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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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Prospects for serotonin 5-HT2R pharmacotherapy in psychostimulant abuse
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On the Origin of Cortical Dopamine: Is it a Co-Transmitter in Noradrenergic Neurons?
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“The mesostriatal and mesolimbic inputs to the caudateputamen, the nucleus accumbens, and the amygdala arise from DA neurons in the ventral tegmental area (VTA), the substantia nigra, and the retrorubral fields (Fallon et al., 1978; Fallon and Moore, 1978b; Swanson, 1982; Deutch et al., 1988).”
BackgroundResultInfluentialMesocorticolimbic Dopamine Pathways Across Adolescence: Diversity in Development
Reynolds, L. M., & Flores, C. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.735625 · Cited by 137
Hippocampal dopamine/DRD1 signaling dependent on the ghrelin receptor
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“Dopaminergic neurons in the VTA innervate the hippocampus, implicating a VTA-hippocampal loop that regulates hippocampal plasticity (Gasbarri et al., 1994; Lisman and Grace, 2005; Swanson, 1982).”
Infralimbic D2 Receptors Are Necessary for Fear Extinction and Extinction-Related Tone Responses
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Stressor-induced anhedonia in the mesocorticolimbic system
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Specific A10 Dopaminergic Nuclei in the Midbrain Degenerate in Parkinson's Disease
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Functional connectivity and network analysis of midbrain and brainstem nuclei
Bär, K.-J., de la Cruz, F., Schumann, A., Koehler, S., Sauer, H., Critchley, H., & Wagner, G. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.03.071 · Cited by 134
“In contrast, the SNc projects primarily to more lateral-ventral cortical regions, putamen and globus pallidus (Fallon and Moore, 1978; Swanson, 1982).”
BackgroundHuston, J. P., Wagner, U. A. G., & Hasenöhrl, R. U. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)86052-4 · Cited by 134
Development and function of the midbrain dopamine system: what we know and what we need to
Bissonette, G. B., & Roesch, M. R. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12257 · Cited by 141
“from the VTA do sometimes target striatal cells, and SNc neurons do sometimes project to limbic or cortical regions (Bromberg-Martin et al. 2010; Fallon & Loughlin 1982; Loughlin & Fallon 1984; Swanson 1982) and these projections likely carry different types of neural signals (Haruno & Kawato 2006; Lau & Glimcher 2008…”
BackgroundDistinct nigrostriatal projection systems innervate striosomes and matrix in the primate striatum
Langer, L. F., & Graybiel, A. M. (1989) · Brain Research · doi:10.1016/0006-8993(89)91114-1 · Cited by 133
Mejias-Aponte, C., Drouin, C., & Aston-Jones, G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4632-08.2009 · Cited by 137
“DA neurons send stronger projections to entorhinal cortex and hippocampus than do DA neurons in SN or VTA; thus, RRF DA cells may serve a modulatory role in declarative and spatial memory, functions associated with entorhinal and hippocampal cortices (Swanson, 1982; Deutch et al., 1988; Gasbarri et al., 1996).”
BackgroundLamont, E. W., & Kokkinidis, L. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00281-9 · Cited by 132
Brain areas that influence general anesthesia
Leung, L. S., Luo, T., Ma, J., & Herrick, I. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.08.001 · Cited by 126
Wenzel, J. M., Rauscher, N. A., Cheer, J. F., & Oleson, E. B. (2015) · ACS Chemical Neuroscience · doi:10.1021/cn500255p · Cited by 131
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“The PBP and PN are major nuclei of the ventral tegmental area (VTA; Swanson 1982).”
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“The above-mentioned terminal regions of the mesocorticolimbic DA system (Swanson, 1982) were chosen because of their role in the conditioned rewarding effects of drugs and non-drug reinforcers (Everitt et al., 1999), cue-induced reinstatement (See, 2002), and extinction behavior (Neisewander et…”
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“Within the VTA are two main cell populations, DAergic projection neurons, which comprise ∼60% of cells in this region (Swanson, 1982), as well as local GABAergic interneurons and projection neurons (Carr and Sesack, 2000; Margolis et al.”
