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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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BackgroundInfluential
Effects of ibotenic acid lesions of the ventral striatum and the medial prefrontal cortex on ethanol consumption in the rat
Hansen, S., Fahlke, C., Hȧrd, E., & Thomasson, R. (1995) · Alcohol · doi:10.1016/0741-8329(95)00008-f · Cited by 28
Locomotion towards a goal alters the synchronous firing of neurons recorded simultaneously in the subiculum and nucleus accumbens of rats
Martin, P. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00209-1 · Cited by 28
t Enhanced Amygdala Kindling after Electrical Stimulation of the Ventral Tegmental Area: Implications for Fear and Anxiety
Gelowitz, T. D. L., & Kokkinidis, L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-22-j0004.1999 · Cited by 28
“…area (VTA) dopamine (DA) neurons mediate conditioned fear responding through their ascending projections to the central and basolateral amygdala (Swanson, 1982; Trulson and Preussler, 1984; Deutch et al., 1985; Oades and Halliday, 1987; Borowski and Kokkinidis, 1996; Munro and Kokkinidis, 1997;…”
Background
Dopamine Depletion Reorganizes Projections from the Nucleus Accumbens and Ventral Pallidum That Mediate Opioid-Induced Motor Activity
Churchill, L., Klitenick, M. A., & Kalivas, P. W. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-19-08074.1998 · Cited by 28
“Dopamine in the nucleus accumbens arises from a dense innervation by the ventral mesencephalon, including the VTA and substantia nigra ( Swanson, 1982 ), and dopamine lesions of the mesoaccumbens projection augment the behavioral response produced by DAMGO microinjection into the nucleus accumbens (Kalivas and Bronson…”
Prior exposure to cocaine diminishes behavioral and biochemical responses to aversive conditioning: Reversal by glycine/N-methyl-d-aspartate antagonist co-treatment
Morrow, B. A., Taylor, J. R., & Roth, R. H. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00184-k · Cited by 28
Chronic haloperidol inactivates brain noradrenergic neurons
Dinan, T. G., & Aston‐Jones, G. (1985) · Brain Research · doi:10.1016/0006-8993(85)90346-4 · Cited by 28
Neuropharmacological and electrophysiological evidence implicating the mesolimbic dopamine system in feeding responses elicited by electrical stimulation of the medial forebrain bundle
Mogenson, G. J., & Wu, M. (1982) · Brain Research · doi:10.1016/0006-8993(82)90691-6 · Cited by 28
Neuroanatomy and Neurochemical Mechanisms of Time-Dependent Sensitization
Sorg, B. A., Hooks, M. S., & Kalivas, P. W. (1994) · Toxicology and Industrial Health · doi:10.1177/074823379401000511 · Cited by 28
Dopamine neurons drive spatiotemporally heterogeneous striatal dopamine signals during learning
Engel, L., Wolff, A. R., Blake, M., Collins, V. L., Sinha, S., & Saunders, B. T. (2024) · Current Biology · doi:10.1016/j.cub.2024.05.069 · Cited by 30
Afferent connections of septal nuclei of the domestic chick (Gallus domesticus): A retrograde pathway tracing study
Montagnese, C. M., Zachár, G., Bálint, E., & Csillag, A. (2008) · The Journal of comparative neurology · doi:10.1002/cne.21837 · Cited by 29
“For example, the VTA of mammals projects heavily to SL (Beckstead et al., 1979; Swanson, 1982; Oades and Halliday, 1987; Staiger and Nürnberger, 1989; Jakab and Leranth, 1993), preferentially to the rostral SL (Risold and Swanson, 1997).”
Background
High-Sugar, but Not High-Fat, Food Activates Supraoptic Nucleus Neurons in the Male Rat
Hume, C., Sabatier, N., & Menzies, J. R. W. (2017) · Endocrinology · doi:10.1210/en.2016-1640 · Cited by 27
“Neither the ventral tegmental area (59) nor the nucleus accumbens (60) of the mesolimbic reward system directly project to the SON or PVN in the rat.”
Background
Social defeat stress induces hyperalgesia and increases truncated BDNF isoforms in the nucleus accumbens regardless of the depressive‐like behavior induction in mice
Pagliusi, M., Bonet, I. J. M., Dias, E. V., Vieira, A. S., Tambeli, C. H., Parada, C. A., & Sartori, C. R. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13994 · Cited by 26
“, 2015) that, like NAc, receives projections from VTA (Swanson, 1982).”
Background
Cannabinoid Modulation of Dopamine Release During Motivation, Periodic Reinforcement, Exploratory Behavior, Habit Formation, and Attention
Oleson, E. B., Hamilton, L. R., & Gomez, D. M. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.660218 · Cited by 28
“%) neurons also exist and are capable of modulating DA neural activity, mesocorticolimbic output, and behavior (Swanson, 1982; Morales and Root, 2014; Yoo et al., 2016).”
