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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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“The medial prefrontal cortex represents a further key terminal region for ascending monoaminergic pathways, some of which originate in the ventral tegmental area [52].”
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“…DA neurons projecting primarily to the dorsal striatum (i.e., the caudate/putamen) and the VTA projecting primarily to the ventral striatum (the nucleus accumbens (NAc) and olfactory tubercle) as well as prefrontal cortex, the amygdala and the hippocampus (Beckstead et al., 1979; Swanson, 1982).”
InfluentialDistinct Medial Temporal Lobe Network States as Neural Contexts for Motivated Memory Formation
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“Anatomically, the VTA innervates, though not uniformly, the entire MTL (Swanson 1982; Gasbarri et al. 1994).”
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“…histochemistry revealed that restricted cortical areas are also innervated by dopamine(DA)containing axons originating from rostral mesencephalic neuronal groups (Fuxe et al., 1974; Lindvall et al., 1974, 1978; Berger et al., 1976; Carter and Fibiger, 1977; Emson and Koob, 1978; Swanson, 1982).”
BackgroundDopaminergic Modulation of Appetitive and Aversive Predictive Learning
Iordanova, M. D. (2009) · Reviews in the Neurosciences · doi:10.1515/revneuro.2009.20.5-6.383 · Cited by 50
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“These functional differences may be related to differences in axonal projections (see, for review Ikemoto, 2007), as more posterior VTA dopamine neurons project to the NAc than anterior neurons (Swanson, 1982).”
BackgroundCousineau, J., Plateau, V., Baufreton, J., & Bon-Jégo, M. L. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105674 · Cited by 48
“A decade later, DAergic terminals were clearly described in the frontal cortex, coming from the ventral tegmental area (VTA) and the substantia nigra pars compacta (SNc; Fallon, 1981; Swanson, 1982).”
BackgroundEstablishing diversity in the dopaminergic system
Bodea, G. O., & Blaess, S. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.09.016 · Cited by 50
Striatal and Medial Temporal Lobe Functional Interactions during Visuomotor Associative Learning
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“These circuits originate in the ventral tegmental area and project to limbic and cortical structures, especially the nucleus accumbens, prefrontal cortex, and amygdala (Swanson, 1982; Walsh and Han, 2014).”
BackgroundUnderstanding the role of dopamine in conditioned and unconditioned fear
Brandão, M. L., & Coimbra, N. C. (2018) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0023 · Cited by 49
Different laminar distributions of dopamine D1 and D2 receptors in the rat hippocampal region
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BackgroundMcDannald, M. A., Kerfoot, E. C., Gallagher, M., & Holland, P. C. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03458.x · Cited by 49
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“…identifying monosynaptic axonal pathways is the chemical tracer technique that require ex-vivo tissue processing (Abe et al., 2018; Burman et al., 2015; Majka et al., 2016; Reser et al., 2017, 2013; Swanson, 1982; Warner et al., 2015; Zeater et al., 2019) and thus can only be used in animal models.”
Han, Z., Luo, N., Ma, W., Liu, X., Cai, Y., Kou, J., Wang, J., Li, L., Peng, S., Xu, Z., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39554-7 · Cited by 50
Local Hippocampal Methamphetamine-Induced Reinforcement
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“1B) (Swanson, 1982; Brog et al., 1993) as WT and Clock- 19 mice performed an elevated zero-maze task (a modified version of the elevated plus maze).”
MethodNeurotrophins in the ventral tegmental area: Role in social stress, mood disorders and drug abuse
Nikulina, E. M., Johnston, C. E., Wang, J., & Hammer, R. P. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.028 · Cited by 50
“The VTA as a whole contains mainly dopaminergic neurons (50–65%), with approximately 1/3 GABAergic neurons (30–35%; Swanson, 1982; Oades and Halliday, 1987; Yamaguchi et al., 2007; Nair-Roberts et al., 2008) and a few glutamatergic neurons (2–3%; Nair-Roberts et al., 2008).”
