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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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“036 the amygdala and the olfactory tubercule (Swanson, 1982).”
BackgroundCellular taxonomy and spatial organization of the murine ventral posterior hypothalamus
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“For example, the dopaminergic component constitutes 72% of the total VTA projection to the lateral septum (Swanson 1982), but only 10% of that to the lateral habenula (Skagerberg et al.”
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Role of Substantia Nigra–Amygdala Connections in Surprise-Induced Enhancement of Attention
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“Given the dense interconnections between the SNc and CeA (Fallon and Moore, 1978; Swanson, 1982; Gonzales and Chesselet, 1990; Fudge and Haber, 2000), this circuitry seems to be an ideal substrate by which DA prediction error signals could influence the enhancement of associative learning that involves the CeA– cholin…”
BackgroundPioli, E. Y., Meissner, W. G., Sohr, R., Gross, C. E., Bézard, E., & Bioulac, B. H. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.01.084 · Cited by 80
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Organization of Mammalian Neuroendocrine System
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VTA Projection Neurons Releasing GABA and Glutamate in the Dentate Gyrus
Ntamati, N. R., & Lüscher, C. (2016) · eNeuro · doi:10.1523/eneuro.0137-16.2016 · Cited by 78
“…Cowan, 1980; Scatton et al., 1980; McNamara et al., 2014; Rosen et al., 2015; Broussard et al., 2016), most have focused solely on the DA projections, with only a few acknowledging the presence of non-DA neurons connecting the VTA or SNc with the hippocampus (Swanson, 1982; Gasbarri et al., 1994).”
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“Similar to the PFC projection, DA afferents are particularly dense within the ICMs and the BLA, but also provide a dense projection to the central nucleus (Ce) (Asan 1998; Brinley-Reed and McDonald 1999; Fallon and Ciofi 1992; Marowsky et al. 2005; Swanson 1982 ).”
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Frequency-dependent gating of synaptic transmission and plasticity by dopamine
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“One of the targets of dopaminergic neurons is the hippocampus, a brain structure crucial for some types of learning and memory (Gasbarri et al., 1994a, 1994b, 1996a; Scoville and Milner, 1957; Squire et al., 2004; Swanson, 1982; Zola-Morgan and Squire, 1986).”
BackgroundActivation of the locus coeruleus induced by selective stimulation of the ventral tegmental area
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“These regions correspond to the known afferents to the PBR (Hopkins and Holstege, 1978; Loewy and Burton, 1978; Norgren, 1978; Saperet al., 1979; Swanson, 1982).”
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Ventral tegmental area involvement in pair bonding in male prairie voles
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“The lateral septum also receives both catecholaminergic and non-catecholaminergic projections from the VTA [43].”
MethodInfluentialWatanabe, M., Narita, M., Hamada, Y., Yamashita, A., Tamura, H., Ikegami, D., Kondo, T., Shinzato, T., Shimizu, T., Fukuchi, Y., et al. (2018) · Molecular Pain · doi:10.1177/1744806918756406 · Cited by 74
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“Depending on the injection site in the LHb, between 1% (Swanson, 1982) and 45% (Gruber et al., 2007) of the retrogradely labeled neurons in the VTA were double-stained for the catecholaminergic marker tyrosine hydroxylase (TH).”
BackgroundMPTP lesions and dopaminergic drugs alter eye blink rate in African green monkeys
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“…of the SN and VTA send numerous projections to distant regions of the brain (Gasbarri, et al., 1997, Gasbarri, et al., 1994, Scatton, et al., 1980, Swanson, 1982, Verney, et al., 1985); thus, degeneration of the SN dopaminergic neurons, a hallmark of Parkinson's disease, may have profound…”
BackgroundReducing Ventral Tegmental Dopamine D2 Receptor Expression Selectively Boosts Incentive Motivation
de Jong, J. W., Roelofs, T. J. M., Mol, F., Hillen, A. E. J., Meijboom, K. E., Luijendijk, M. C. M., van der Eerden, H. A. M., Garner, K. M., Vanderschuren, L. J. M. J., & Adan, R. A. H. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.60 · Cited by 77
“These DA neurons project throughout the forebrain, and the most dense projection reaches the ventral striatum (nucleus accumbens (NAcc) core, shell and olfactory tubercle).”
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“The role of Acb and Amy dopamine receptors, and Acb NMDA receptors in locomotor activity during testing Previous studies involving systemic administration of D1 and D2 antagonists (e.g., Dickinson et al., 2003) or dopamine receptor knockout mice (Holmes, Lachowiez, & Sibley, 2004) have shown that dopamine receptor blo…”
InfluentialHow may the basal ganglia contribute to auditory categorization and speech perception?
