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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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Dopamine, the prefrontal cortex and schizophrenia
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“amygdala, nucleus accumbens, tuberculum olfactorium) limbic regions originate mainly from separate pools of neurons within the VTA (Deniau et al., 1980; Fallon, 1981; Swanson, 1982).”
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BackgroundResultVentral Tegmental Area Glutamate Neurons: Electrophysiological Properties and Projections
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“However, these properties are not unique to VTA dopamine neurons (Margolis et al., 2006, 2008; Lammel et al., 2008), which comprise only 55% of cells in the rat VTA (Swanson, 1982; Margolis et al., 2006; Nair-Roberts et al., 2008).”
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“Such local signaling is likely to regulate the DAergic and non-DAergic neurotransmission to VTA target structures (Swanson, 1982; Fallon et al., 1984; Van Bockstaele and Pickel, 1995; Carr and Sesack, 2000; Margolis et al., 2006).”
BackgroundPreferential stimulation of ventral tegmental area dopaminergic neurons by nicotine
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“Anatomical, cell-biological, and neuropharmacological data have indicated a VTA projection to the HPC, the presence of DA in the dorsal HPC, and the presence of metabotropic D1 receptors whose activation can lead to transcriptional regulation of plasticity-related genes such as the cAMP response element-binding protei…”
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“AMY amygdala, BNST bed nucleus of the stria terminalis, DA dopamine, DRN dorsal raphe nucleus, HIP hippocampus, KOR kappa-opioid receptor, PFC prefrontal cortex, NAc nucleus accumbens, VTA ventral tegmental area Psychopharmacology (2013) 229:435–452 441 aversions (Bals-Kubik et al. 1993) whereas intra-PFC KOR antagoni…”
InfluentialMidbrain dopaminergic neurons (nuclei A8, A9, and A10): Three‐dimensional reconstruction in the rat
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Self-citationThe cytoarchitecture, histochemistry and projections of the tuberomammillary nucleus in the rat
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Self-citationDopaminergic and glutamatergic microdomains in a subset of rodent mesoaccumbens axons
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“…preferentially comes from our observation that these synapses were detected more frequently onto mesoprefrontal versus mesoaccumbens neurons, as the former cell group includes a substantially larger proportion of GABA neurons (Swanson, 1982; Van Bockstaele and Pickel, 1995; Carr and Sesack, 2000a).”
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A role for nucleus accumbens glutamate transmission in the relapse to cocaine-seeking behavior
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“Dopamine (DA) neurons in the VTA and RRF give rise to the mesolimbic DA system, which ascends to the telencephalon, with a major projection to the nucleus accumbens (NA; Deutch, Goldstein, Baldino, & Roth, 1988; Pennartz, Groenewegen, & Lopes Da Silva, 1994; Swanson, 1982).”
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“Thus, the elements necessary for functional DA transmission have been shown to be present in the BLA (Swanson, 1982; Loughlin and Fallon, 1983; Scibilia et al., 1992; Revay et al., 1996; Asan, 1997).”
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Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memoryPreprint
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“The hippocampus receives dopaminergic projections from mesolimbic structures such as the ventral tegmental area (VTA) and substantia nigra (Carter and Fibiger 1977; Scatton et al. 1980; Swanson 1982; Gasbarri et al. 1994a,b).”
BackgroundCalculating utility: preclinical evidence for cost–benefit analysis by mesolimbic dopamine
Phillips, P. E. M., Walton, M. E., & Jhou, T. C. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0626-6 · Cited by 237
“It is important to note that dopaminergic projections to the nucleus accumbens, prefrontal cortex and other areas such as the amygdala are anatomically and functionally distinct, arising from separate subsets of dopamine neurons (Swanson 1982; Bassareo et al. 1996; Ford et al. 2006; Margolis et al. 2006).”
BackgroundSelective prefrontal cortex inputs to dopamine cells: implications for schizophrenia
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“In contrast, only 60% of VTA neurons are DAergic (Swanson, 1982; Margolis et al., 2006b; Nair-Roberts et al., 2008),”
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“DA cells constitute approximately 45–65% of the VTA population, depending on the subdivision (Swanson, 1982; McCormack et al., 2006; Nair-Roberts et al., 2008).”
