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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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“…apparent medially, dorsal to the mammilary peduncle; this area of the VTA, together with immediately adjacent regions such as the supramamillary nucleus, is known to contain significant numbers of TH-containing neurons from the A10 (mesolimbic) cell group (Dahlstrom and Fuxe, 1964; Swanson, 1982).”
BackgroundMultiplexed neurochemical signaling by neurons of the ventral tegmental area
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“We provide evidence that GLP-1R-positive cells in the dLS are predominantly GABAergic and it is known that LS projections terminate in the VTA and NAc (Onteniente et al, 1987; Risold and Swanson, 1997b; Swanson, 1982).”
BackgroundNociceptin/orphanin FQ and opioid receptor‐like receptor mRNA expression in dopamine systems
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“The projection from the VTA to the hippocampus is 82–94% nondopaminergic (Swanson, 1982; Gasbarri et al., 1994).”
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“Another well-described input to the SUM originates in the nucleus incertus (NI) and targets differently the SUMl and SUMm such that the NI compact part sends a prominent input to the SUMm and sparse input to the SUMl, whereas for the NI diffuse part the opposite is true (Goto et al., 2001); the NI also sends a promine…”
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“In rodents, although only a small percentage of its VTA-derived afferents seem to be dopaminergic [109], DA receptors mainly of the D2-like subtype have been identified in this brain area [110].”
BackgroundBoth Kappa and Mu Opioid Agonists Inhibit Glutamatergic Input to Ventral Tegmental Area Neurons
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“…major glutamate input to the non-dopaminergic neurons that comprise 60% of the VTA projection to the mPFC, the dopaminergic neurons that comprise 80% of the VTA projection to the NAc, and possibly the VTA neurons that project to other targets such as the amygdala and hippocampus (Swanson 1982).”
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“Consideration of retrograde tracing exclusively, however, provides a potentially misleading picture of inputs to a CNS structure.”
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Lohani, S., Poplawsky, A. J., Kim, S.-G., & Moghaddam, B. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.102 · Cited by 89
“The ROIs were chosen based on known output regions of VTA dopamine neurons 6, 35–38 and observed signal changes in group activation maps.”
Meredith, G. E., Farrell, T., Kellaghan, P., Tan, Y., Zahm, D. S., & Totterdell, S. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00774.x · Cited by 89
Habitual alcohol seeking: Modeling the transition from casual drinking to addiction
Barker, J. M., & Taylor, J. R. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.08.012 · Cited by 89
Amygdala Kisspeptin Neurons: Putative Mediators of Olfactory Control of the Gonadotropic Axis
Pineda, R., Plaisier, F., Millar, R. P., & Ludwig, M. (2016) · Neuroendocrinology · doi:10.1159/000445895 · Cited by 90
The Dopamine Prediction Error: Contributions to Associative Models of Reward Learning
Nasser, H. M., Calu, D. J., Schoenbaum, G. M., & Sharpe, M. J. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00244 · Cited by 97
“A sub-nucleus of the amygdala complex, the BLA, is a region that receives extensive dopaminergic input from midbrain dopamine neurons (Swanson, 1982) and shows increases in neural activity when an unexpected event occurs whether it is rewarding or aversive (Belova et al., 2007, 2008; Herry et al.,…”
BackgroundVTA-projecting cerebellar neurons mediate stress-dependent depression-like behaviors
Baek, S. J., Park, J., Kim, J., Yamamoto, Y., & Tanaka, K. (2022) · eLife · doi:10.7554/elife.72981 · Cited by 97
Shigemune, Y., Tsukiura, T., Kambara, T., & Kawashima, R. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs415 · Cited by 99
Borowski, T. B., & Kokkinidis, L. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.6.1349 · Cited by 88
Wood, J., & Ahmari, S. E. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00171 · Cited by 85
“Approximately two thirds of the neurons in the VTA are dopaminergic, and the majority of the remaining neurons are GABAergic (Swanson, 1982; Nair-Roberts et al., 2008; Sesack and Grace, 2010).”
BackgroundInfluentialOnaolapo, A. Y., & Onaolapo, O. J. (2018) · Pathophysiology · doi:10.1016/j.pathophys.2018.04.002 · Cited by 102
Glutamate neurons in the substantia nigra compacta and retrorubral field
Yamaguchi, T., Wang, H., & Morales, M. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12359 · Cited by 87
“It has long been known that RRF dopaminergic neurons project to the dorsal striatum, olfactory tubercle, amygdala, nucleus of the stria terminalis, and piriform and enthorhinal cortex (Swanson, 1982; Deutch et al., 1988).”
BackgroundNuman, M., Stolzenberg, D. S., Dellevigne, A. A., Correnti, C. M., & Numan, M. J. (2009) · Behavioral Neuroscience · doi:10.1037/a0016204 · Cited by 86
Vogel, H., Wolf, S., Rabasa, C., Rodriguez-Pacheco, F., Babaei, C. S., Stöber, F., Goldschmidt, J., DiMarchi, R. D., Finan, B., Tschöp, M. H., et al. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.07.039 · Cited by 86
Park, J., Aragona, B. J., Kile, B. M., Carelli, R. M., & Wightman, R. M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.076 · Cited by 86
“…consistent with previous immunohistochemistry studies have shown that noradrenergic neurons innervate the caudal NAc shell to a greater degree than the rostral region (Delfs et al. 1998), whereas dopaminergic neurons originating in the VTA project to both subregions (Ikemoto 2007; Swanson 1982).”