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“The dopamine neurons that project to the dorsal striatum are located in the substantia nigra (the pars compacta sector), whereas those that project to the ventral striatum are located in the ventral tegmental area (Nauta et al., 1974; Simon et al., 1979; Swanson, 1982; Amalric and Koob, 1993; Haber and Fudge, 1997).”
BackgroundVertes, R. P. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90051-4 · Cited by 76
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“DA neurons in the VTA largely project to the ventral striatum, in particular, the nucleus accumbens (NAc) core and shell, comprising the mesostriatal pathway, and to other frontal targets in the pallidum, amygdala, and prefrontal cortex (Swanson, 1982; Ikemoto, 2007).”
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“Given that both SNc and VTA have dopaminergic projections to ACB (Swanson, 1982; Brog et al., 1993), the observation of partial impairment in PIT”
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The limbic circuitry underlying cocaine seeking encompasses the PPTg/LDT
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“The VTA is a heterogeneous structure composed of at least two anatomically (Swanson, 1982; German & Manaye, 1993; Olson et al., 2005) and functionally (Ikemoto et al.”
BackgroundDopamine-glutamate neuron projections to the nucleus accumbens medial shell and behavioral switching
Mingote, S., Amsellem, A., Kempf, A., Rayport, S., & Chuhma, N. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.104482 · Cited by 75
“The majority of VTA DA neurons project to the NAc (Breton et al., 2018; Ikemoto, 2007; Swanson, 1982), which is further divided into three subregions, the medial Shell, lateral Shell and the Core (Groenewegen et al.”
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“nucleus accumbens, olfactory tubercles, central nucleus of the amygdala, septum, and a number of cortical areas (Bjorklund and Lindvall, 1984; Swanson, 1982).”
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“While Neurod6 has previously been identified as a VTA marker (Chung et al., 2005; La Manno et al., 2016; Viereckel et al., 2016; Khan et al., 2017), our study is the first to systematically map the projection sites of these cells, revealing a strong medial shell NAc projection with very little output to other DA targe…”
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“It has been a challenge to define the boundaries of VTA subregions consistently because early characterizations of dopaminergic neurons in the rat VTA (Lindvall and Björklund, 1974; Fallon and Moore, 1978; Swanson, 1982).”
BackgroundMikhailova, M. A., Bass, C. E., Grinevich, V. P., Chappell, A. M., Deal, A. L., Bonin, K., Weiner, J. L., Gainetdinov, R. R., & Budygin, E. A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.07.006 · Cited by 74
“However, the VTA sends dopamine projections not only to the nucleus accumbens but also to the amygdala, prefrontal cortex and hippocampus (Beckstead et al., 1979; Swanson, 1982).”
Central amygdala circuits in valence and salience processing
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“This survey revealed the effect of satisfaction on intention to recommend in association with similar investigations [13,29,63,105,111,112,69], whereas the effect of satisfaction on adoption intention was not accepted, in contradiction to the results of former analyses [27,55,98,101,86,20,79,114].”
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Roeling, T. A. P., Veening, J. G., Peters, J. P. W., Vermelis, M. E. J., & Nieuwenhuys, R. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90574-y · Cited by 79
Integrating early results on ventral striatal gamma oscillations in the rat
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“As ventral striatum receives a strong dopaminergic projection from the midbrain (Mogenson et al., 1980; Swanson, 1982) and synaptic and intrinsic membrane properties of ventral striatal neurons are modulated by dopamine (DA) receptor activity (Bracci et al., 2003; Kreitzer and Malenka, 2008) it is…”
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“Since the SNc and the lateral VTA provide essential and extensive DA modulatory inputs to striatal and mesolimbic targets (Swanson, 1982), this suggests that KCNQ channel modulation occurs in both nigrostriatal and limbic pathways.”
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“circulating testosterone may affect dopaminergic neurons in the A10 which control the septohippocampal cholinergic neurons through the A10-septal dopaminergic pathway in male rats [”
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“system and cortical areas that influence behavioral flexibility (Fallon, 1981; Swanson, 1982; Oades and Halliday, 1987).”
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Low and Moderate Doses of Ethanol Produce Distinct Patterns of Cerebral Metabolic Changes in Rats
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Striplin, C. D., & Kalivas, P. W. (1992) · Brain Research · doi:10.1016/0006-8993(92)90049-f · Cited by 71
Berger, B., Verney, C., Febvret, A., Vigny, A., & Helle, K. B. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90021-5 · Cited by 71
Holmstrand, E. C., & Sesack, S. R. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0320-2 · Cited by 72
“At least two of these might include: (1) a prefrontal–accumbens–ventral pallidal– intralaminar thalamic circuit that is heavily influenced by dopaminergic projections from the midbrain VTA and SNc; and (2) a circuit involving the AVN, the retrosplenial cortex, hippocampal structures, the mammillary body and other hypo…”
Differential Effects of Cocaine on Dopamine Neuron Firing in Awake and Anesthetized Rats
Koulchitsky, S., Backer, B. D., Quertemont, É., Charlier, C., & Seutin, V. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.339 · Cited by 70
“According to tracing experiments, the caudal VTA contains a higher proportion of DA than GABAergic neurons and gives rise to more mesoaccumbal projections than does the rostral VTA (Swanson, 1982).”