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“%) neurons making up the rest (Swanson, 1982; Nair-Roberts et al., 2008).”
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Seroogy, K. B., Ceccatelli, S., Schalling, M., Ho¨kfelt, T., Frey, P., Walsh, J. H., Dockray, G. J., Brown, J. C., Buchan, A. M. J., & Goldstein, M. (1988) · Brain Research · doi:10.1016/0006-8993(88)90117-5 · Cited by 127
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“The forebrain projections of the VTA (Swanson, 1982; Loughlin and Fallon, 1984) arise from both DA and GABA cells (Van Bockstaele and Pickel, 1995; Carr and Sesack, 2000a), with related but discrete functions (Laviolette and van der Kooy, 2001; Lee et al., 2001; Steffensen et al., 2001).”
BackgroundResultInfluentialFunctional implications of glutamatergic projections to the ventral tegmental area
Geisler, S., & Wise, R. A. (2008) · Reviews in the Neurosciences · doi:10.1515/revneuro.2008.19.4-5.227 · Cited by 125
Generalization of value in reinforcement learning by humans
Wimmer, G. E., Daw, N. D., & Shohamy, D. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08017.x · Cited by 111
“Conversely, value information in the hippocampus may arrive via significant projections from midbrain dopaminergic neurons of the ventral tegmental area (Dahlström & Fuxe, 1964; Swanson, 1982; Frey et al., 1990; Gasbarri et al., 1994; Huang & Kandel, 1995; Otmakhova & Lisman, 1996).”
BackgroundTang, W., Kochubey, O., Kintscher, M., & Schneggenburger, R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1796-19.2020 · Cited by 131
“Together, these functional and genetic circuit studies corroborate the anatomic notion that distinct populations of midbrain dopamine neurons have largely separate projection targets (Swanson, 1982; Menegas et al., 2015).”
ResultBockstaele, E. J. V., Cestari, D. M., & Pickel, V. M. (1994) · Brain Research · doi:10.1016/0006-8993(94)91330-7 · Cited by 126
Ishikawa, A., Ambroggi, F., Nicola, S. M., & Fields, H. L. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0253-08.2008 · Cited by 129
“…prefrontal cortex (mPFC) and basolateral amygdala (BLA) to the NAc core (McGeorge and Faull, 1989; Sesack et al., 1989; Brog et al., 1993; Pennartz et al., 1994; O’Donnell and Grace, 1995; Zahm, 2000), as well as the dopaminergic projection from the ventral tegmental area (VTA) (Swanson, 1982).”
Lecourtier, L., Oranburg, T. D., & Moghaddam, B. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06130.x · Cited by 125
“Anatomical studies indirectly support this notion; axons from the LHb predominantly innervate the posterior part of the VTA whereas VTA projections to the PFC primarily originate from the anterior portion of this structure (Swanson, 1982).”
ResultClonidine modulates dopamine cell firing in rat ventral tegmental area
Grenhoff, J., & Svensson, T. H. (1989) · European Journal of Pharmacology · doi:10.1016/0014-2999(89)90765-6 · Cited by 124
Wan, F.-J., & Swerdlow, N. R. (1996) · Brain Research · doi:10.1016/0006-8993(96)00209-0 · Cited by 124
Salès, N., Martres, M., Bouthenet, M.-L., & Schwartz, J. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90014-6 · Cited by 124
Barnett, E. M., Cassell, M. D., & Perlman, S. M. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90045-h · Cited by 124
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“The majority of the dopamine (DA) cells in this region are located throughout the substantia nigra (A9) and ventral tegmental area (A10) and extensively innervate limbic, striatal, and cortical telencephalic areas (Anden et al. 1966; Fallon et at. 1978; Fallon and Moore 1978a, b; Swanson 1982; Ungerstedt 1971; for rev…”
Ikemoto, S., & Bonci, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.031 · Cited by 129
“(A) Schematic drawing shows a flat map adopted andmodified from Swanson (2004). (BeF) Afferent, efferent, and reciprocal pro-”
BackgroundDopamine Invigorates Reward Seeking by Promoting Cue-Evoked Excitation in the Nucleus Accumbens
du Hoffmann, J., & Nicola, S. M. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3492-14.2014 · Cited by 122
“In contrast, even though cue-evoked inhibitions were reduced by VTA inactivation (Yun et al., 2004), they were not reduced by local dopamine antagonist injection, and therefore these inhibitions are unlikely to be the result of a direct action of dopamine within the NAc.”