Gadziola, M. A., & Wesson, D. W. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3328-15.2016 · Cited by 52
“…et al., 1996), subiculum of the hippocampus (Kelley and Domesick, 1982; Groenewegen et al., 1987; Brog et al., 1993), paraventricular thalamic nucleus (Berendse and Groenewegen, 1990; Moga et al., 1995), and ventral tegmental area (Fallon and Moore, 1978; Swanson, 1982; Del-Fava et al., 2007).”
BackgroundHalje, P., Brys, I., Mariman, J. J., Cunha, C. D., Fuentes, R., & Petersson, P. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00590.2018 · Cited by 49
“The SNc and VTA and the PPTg and LDTg exert dopaminergic and cholinergic modulatory effects, respectively, on the glutamatergic input synapses of the striatum (Garcia-Rill 1991; Swanson 1982; Wang and Morales 2009).”
BackgroundAssessments of Cognitive Deficits in Mutant Mice
Levin, E. D., & Buccafusco, J. J. (2006) · CRC Press eBooks · doi:10.1201/9781420004335-17 · Cited by 48
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Limbic System Participates in Mediating the Effects of General Anesthetics
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“…serotonergic and nonserotonergic inputs to the septum and hippocampus (Vertes et al, 1999), and (3) the ventral tegmental area (VTA), which projects dopaminergic inputs to the nucleus accumbens (NAC), septal complex, hippocampus, and medial prefrontal cortex (Gasbarri et al, 1997; Swanson, 1982).”
BackgroundMethodHaaker, J., Lonsdorf, T. B., & Kalisch, R. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.07.016 · Cited by 47
“…thus augment endogenous dopamine-related consolidation processes that occur after extinction learning in the prefrontal cortex, notably the vmPFC, an area that receives strong dopaminergic input from the midbrain and has high dopamine receptor concentrations (Swanson, 1982; Vincent et al., 1993).”
Touzani, K., Bodnar, R. J., & Sclafani, A. J. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.05.009 · Cited by 47
Cocaine-induced adaptations in metabotropic inhibitory signaling in the mesocorticolimbic system
Hearing, M. C., Zink, A. N., & Wickman, K. (2012) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0045 · Cited by 50
“Furthermore, while VTA DA neurons project to numerous limbic and cortical structures, most of these neurons do not project to more than one forebrain region (Deniau et al., 1980; Fallon, 1981; Swanson, 1982; Margolis et al., 2006).”
Sárvári, M., Deli, L., Kocsis, P., Márk, L., Maász, G., Hrabovszky, E., Kalló, I., Gajári, D., Vastagh, C., Sümegi, B., et al. (2014) · Brain Research · doi:10.1016/j.brainres.2014.06.020 · Cited by 47
“The information transfer between the VTA and the PFC is reciprocal [13, 14].”
Dopamine regulates stimulus generalization in the human hippocampus
Kahnt, T., & Tobler, P. N. (2016) · eLife · doi:10.7554/elife.12678 · Cited by 44
Dopaminergic medication reduces striatal sensitivity to negative outcomes in Parkinson’s disease
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“…tegmental area (VTA) midbrain neurons use bursts and dips in dopaminergic signalling to relay positive and negative RPEs to prefrontal cortex (Deniau et al. , 1980; Swanson, 1982) and the striatum, activating the so-called Go and NoGo pathways (Beckstead et al. , 1979; Surmeier et al. , 2007).”