BackgroundWang, H., & Morales, M. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21751 · Cited by 70
“The existence of subpopulations of VTA DAergic neurons is also supported by tracttracing studies showing a selective organization of the efferent and afferent connectivity among the different VTA DAergic neurons (Swanson, 1982; Carr and Sesack, 2000; Omelchenko and Sesack, 2006).”
Hernandez, L., Auerbach, S. B., & Hoebel, B. G. (1988) · Life Sciences · doi:10.1016/0024-3205(88)90037-9 · Cited by 70
The Medial Septum as a Potential Target for Treating Brain Disorders Associated With Oscillopathies
Takeuchi, Y., Nagy, A. J., Barcsai, L., Li, Q., Ohsawa, M., Mizuseki, K., & Berényi, A. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.701080 · Cited by 74
“Combined retrograde studies proved that the A10 dopaminergic neurons of the VTA send ascending projections to the diagonal band of Broca and the LS (Swanson, 1982; Kalivas, 1985).”
BackgroundRole of dopamine receptors in the ventral tegmental area in conditioned fear
de Oliveira, A. R., Reimer, A. E., & Brandão, M. L. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.004 · Cited by 68
Molecular Mechanism: ERK Signaling, Drug Addiction, and Behavioral Effects
Sun, W., Quizon, P. M., & Zhu, J. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.10.017 · Cited by 71
Midbrain dopaminergic neurons from postnatal rat in long-term primary culture
Cardozo, D. L. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90342-d · Cited by 69
Electrophysiological and Morphological Evidence for a GABAergic Nigrostriatal Pathway
Rodrı́guez, M., & González‐Hernández, T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04682.1999 · Cited by 69
“Thus, not all SN cells projecting to the striatum show catecholamine fluorescence (van der Kooy et al., 1981) or tyrosine hydroxylase immunoreactivity (Swanson, 1982; Gerfen et al., 1987).”
BackgroundResultGhanbarian, E., & Motamedi, F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058844 · Cited by 71
“minergic but the identity of the remaining fibers has not been clearly explained [9,20].”
Backgroundl ‐Dopa activates histaminergic neurons
Yanovsky, Y., Li, S., Klyuch, B. P., Yao, Q.-L., Blandina, P., Passani, M. B., Lin, J., Haas, H. L., & Sergeeva, O. A. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.203257 · Cited by 68
“Previous studies have shown that midbrain dopaminergic neurons from substantia nigra compacta (SNc) and from VTA do not project to the TMN (Arbuthnott & Wright, 1982; Swanson, 1982).”
ResultBerlanga, M. L., Simpson, T. K., & Alcantara, A. A. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20684 · Cited by 68
“Dopaminergic innervation of these cholinergic brain regions occurs primarily through the dopamine (DA) afferents arising from the mesencephalon, more specifically the ventral tegmental area (VTA) and the substantia nigra (SN) (Swanson, 1982).”
BackgroundSpano, M. S., Fattore, L., Fratta, W., & Fadda, P. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.02.012 · Cited by 68
Single thalamic dopaminergic neurons project to both the neocortex and spinal cord
Takada, M., Li, Z. K., & Hattori, T. (1988) · Brain Research · doi:10.1016/0006-8993(88)90093-5 · Cited by 68
Neural Correlates of Variations in Event Processing during Learning in Central Nucleus of Amygdala
Calu, D. J., Roesch, M. R., Haney, R. Z., Holland, P. C., & Schoenbaum, G. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.019 · Cited by 67
“…from the midbrain dopamine neurons most closely associated with signaling of simple bidirectional reward prediction errors (Pitkanen, 2000; Swanson, 1982; Wallace et al., 1992), and communication between CeA and the midbrain has been shown to be essential for enhancement of learning after…”
Coordination of Brain-Wide Activity Dynamics by Dopaminergic Neurons
Decot, H., Namboodiri, V. M. K., Gao, W., McHenry, J. A., Jennings, J. H., Lee, S., Kantak, P. A., Kao, Y. J., Das, M., Witten, I. B., et al. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.151 · Cited by 66
“All GLMextracted voxels largely fell into ROIs within striatal subregions and frontal cortices as predicted based on innervation patterns of THVTA neurons (Swanson, 1982) (Figures 1e and f).”