BackgroundInfluentialModulation of the locomotor response to amphetamine by corticosterone
Cador, M., Dulluc, J., & Mormède, P. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90144-5 · Cited by 122
Functional significance of mesolimbic dopamine
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“…VTA and IF (e.g., the nucleus accumbens) but rather innervate nuclei further downstream, including the ventral pallidum, which receives projections from the nucleus accumbens, and the mediodorsal thalamus, which receives projections from the ventral pallidum (Swanson, 1982; Everitt and Wolf, 2002).”
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“The VTA, dorsal tier of the zona compacta of the substantia nigra and retrorubal fields provide dopaminergic innervation to limbic and cortical regions and so are of considerable interest in schizophrenia (64,65).”
From Malthus to motive: How the HPA axis engineers the phenotype, yoking needs to wants
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VGLUT2 in dopamine neurons is required for psychostimulant-induced behavioral activation
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Dorsal tegmental dopamine neurons gate associative learning of fear
Groessl, F., Munsch, T., Meis, S., Griessner, J., Kaczanowska, J., Pliota, P., Kargl, D., Badurek, S., Kraitsy, K., Rassoulpour, A., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0174-5 · Cited by 118
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5-HT2C Receptors Localize to Dopamine and GABA Neurons in the Rat Mesoaccumbens Pathway
Bubar, M. J., Stutz, S. J., & Cunningham, K. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020508 · Cited by 118
“While the existence of non-dopaminergic efferent projections from the VTA has been repeatedly documented [2,3,33,40], the nature and role for these remain undisclosed.”
BackgroundBreton, J., Charbit, A. R., Snyder, B. J., Fong, P. T. K., Dias, E. V., Himmels, P., Lock, H., & Margolis, E. B. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24572 · Cited by 126
“The fact that individual VTA neurons rarely collateralize to multiple projection targets (Fallon, 1981; Margolis, Lock, Chefer, et al., 2006; Swanson, 1982) raises the possibility that these different projections may contribute to different aspects of behavior.”
BackgroundMethodResultInfluentialRapid dopamine dynamics in the accumbens core and shell Learning and action
Saddoris, M. P. (2012) · Frontiers in Bioscience-Elite · doi:10.2741/e615 · Cited by 118
Identified postnatal mesolimbic dopamine neurons in culture: morphology and electrophysiology
Rayport, S., Sulzer, D. L., Shi, W., Sawasdikosol, S., Monaco, J., Batson, D., & Rajendran, G. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04264.1992 · Cited by 117
“Considering the 50% of DA cells ipsilateral to the injection site, and given that one-third of DA VTA cells project to the accumbens (Swanson, 1982) about 800 cells per dish should be mesoaccumbens DA cells.”
BackgroundStefanik, M. T., Kupchik, Y. M., Brown, R. M., & Kalivas, P. W. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1570-13.2013 · Cited by 120
“Neurons in the VTA project densely to the NAcore (Swanson, 1982) and this projection is critical for the rewarding and reinforcing properties of cocaine (Koob and Volkow, 2010).”
BackgroundExtrinsic afferent systems to the dentate gyrus
Léránth, C., & Hajszán, T. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63004-0 · Cited by 120
“In contrast to the very dense noradrenergic innervation of the dentate gyrus, this structure receives only a minor and diffusely distributed dopaminergic projection that arises mainly from the ventral tegmental area (Swanson, 1982).”