Modeling fast dopamine neurotransmission in the nucleus accumbens during behavior
Garris, P. A., & Rebec, G. V. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00284-x · Cited by 47
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CHOLINERGIC INNERVATION IN THE HUMAN STRIATUM: A THREE-COMPARTMENT MODEL
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Further analysis of presence of peptides in dopamine neurons
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“(Carter and Fibiger 1977; Swanson 1982; see especially Saper 1985), the anterior thalamic nuclei (Seki and Zyo 1984), medial preoptic area (Chiba and Murata 1985), amygdala (Ottersen 1980; Swanson 1982), nucleus accumbens (Carter and Fibiger 1977; Phillipson and Griffiths 1985), interpeduncular nucleus (Contestabile a…”
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“Though heterogeneous, dopaminergic neurons are the primary neuronal subtype, accounting for 60%–65% of all VTA neurons in rodent models (Swanson, 1982; Nair-Roberts et al., 2008).”
BackgroundJames, M. H., McGlinchey, E. M., Vattikonda, A., Mahler, S. V., & Aston‐Jones, G. (2017) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyx107 · Cited by 46
“Surprisingly, a role for DA signaling in cued reinstatement of cocaine seeking has not been shown, despite evidence that the VTA dopamine system is recruited by stimuli associated with drugs and other rewards (Kufahl et al., 2009; Mahler and Aston-Jones, 2012).”
BackgroundInfluentialMesolimbic dopaminergic system is involved in diurnal blood pressure regulation
Sakata, M., Séi, H., Toida, K., Fujihara, H., Urushihara, R., & Morita, Y. (2002) · Brain Research · doi:10.1016/s0006-8993(01)03402-3 · Cited by 46
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“Although the hippocampus is not considered to be a major part of any dopaminergic system, there is some evidence of a mesencephalic dopamine (DA) containing projection ( Swanson 1982 ) and so hippocampal slices have been treated as a model system in which to examine the postsynaptic actions of DA. Bernardo and Prince…”
Distinct prestimulus and poststimulus activation of VTA neurons correlates with stimulus detection
Totah, N. K. B., Kim, Y., & Moghaddam, B. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00784.2012 · Cited by 47
“Single units were divided into groups using standard extracellular electrophysiology criteria, as described previously (Kim et al. 2010, 2012; Ungless and Grace 2012) (see MATERIALS AND METHODS for details).”
Drug withdrawal conceptualized as a stressor
Chartoff, E. H., & Carlezon, W. A. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000080 · Cited by 44
“Given that the actions of CRF in the VTA are excitatory and most likely contribute to arousal and the reinforcing aspects of stress, drug withdrawalinduced CRF release in the amygdala and BNST may play a more important role in negative affective states.”
BackgroundInfluentialUsunoff, K. G., Itzev, D. E., Rolfs, A., Schmitt, O., & Wree, A. (2006) · Anatomy and Embryology · doi:10.1007/s00429-006-0099-8 · Cited by 47
“…degenerating axons (Kaelber and Afifi 1977), autoradiography (Beckstead et al. 1979), retrograde tracing (Mehler 1980; Ottersen 1981; Russchen 1982; Swanson 1982; Volz et al. 1990), immunocytochemistry (Pearson et al. 1990; Sadikot and Parent 1990; Asan 1998; Asan et al. 2005), electron microscopy…”
BackgroundResultInfluentialBroderick, P. A., Kornak, E. P., Eng, F., & Wechsler, R. T. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90567-d · Cited by 45
“, the middle rostro-caudal VTA) has been shown with anterograde and retrograde tract tracing studies (19,59,60).”
Neurotensin in the ventromedial mesencephalon of the rat: Anatomical and functional considerations
Kalivas, P. W. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902260405 · Cited by 45
Distribution of melanin-concentrating hormone neurons projecting to the medial mammillary nucleus
Casatti, C. A., Elias, C. F., Sita, L. V., Frigo, L., Furlani, V. C. G., Bauer, J. A., & Bittencourt, J. C. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00508-0 · Cited by 44
Immunohistochemical investigation of the internal structure of the mouse subiculum
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Altered prefrontal correlates of monetary anticipation and outcome in chronic pain
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“The VTA projects directly to both the NAcc and mPFC.(77) We anticipated that altered VTA reward anticipatory response might be reduced in our patients.”