MethodPuighermanal, E., Cutando, L., Boubaker-Vitre, J., Honoré, È., Longueville, S., Hervé, D., & Valjent, E. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1314-x · Cited by 72
“Although the mesohippocampal DA pathway has been characterized almost three decades ago (Gasbarri et al. 1994a, b; Swanson 1982), the mechanisms by which DA mediates its effect in the hippocampus remain largely unknown.”
Social defeat disrupts reward learning and potentiates striatal nociceptin/orphanin FQ mRNA in rats
Der‐Avakian, A., D’Souza, M. S., Potter, D. N., Chartoff, E. H., Carlezon, W. A., Pizzagalli, D. A., & Markou, A. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4584-y · Cited by 69
Sala, A., Caminiti, S. P., Presotto, L., Pilotto, A., Liguori, C., Chiaravalloti, A., Garibotto, V., Frisoni, G. B., D’Amelio, M., Paghera, B., et al. (2021) · Alzheimer s Research & Therapy · doi:10.1186/s13195-021-00925-1 · Cited by 67
“Speci cally, we observed loss of DAT activity in the ventral striatum and hippocampus, and in the middle cingulate gyrus, receiving dopaminergic input from the ventral and dorsal portions of VTA, respectively[41] (Fig.”
BackgroundKlein, C., Hain, E. G., Braun, J., Riek, K., Mueller, S. G., Steiner, B., & Sack, I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092582 · Cited by 72
“Therefore, we applied MRE to such a mouse model of dopamine depletion, which is induced by the neurotoxin 1methyl-4-phenyl-1,2,3,6-tetrahydropyridine hydrochloride (MPTP) leading to degeneration of dopaminergic neurons in the substantia nigra pars compacta (SNpc) with a subsequent dopamine deficit in the striatum, hip…”
MethodPeleg‐Raibstein, D., & Feldon, J. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.002 · Cited by 67
Two substrates for medial forebrain bundle self-stimulation: Myelinated axons and dopamine axons
Yeomans, J. S. (1989) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(89)80016-8 · Cited by 67
Gaspar, P., Jelloun, N. B., & Febvret, A. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90232-1 · Cited by 67
Sarabi, A., Hoffer, B. J., Olson, L., & Morales, M. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1400 · Cited by 67
“However, it is likely that GFRa1/TH- and GFRa-1/GABA-containing neurons in the VTA might project to the same regions, with the exception of projections to the locus coeruleus (LC), as previous studies demonstrated that projections from the VTA to the LC are GABAergic (Swanson, 1982).”
ResultOlmstead, M. C., & Franklin, K. B. J. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90072-n · Cited by 67
Neuroanatomical Organization of Dopamine Neurons in the Ventral Tegmental Areaa
Domesick, V. B. (1988) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1988.tb42094.x · Cited by 67
Rosin, D. L., Clark, W. A., Goldstein, M., Roth, R. H., & Deutch, A. Y. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90271-3 · Cited by 67
Mechanistic insights into nicotine withdrawal
Paolini, M., & De Biasi, M. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.07.075 · Cited by 66
Neurochemical Mediation of Affiliation and Aggression Associated With Pair-Bonding
Gobrogge, K. L., Jia, X., Liu, Y., & Wang, Z. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.02.013 · Cited by 63
“Finally, dopamine signaling in the rostral nucleus accumbens shell (NAcc) is also involved in selective aggression to maintain monogamous pair-bonds (18).”
InfluentialDopaminergic regulation of hippocampal plasticity, learning, and memory
Tsetsenis, T., Broussard, J. I., & Dani, J. A. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1092420 · Cited by 71
“The first evidence came from experiments using co-localization analysis of retrogradely transported True Blue (TB) from the hippocampus with tyrosine hydroxylase (TH) expressing cells in midbrain dopaminergic areas (Swanson, 1982).”
MethodImpulse activity of ventral tegmental area neurons during heroin self-administration in rats
Kiyatkin, E. A., & Rebec, G. V. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00492-9 · Cited by 66
Colocalization of tyrosine hydroxylase and GAD65 mRNA in mesostriatal neurons
González‐Hernández, T., Barroso‐Chinea, P., Acevedo‐Arozena, A., SALIDO, E. C., & Rodrı́guez, M. (2001) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2001.01371.x · Cited by 66
“…20 years have shown the existence of a nondopaminergic nigrostriatal pathway (Fibiger et al., 1972; Maler et al., 1973; van der Kooy et al., 1981; Swanson, 1982; Gerfen et al., 1987; Hattori et al., 1991), and we have recently identi®ed a subpopulation of nondopaminergic nigrostriatal neurons…”
Background
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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