BackgroundD�rries, U., Taylor, J., Xiao, Z., Lochter, A., Montag, D., & Schachner, M. (1996) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19960215)43:4 · Cited by 62
Yang, C., & Mogenson, G. J. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-08-02470.1986 · Cited by 116
“The mesolimbic dopaminergic (DA) pathway, which originates from the ventral tegmental area (VTA) and terminates in the nucleus accumbens of the ventral striatum (Dahlstrom and Fuxe, 1964; Swanson, 1982), has a modulatory role in limbic-motor integration (Mogenson, 1984).”
BackgroundMazei‐Robison, M. S., & Nestler, E. J. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012070 · Cited by 113
“(Swanson 1982; Nair-Roberts et al. 2008; Sesack and Grace 2010).”
Dopaminergic innervation and modulation of hippocampal networks
Edelmann, E., & Leßmann, V. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2800-7 · Cited by 117
“…origin of the corresponding axons, the input fibers from VTA, SNpc and the LC all show comparably sparse projection densities in the hippocampus (dorsal hippocampus: Swanson 1982, ventral or dorsal hippocampus: Gasbarri et al. 1994a, for co-release of dopamine from LC: see Smith and Greene 2012).”
BackgroundKalivas, P. W., & Abhold, R. H. (1987) · Brain Research · doi:10.1016/0006-8993(87)90015-1 · Cited by 115
Kolk, S. M., Gunput, R.-A. F., Tran, T. S., van den Heuvel, D. M. A., Prasad, A. A., Hellemons, A. J. C. G. M., Adolfs, Y., Ginty, D. D., Kolodkin, A. L., Burbach, J. P. H., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2521-09.2009 · Cited by 114
“In the adult mouse, mesoprefrontal mdDA projections originate in the medial VTA (Fallon, 1981; Swanson, 1982; Margolis et al., 2006; Lammel et al., 2008).”
BackgroundCappaert, N. L. M., van Strien, N. M., & Witter, M. P. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00020-6 · Cited by 120
Hollerman, J. R., & Grace, A. A. (1990) · Brain Research · doi:10.1016/0006-8993(90)91341-d · Cited by 114
Rocchetti, J., Isingrini, E., Bo, G. D., Sagheby, S., Menegaux, A., Tronche, F., Lévesque, D., Moquin, L., Gratton, A. P., Wong, T. P., et al. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.03.013 · Cited by 113
Rodrı́guez, M., Barroso‐Chinea, P., Abdala, P., Obeso, J. A., & González‐Hernández, T. (2001) · Experimental Neurology · doi:10.1006/exnr.2000.7624 · Cited by 113
Dopaminergic Meso-Cortical Projections to M1: Role in Motor Learning and Motor Cortex Plasticity
Hosp, J. A., & Luft, A. R. (2013) · Frontiers in Neurology · doi:10.3389/fneur.2013.00145 · Cited by 110
“, amygdala and hippocampus) structures (33, 34).”
The antero-posterior heterogeneity of the ventral tegmental area
Sánchez-Catalán, M. J., Kaufling, J., Georges, F. E., Veinante, P., & Barrot, M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.09.025 · Cited by 118
“…20,000 dopamine neurons unilaterally in the rat according to different studies (Swanson, 1982; German and Manaye, 1993; Nair-Roberts et al., 2008), constituting around 2/3 of the VTA neuronal population (Swanson, 1982; German and Manaye, 1993; Harris and Nestler, 1996; Nair-Roberts et al., 2008).”
InfluentialPan, W. X., & McNaughton, N. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02267.x · Cited by 112
“The LH lesions were in an area that is classified as the lateral part of the supramammillary area, rather than lateral hypothalamus, by Swanson (1982) and Risold & Swanson (1997).”
BackgroundOptogenetic Modulation of Neural Circuits that Underlie Reward Seeking
Stuber, G. D., Britt, J. P., & Bonci, A. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.11.010 · Cited by 124
“The VTA, on the other hand, contains a mixture of DAergic (~65%), GABAergic (~30%), and glutamatergic neurons (~ 5%; 22) that project throughout the forebrain to structures including the amygdala, prefrontal cortex, and NAc (20).”