ResultMihailoff, G. A., Kosinski, R. J., Azizi, S. A., & Border, B. G. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902820411 · Cited by 86
Fassio, A., Evans, G., Grisshammer, R., Bolam, J. P., Mimmack, M. L., & Emson, P. C. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(00)00060-5 · Cited by 86
Anatomical Relationships Between the Prefrontal Cortex and the Basal Ganglia in the Rat
Groenewegen, H. J., & Berendse, H. W. (1994) · Research and perspectives in neurosciences · doi:10.1007/978-3-642-85007-3_4 · Cited by 86
Mayer, U., Salva, O. R., & Vallortígara, G. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.031 · Cited by 81
“terminalis (BNST), the medial amygdala [7–9] and dopaminergic projections from the ventral tegmental area (VTA) [10].”
BackgroundOrganization of afferents to the orbitofrontal cortex in the rat
Murphy, M. J. M., & Deutch, A. Y. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24424 · Cited by 85
“Our findings are consistent with the early studies of Fallon and colleagues (Fallon, 1981; Loughlin & Fallon, 1984) and Swanson (1982), who noted that there is little collateralization of VTA neurons to innervate more than one forebrain target in the rodent.”
BackgroundResultFunctional neuroanatomical review of the ventral tegmental area
Trutti, A. C., Mulder, M., Hommel, B., & Forstmann, B. U. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.01.062 · Cited by 97
Modulation of singing‐related activity in the songbird ventral tegmental area by social context
Yanagihara, S., & Hessler, N. A. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05228.x · Cited by 96
“However, in mammals, some GABAergic neurons with shortduration action potentials do project to the cortex or striatum (Swanson, 1982; Van Bockstaele & Pickel, 1995; Steffensen et al., 1998; Carr & Sesack, 2000; Gonzalez-Hernandez et al., 2001).”
BackgroundGruber, C., Kahl, A., Lebenheim, L., Kowski, A. B., Dittgen, A., & Veh, R. W. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.09.016 · Cited by 85
Prominent Activation of Brainstem and Pallidal Afferents of the Ventral Tegmental Area by Cocaine
Geisler, S., Marinelli, M., DeGarmo, B., Becker, M. L., Freiman, A. J., Beales, M., Meredith, G. E., & Zahm, D. S. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301650 · Cited by 87
Kappa Opioid Inhibition of Somatodendritic Dopamine Inhibitory Postsynaptic Currents
Ford, C., Beckstead, M. J., & Williams, J. T. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00963.2006 · Cited by 84
“I N T R O D U C T I O N Dopamine neurons of the ventral tegmental area (VTA) and substantia nigra compacta (SNc) project to target areas, including the basal ganglia, striatum, nucleus accumbens (NAc), and prefrontal cortex (Albanese and Minciacchi 1983; Swanson 1982).”
BackgroundMartin, P. D., & Ono, T. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00249-7 · Cited by 84
Holland, P. C., & Gallagher, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0390-06.2006 · Cited by 85
“The data of Lee et al. (2005a) suggest that this system for controlling the associability of cues may gain access to prediction error information through its connections with the SNc, which innervates both the CeA (Swanson, 1982) and SI/nBm (Hasue and Shammah-Lagnado, 2002).”
BackgroundSchizophrenia: a disease of interhemispheric processes at forebrain and brainstem levels?
Doty, R. W. (1989) · Behavioural Brain Research · doi:10.1016/s0166-4328(89)80087-7 · Cited by 84
Stellar, J. R., & Corbett, D. (1989) · Brain Research · doi:10.1016/0006-8993(89)91400-5 · Cited by 83
Physiological arousal: a role for hypothalamic systems
Adamantidis, A., & de Lecea, L. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-7521-8 · Cited by 95
Norepinephrine Activates Dopamine D 4 Receptors in the Rat Lateral Habenula
Root, D. H., Hoffman, A. F., Good, C. H., Zhang, S., Gigante, E. D., Lupica, C. R., & Morales, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4525-13.2015 · Cited by 84
“However, VTA TH-expressing/VMAT2negative neurons are consistently found in the anteromedial VTA (Li et al., 2013), where the majority of LHb-projecting VTA neurons are found (Phillipson and Griffith, 1980; Swanson, 1982; Skagerberg et al., 1984; Gruber et al., 2007; Root et al., 2014a).”
BackgroundDopamine and learned food preferences
Sclafani, A. J., Touzani, K., & Bodnar, R. J. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.04.039 · Cited by 86
“DA neurons originating in the ventral tegmental area (VTA) project not only to the NAc but to other areas including the amygdala (AMY) and medial prefortal cortex (mPFC) (Swanson, 1982).”
BackgroundChuhma, N., Mingote, S., Kalmbach, A., Yetnikoff, L., & Rayport, S. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.07.002 · Cited by 93
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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