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“%) of non-DA neurons (Swanson, 1982), and subsequent work has demonstrated that only 13% of these non-DA neurons also show I h (Cameron et al., 1997).”
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The supramammillary area: its organization, functions and relationship to the hippocampus
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“…limbic cortex, amygdala, entorhinal cortex, dentate gyrus, septum, preoptic area, anterior hypothalamus, LH, thalamus, locus coeruleus, DR and MR (Swanson, 1976, 1982; Shibata, 1987; Vertes, 1992; Hayakawa et al., 1993; Thinschmidt, 1993; Risold and Swanson, 1997; Vertes et al., 1999; Swanson…”
BackgroundResultInfluentialDifferential roles of medial prefrontal subregions in the regulation of drug seeking
Moorman, D. E., James, M. H., McGlinchey, E. M., & Aston‐Jones, G. (2014) · Brain Research · doi:10.1016/j.brainres.2014.12.024 · Cited by 230
“Rat mPFC receives dopaminergic input from fibers originating from the A10 group within the ventral tegmental area (Swanson, 1982), as well as from various limbic and sensory regions, including amygdala and hippocampus (Hoover and Vertes, 2007).”
BackgroundCell-type-specific expression of catecholamine transporters in the rat brain
Lorang, D., Amara, S. G., & Simerly, R. B. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-08-04903.1994 · Cited by 223
Smeltzer, M. D., Curtis, J. T., Aragona, B. J., & Wang, Z. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.10.019 · Cited by 222
See, R. E., Kruzich, P. J., & Grimm, J. W. (2001) · Psychopharmacology · doi:10.1007/s002130000636 · Cited by 224
“The BLA receives dopaminergic input from mesencephalic neurons ( Swanson 1982; Brinley-Reed and McDonald 1999), which have been extensively implicated in drug reinforcement (Koob 1992).”
BackgroundDeutch, A. Y. (1992) · Springer eBooks · doi:10.1007/978-3-7091-9211-5_5 · Cited by 221
Glutamate neurons within the midbrain dopamine regions
Morales, M., & Root, D. H. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.032 · Cited by 218
“Because VTA projections rarely collateralize (Fallon, 1981; Swanson, 1982; Albanese and Minciacchi, 1983), we suggest that the nAcc is a preferential target of the VGluT2-TH neurons.”
BackgroundConnections of the nucleus incertus
Goto, M., Swanson, L. W., & Canteras, N. S. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1303 · Cited by 219
“…and posterior hypothalamic nuclei, the medial septal nucleus and nucleus of the diagonal band, and the dorsal and ventral tegmental nuclei (Swanson, 1982; Haglund et al., 1984; Taube, 1988; Vertes, 1992; Vertes et al., 1995; Vertes and Kocsis, 1997; Oddie and Bland, 1998; Sharp and Cho,…”
BackgroundSelf-citationThe dopamine mesocorticolimbic pathway is affected by deficiency in n−3 polyunsaturated fatty acids
Zimmer, L., Vancassel, S., Cantagrel, S., Breton, P., Delamanche, S., Guilloteau, D., Durand, G., & Chalon, S. (2002) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/75.4.662 · Cited by 218
Nucleus Accumbens Medium Spiny Neurons Target Non-Dopaminergic Neurons in the Ventral Tegmental Area
Xia, Y., Driscoll, J. R., Wilbrecht, L., Margolis, E. B., Fields, H. L., & Hjelmstad, G. O. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1504-11.2011 · Cited by 218
Blaha, C. D., Allen, L., Das, S., Inglis, W. L., LATIMER, M. L., Vincent, S., & Winn, P. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00714.1996 · Cited by 223
“Several studies have suggested the existence of a crossed VTA-accumbens pathway (Swanson, 1982; Bjiirklund and Lindvall , 1986).”