Presynaptic dopamine-glutamate interactions in the nucleus accumbens regulate sensorimotor gating
Wan, F. J., Geyer, M. A., & Swerdlow, N. R. (1995) · Psychopharmacology · doi:10.1007/bf02245815 · Cited by 112
Oades, R. D., Rivet, J., Taghzouti, K., Kharouby, M., Simon, H., & Moal, M. L. (1987) · Brain Research · doi:10.1016/0006-8993(87)90778-5 · Cited by 110
Bentivoglio, M., & Morelli, M. (2005) · Handbook of chemical neuroanatomy · doi:10.1016/s0924-8196(05)80005-3 · Cited by 111
Immunohistochemical mapping of neuropeptides in the premamillary region of the hypothalamus in rats
Lantos, T., Görcs, T. J., & Palkovits, M. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(94)00013-f · Cited by 107
Nicot, A. B., Rostène, W. H., & Bérod, A. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410310 · Cited by 111
Dopaminergic input to GABAergic neurons in the rostral agranular insular cortex of the rat
Ohara, P. T., Granato, A., Moallem, T. M., Wang, B.-R., Tillet, Y., & Jasmin, L. (2003) · Journal of Neurocytology · doi:10.1023/b:neur.0000005598.09647.7f · Cited by 111
The amygdala: securing pleasure and avoiding pain
Fernando, A. B. P., Murray, J. E., & Milton, A. L. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00190 · Cited by 119
Bass, C. E., Grinevich, V. P., Gioia, D. A., Day‐Brown, J. D., Bonin, K., Stuber, G. D., Weiner, J. L., & Budygin, E. A. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00173 · Cited by 112
“, Li, J., and Samulski, R. J., (1998). Production of high-titer recombinant”
MethodContributions of the amygdala and medial prefrontal cortex to incentive cue responding
Ishikawa, A., Ambroggi, F., Nicola, S. M., & Fields, H. L. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.037 · Cited by 110
Murase, S., Math�, J. M., Grenhoff, J., & Svensson, T. H. (1993) · Journal of Neural Transmission · doi:10.1007/bf01244915 · Cited by 109
“Thus, VTA projection areas involved in motor function, such as caudate-putamen, nucleus accumbens and septum, seem to be predominantly innervated by DA neurons in the PN (Simon et al., 1979; Deniau et al., 1980; Fallon, 1981; Swanson, 1982 ), while the rat prefrontal (prelimbic) cortex DA innervation, which has been i…”
BackgroundEricson, H., Blomqvist, A. G., & Köhler, C. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902810203 · Cited by 109
Neurotensin neurons in the ventral tegmental area project to the medial nucleus accumbens
Kalivas, P. W., & Miller, J. S. (1984) · Brain Research · doi:10.1016/0006-8993(84)91351-9 · Cited by 109
Immunohistochemical and neurochemical correlates of learning deficits in aged rats
Stemmelin, J., Lazarus, C., Cassel, S. L., Kelche, C. R., & Cassel, J. (2000) · Neuroscience · doi:10.1016/s0306-4522(99)00561-8 · Cited by 109
Pujol, J., Blanco‐Hinojo, L., Batalla, A., López‐Solà, M., Harrison, B. J., Soriano‐Mas, C., Crippa, J. A. S., Fagundo, A. B., Deus, J., de la Torre, R., et al. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.12.008 · Cited by 110
“…overlaps with the classical dopamine rewarding system at the level of the medial frontal cortex, hippocampus and amygdale (Morales & Pickel, 2012; Swanson, 1982), and that cannabis-related alterations within the dopamine system have also been described (Iversen, 2003; Nestor et al, 2010; van…”
BackgroundGarzón, M., & Pickel, V. M. (2001) · Synapse · doi:10.1002/syn.1088 · Cited by 106
West, E. A., & Carelli, R. M. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2976-15.2016 · Cited by 113
“…lateral and lateral subregions) does not send direct projections to the medial shell (Schilman et al., 2008) and instead may send information regarding the updated motivational state during behavioral performance, perhaps through the ventral tegmental area (Swanson, 1982; Takahashi et al., 2011).”
BackgroundKiyatkin, E. A., & Rebec, G. V. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00054-2 · Cited by 107
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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