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“1981) (rat, cat and monkey), (Phillipson and Pycock 1982) (rat), (Swanson 1982) (rat), (Skagerberg et al.”
Bockstaele, E. J. V., Wright, A. M., Cestari, D. M., & Pickel, V. M. (1994) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(94)90042-6 · Cited by 44
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Sotty, F., Brun, P., Leonetti, M., Steinberg, R., Soubrié, P., Renaud, B., & Suaud‐Chagny, M. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)90023-x · Cited by 44
Ding, Z., Oster, S. M., Hall, S. R., Engleman, E. A., Hauser, S. R., McBride, W. J., & Rodd, Z. A. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2208-5 · Cited by 44
“However, neuro-anatomical evidence does not support this idea because both the aVTA and pVTA appear to project to the VP and mPFC (Klitenick et al. 1992; Swanson 1982).”
BackgroundOpioid-Induced Molecular and Cellular Plasticity of Ventral Tegmental Area Dopamine NeuronsPreprint
Doyle, M. A., & Mazei‐Robison, M. S. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a039362 · Cited by 45
“This heterogeneous region is composed of 60%–65% DA, 30%–35% GABA, and 2%–3% glutamate neurons (Swanson 1982; Nair-Roberts et al. 2008).”
BackgroundOn the role of subsecond dopamine release in conditioned avoidance
Oleson, E. B., & Cheer, J. F. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00096 · Cited by 44
Serotonin-like immunoreactive cells and fibres in the rat ventromedial mesencephalic tegmentum
Halliday, G. M., & Törk, I. (1989) · Brain Research Bulletin · doi:10.1016/0361-9230(89)90092-0 · Cited by 43
Post‐training cocaine exposure facilitates spatial memory consolidation in C57BL/6 mice
Iñiguez, S. D., Charntikov, S., Baella, S. A., Herbert, M. S., Bolaños‐Guzmán, C. A., & Crawford, C. A. (2011) · Hippocampus · doi:10.1002/hipo.20941 · Cited by 45
Castilho, R. F., Hansson, O., & Brundin, P. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)27011-8 · Cited by 44
The Supramammillary Nucleus Mediates Primary Reinforcement via GABAA Receptors
Ikemoto, S. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300660 · Cited by 43
“While this area has dopaminergic neurons, they are much sparser than those in more posterior portions of the VTA (Swanson, 1982).”
BackgroundBhardwaj, A., Brannan, T. S., Martinez-Tica, J. F., & Weinberger, J. M. (1990) · Journal of Neural Transmission · doi:10.1007/bf01245121 · Cited by 43
de Bruin, N. M. W. J., Ellenbroek, B. A., van Luijtelaar, E. L. J. M., Cools, A. R., & Stevens, K. E. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00183-x · Cited by 43
Repeated d -amphetamine enhances stimulated mesoamygdaloid dopamine transmission
Harmer, C. J., Hitchcott, P. K., Morutto, S. L., & Phillips, G. D. (1997) · Psychopharmacology · doi:10.1007/s002130050342 · Cited by 43
“dopamine neurons originating in the ventral tegmental area of the mesencephalon innervate the amygdala as well as the accumbens; terminating primarily, but not exclusively, within the central nucleus (Fallon et al. 1978; Swanson 1982; Price et al. 1987).”