kappa-Opioid receptor signaling and brain reward function
Bruijnzeel, A. W. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.09.008 · Cited by 214
The entorhinal cortex of the monkey: III. Subcortical afferents
Insausti, R., Amaral, D. G., & Cowan, W. M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902640307 · Cited by 214
Ventral tegmental area glutamate neurons co-release GABA and promote positive reinforcement
Yoo, J. H., Zell, V., Gutierrez-Reed, N. A., Wu, J., Ressler, R. L., Shenasa, M. A., Johnson, A. B., Fife, K. H., Faget, L. C., & Hnasko, T. S. (2016) · Nature Communications · doi:10.1038/ncomms13697 · Cited by 223
Cearley, C. N., & Wolfe, J. H. N. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2185-07.2007 · Cited by 220
GABAergic and glutamatergic efferents of the mouse ventral tegmental area
Taylor, S. R., Badurek, S., Dileone, R., Nashmi, R., Minichiello, L., & Picciotto, M. R. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23603 · Cited by 226
“Infusion of AAV-Ef1a-DIO-mCherry permits visualization of Creexpressing cells in the ventral tegmental area (VTA; A,E).”
BackgroundResultInfluentialIkai, Y., Takada, M., Shinonaga, Y., & Mizuno, N. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90310-x · Cited by 210
Camps, M., Kelly, P. H., & Palacios, J. M. (1990) · Journal of Neural Transmission · doi:10.1007/bf01257077 · Cited by 210
“However, the injection of retrograde tracers into rat cerebellum failed to demonstrate any dopaminergic projection arising in the mesencephalon (Swanson, 1982).”
BackgroundInteractions between dopamine and amino acid-induced excitation and inhibition in the striatum
Chiodo, L. A., & Berger, T. W. (1986) · Brain Research · doi:10.1016/0006-8993(86)90976-5 · Cited by 210
Telencephalic Projections of the A8 Dopamine Cell Group
Deutch, A. Y., Goldstein, M., Baldino, F., & Roth, R. H. (1988) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1988.tb42095.x · Cited by 205
Louilot, A., Moal, M. L., & Simon, H. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90331-x · Cited by 209
Swerdlow, N. R., & Koob, G. F. (1987) · Brain Research · doi:10.1016/0006-8993(87)91129-2 · Cited by 208
Brainstem afferents to the basal forebrain in the rat
Vertes, R. P. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90077-2 · Cited by 205
Supramammillary glutamate neurons are a key node of the arousal system
Pedersen, N. P., Ferrari, L., Venner, A., Wang, J. L., Abbott, S. B. G., Vujovic, N., Arrigoni, E., Saper, C. B., & Fuller, P. M. (2017) · Nature Communications · doi:10.1038/s41467-017-01004-6 · Cited by 203
Anderson, S. M., & Pierce, R. C. (2005) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2004.12.004 · Cited by 212
Laviolette, S. R., Gallegos, R. A., Henriksen, S. J., & van der Kooy, D. (2004) · Nature Neuroscience · doi:10.1038/nn1182 · Cited by 203
“Perestroika” in the basal forebrain: Opening the border between neurology and psychiatry
Heimer, L., de Olmos, J. S., Alheid, G. F., & Záborszky, L. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63050-2 · Cited by 203
Bechara, A., & van der Kooy, D. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-10-03400.1989 · Cited by 204
“…evidence indicates that the TPP region of the midbrain and pons receives neuronal inputs from all of these structures identified as positive reward sites, via direct monosynaptic or indirect multisynaptic pathways (Nauta et al., 1978; Saper et al., 1979; Swanson, 1982; Swanson et al., 1984, 1987).”
BackgroundWhite, F. J., & Wang, R. Y. (1984) · Life Sciences · doi:10.1016/0024-3205(84)90088-2 · Cited by 200
A SELECTIONIST APPROACH TO REINFORCEMENT
Donahoe, J. W., Burgos, J. E., & Palmer, D. C. (1993) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1993.60-17 · Cited by 203
Glucocorticoids, chronic stress, and obesity
Dallman, M. F., Pecoraro, N. C., La Fleur, S. E., Warne, J. P., Ginsberg, A. B., Akana, S. F., Laugero, K. C., Houshyar, H., Strack, A. M., Bhatnagar, S., et al. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)53004-3 · Cited by 198
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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