Background
Lateral hypothalamus dopamine D1-like receptors and glucose-conditioned flavor preferences in rats
Touzani, K., Bodnar, R. J., & Sclafani, A. J. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.06.006 · Cited by 28
“In this system, dopamine neurons located in the ventral tegmental area (VTA) project heavily to cortical and limbic structures including the nucleus accumbens (NAc), amygdala (AMY) and the prefrontal cortex (Swanson, 1982).”
Influential
Effects of propofol on the dopamine, metabolites and GABAA receptors in media prefrontal cortex in freely moving rats.
Wang, Y., Yu, T., Yuan, C., Yuan, J., Luo, Z., Pan, Y., Zhang, Y., Zhang, Y., & Yu, B. (2016) · PubMed Central · Cited by 27
Neural substrates of updating the prediction through prediction error during decision making
Wang, Y., Ma, N., He, X., Li, N., Wei, Z., Yang, L., Zha, R., Han, L., Li, X., Zhang, D., et al. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.05.041 · Cited by 27
“Three distinct ascending DA projection systems from the midbrain have been suggested, namely the nigrostriatal (or mesostriatal), mesolimbic, and mesocortical pathways with widespread projections to forebrain targets (Lindvall et al., 1977; Fallon et al., 1978; Swanson, 1982).”
Deconstructing value-based decision making via temporally selective manipulation of neural activity: Insights from rodent models
Orsini, C. A., Hernandez, C. M., Bizon, J. L., & Setlow, B. (2018) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-018-00649-0 · Cited by 28
“…and activation of dopamine (DA) neurons, respectively, in the ventral tegmental area (VTA; Ji & Shepard, 2007; Stopper et al., 2014), a major source of dopaminerg ic a f fe ren t s to bra in reg ions in the mesocorticolimbic circuit (e.g., NAc, BLA; Oades & Halliday, 1987; Swanson, 1982).”
Background
Conventional and Novel Pharmacological Approaches to Treat Dopamine-Related Disorders: Focus on Parkinson’s Disease and Schizophrenia
de la Mora, M. P., Hernández-Mondragón, J. C., Crespo‐Ramírez, M., Rejón-Orantes, J. D. C., Borroto‐Escuela, D. O., & Fuxé, K. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.07.026 · Cited by 28
Assessments of Cognitive Deficits in Mutant Mice
Rodriguiz, R. M., & Wetsel, W. C. (2006) · Frontiers in neuroscience · doi:10.1201/9781420004335.ch12 · Cited by 27
Terminals from the Rat Prefrontal Cortex Synapse on Mesoaccumbens VTA Neurons
CARR, D. B., & Sesack, S. R. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09299.x · Cited by 27
Organization of the Hypothalamus
Simerly, R. B. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00013-9 · Cited by 27
Possible pathways through which neurons of the shell of the nucleus accumbens influence the outflow of the core of the nucleus accumbens
Otake, K., & Nakamura, Y. (2000) · Brain and Development · doi:10.1016/s0387-7604(00)00142-x · Cited by 27
Metabolic Mapping of the Effects of Oral Alcohol Self‐Administration in Rats
Porrino, L. J., Williams‐Hemby, L., Whitlow, C. T., Bowen, C. A., & Samson, H. H. (1998) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1998.tb03635.x · Cited by 27
R-(+)-HA-966, an antagonist for the glycine/NMDA receptor, prevents locomotor sensitization to repeated cocaine exposures
Morrow, B. A., Taylor, J. R., & Roth, R. H. (1995) · Brain Research · doi:10.1016/0006-8993(94)01456-r · Cited by 27
Ovarian steroids alter dopamine receptor populations in the medial preoptic area of female rats: implications for sexual motivation, desire, and behaviour
Graham, M. D., Gregory, J. G., Hussain, D., Brake, W. G., & Pfaus, J. G. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13121 · Cited by 26
“The mPOA could indirectly communicate with these areas as it sends efferents to the ventral tegmental area (Simerly & Swanson, 1988), which in turn has DAergic neuron projections to the nucleus accumbens and striatum (Swanson, 1982; Deutch et al., 1988).”
Background
Stimulation of the ventral tegmental area increased nociceptive thresholds and decreased spinal dorsal horn neuronal activity in rat
Li, A.-L., Sibi, J. E., Yang, X., Chiao, J. ‐., & Peng, Y. B. (2016) · Experimental Brain Research · doi:10.1007/s00221-016-4558-z · Cited by 31
“The VTA has bilateral projections to various key areas in the midbrain that are involved in descending pain modulation, such as the periaqueductal gray (PAG), locus coeruleus, median raphe nucleus and parabrachial nucleus (Swanson 1982).”
