanson, 1982; Swanson and Cowan, 1979).”
BackgroundSelf-citationPavlovian to instrumental transfer: a neurobehavioural perspective.
Holmes, N. M., Marchand, A., & Coutureau, E. (2010) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.03.007 · Cited by 327
Mesocorticolimbic Glutamatergic Pathway
Yamaguchi, T., Wang, H.-L., Li, X., Ng, T. H., & Morales, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1598-11.2011 · Cited by 332
“…further support the view of neurochemical and functional differences between the lateral and medial aspects of the A10 region and strengthen the proposition that the PN and the PBP are regions of the VTA that, together with the RLi, the CLi, and the IF, comprise the A10 region (Swanson, 1982).”
BackgroundMethodInfluential
Metadata
- 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)
- 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
- 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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