Caffeine Modulates Food Intake Depending on the Context That Gives Access to Food: Comparison With Dopamine Depletion
Correa, M., Miguel, N. S., López‐Cruz, L., Carratalá‐Ros, C., Olivares-García, R., & Salamone, J. D. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00411 · Cited by 26
The Impact of Electronic Nicotine Delivery System (ENDS) Flavors on Nicotinic Acetylcholine Receptors and Nicotine Addiction-Related Behaviors
Cooper, S. Y., & Henderson, B. J. (2020) · Molecules · doi:10.3390/molecules25184223 · Cited by 29
“further prompts DA release into the NAc, amygdala, and PFC, which makes up the mesocorticolimbic system [99].”
Background
Inhibition of Dopamine Neurons Prevents Incentive Value Encoding of a Reward Cue: With Revelations from Deep Phenotyping
Iglesias, A. G., Chiu, A. S., Wong, J. W. H., Campus, P., Li, F. R., Liu, Z., Bhatti, J. K., Patel, S. A., Deisseroth, K. A., Akil, H., et al. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0848-23.2023 · Cited by 32
Genetics of Aggression in Voles
Gobrogge, K. L., & Wang, Z. (2011) · Advances in genetics · doi:10.1016/b978-0-12-380858-5.00003-4 · Cited by 26
Postnatal development of dopamine innervation in the amygdala and the entorhinal cortex of the gerbil (Meriones unguiculatus)
Brummelte, S., & Teuchert, G. (2006) · Brain Research · doi:10.1016/j.brainres.2006.10.006 · Cited by 26
Activity of presumed dopamine neurons in the ventral tegmental area during heroin self-administration
Kiyatkin, E. A., & Rebec, G. V. (1997) · Neuroreport · doi:10.1097/00001756-199707280-00032 · Cited by 26
κ Opioid receptor activation in different brain regions differentially modulates anxiety-related behaviors in mice
Wang, Y., Hang, A., Lu, Y., Long, Y., Zan, G., Li, X., Wang, Q., Zhao, Z., He, L., Chi, Z., et al. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.04.022 · Cited by 27
Susceptibility of ascending dopamine projections to 6-hydroxydopamine in rats: effect of hypothermia
Grant, R. J., & Clarke, P. B. S. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00385-8 · Cited by 26
A functional interaction between the mesolimbic dopamine system and vasopressin release in the regulation of blood pressure in conscious rats
Cornish, J. L., Wilks, D. P., & van den Buuse, M. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00157-7 · Cited by 26
Efferent projections of the retrorubral nucleus to the substantia nigra and ventral tegmental area in cats as shown by anterograde tracing
Arts, M. P. M., Groenewegen, H. J., Veening, J. G., & Cools, A. R. (1996) · Brain Research Bulletin · doi:10.1016/0361-9230(96)00048-2 · Cited by 26
A history of human‐like dieting alters serotonergic control of feeding and neurochemical balance in a rat model of binge‐eating
Chandler-Laney, P. C., Castañeda, E., Viana, J. B., Oswald, K. D., Maldonado, C. R., & Boggiano, M. M. (2006) · International Journal of Eating Disorders · doi:10.1002/eat.20349 · Cited by 26
Asymmetrical increases in dopamine turn-over in the nucleus accumbens and lack of changes in locomotor responses following unilateral dopaminergic depletions in the entorhinal cortex
Louilot, A., & Choulli, M. K. (1997) · Brain Research · doi:10.1016/s0006-8993(97)01050-0 · Cited by 26
The anxiogenic β-carboline FG-7142 increases in vivo and in vitro tyrosine hydroxylation in the prefrontal cortex
Knorr, A. M., Deutch, A. Y., & Roth, R. H. (1989) · Brain Research · doi:10.1016/0006-8993(89)90228-x · Cited by 26
Pyridoxine improves hippocampal cognitive function via increases of serotonin turnover and tyrosine hydroxylase, and its association with CB1 cannabinoid receptor-interacting protein and the CB1 cannabinoid receptor pathway
Jung, H. Y., Kim, D. W., Nam, S. M., Kim, J. W., Chung, J. Y., Won, M.-H., Seong, J. K., Yoon, Y. S., Yoo, D. Y., & Hwang, I. K. (2017) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2017.09.006 · Cited by 23
Regionally selective requirement for D1/D5 dopaminergic neurotransmission in the medial prefrontal cortex in object-in-place associative recognition memory
Savalli, G., Bashir, Z. I., & Warburton, E. C. (2015) · Learning & Memory · doi:10.1101/lm.036921.114 · Cited by 19
“The mPFC, PRH, and HPC all receive prominent dopaminergic innervation (Berger et al. 1974; Scatton et al. 1980; Swanson 1982; Sobel and Corbett 1984; Fallon and Laughlin 1995; DiChiara 2002) and exposure to novel stimuli and novel environments increases midbrain dopaminergic cell body firing…”
Background

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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