BackgroundPhelix, C. F., & Broderick, P. A. (1995) · Brain Research Bulletin · doi:10.1016/0361-9230(94)00253-3 · Cited by 43
Østergaard, K., Holm, I. E., & Zimmer, J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903220202 · Cited by 43
Mesencephalic Dopaminergic Neurons: Role in the General Economy of the Brain
Simon, H., & Moal, M. L. (1988) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1988.tb42110.x · Cited by 42
Cre-driven optogenetics in the heterogeneous genetic panorama of the VTA
Pupe, S., & Wallén‐Mackenzie, Å. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.005 · Cited by 44
Bonapersona, V., Joëls, M., & Sarabdjitsingh, R. A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.003 · Cited by 44
Mickiewicz, A. L., Dallimore, J. E., & Napier, T. C. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.111 · Cited by 42
“The VTA provides dopaminergic inputs to the NAc (Fallon and Moore, 1978; Haglund et al, 1979; Swanson, 1982) and VP (Napier et al, 1991a; Klitenick et al, 1992; Mitrovic and Napier, 2002).”
BackgroundHorváth, M., Kovács, G. G., Kövari, V., Majtényi, K., Hurd, Y. L., & Keller, É. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2398-07.2007 · Cited by 42
“In addition to rewardrelated mesolimbic DA neurons that innervate the nucleus accumbens, a mesocortical subpopulation projects to the prefrontal cortex relevant for cognitive function and emotional regulation (Swanson, 1982; Haber and Fudge, 1997).”
BackgroundOhtori, S., Takahashi, K., Chiba, T., Takahashi, Y., Yamagata, M., Sameda, H., & Moriya, H. (2000) · Spine · doi:10.1097/00007632-200010010-00002 · Cited by 42
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Yang, J., Sadler, T. R., Givrad, T. K., Maarek, J.-M. I., & Holschneider, D. P. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.010 · Cited by 41
“The supramammillary nucleus contains many dopaminergic neurons (Swanson, 1982), some of which are extensions of the A10 cell group (ventral tegmental area), which shows a decrease in tyrosine hydroxylase staining cells after striatal lesions (Yuan et al.”
BackgroundTopography and collateralization of dopaminergic projections to primary motor cortex in rats
Hosp, J. A., Nolan, H. E., & Luft, A. R. (2015) · Experimental Brain Research · doi:10.1007/s00221-015-4211-2 · Cited by 38
“Apart from the well-characterized connection between substantia nigra and dorsal striatum, dopaminergic neurons within the midbrain also innervate limbic and neocortical structures (Fallon 1981; Swanson 1982).”
BackgroundPark, J., Bucher, E. S., Budygin, E. A., & Wightman, R. M. (2015) · Pain · doi:10.1097/01.j.pain.0000460312.79195.ed · Cited by 42
Gentry, R. N., Schuweiler, D. R., & Roesch, M. R. (2018) · Brain Research · doi:10.1016/j.brainres.2018.10.008 · Cited by 41
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript cortical output neurons to amygdala, and is heavily innervated by DA projections from VTA (Swanson, 1982; Vincent et al., 1993; Lidow et al., 1998; Mueller et al., 2010).”
BackgroundInfluentialExcitatory VTA to DH projections provide a valence signal to memory circuits
Han, Y., Zhang, Y., Kim, H. R., Grayson, V. S., Jovasevic, V., Ren, W., Centeno, M. V., Guedea, A. L., Meyer, M. A. A., Wu, Y., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15035-z · Cited by 41
Jayaraman, A., Nishimori, T., Dobner, P. R., & Uhl, G. R. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902960209 · Cited by 41
Weiss‐Wunder, L. T., & Chesselet, M. ‐. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903030312 · Cited by 41
Bilateral tectal projection of single nigrostriatal dopamine cells in the rat
Campbell, K. J., & Takada, M. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90211-x · Cited by 41
Anterior brain dysfunctioning as a risk factor in alcoholic behaviors
Deckel, A. W., Bauer, L. O., & HESSELBROCK, V. M. (2003) · Addiction · doi:10.1046/j.1360-0443.1995.901013234.x · Cited by 41
Grenhoff, J., Tung, C., & Svensson, T. H. (1988) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.1988.tb10639.x · Cited by 41
Song, R., Bi, G., Zhang, H., Yang, R., Gardner, E. L., Li, J., & Xi, Z. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.10.010 · Cited by 41
“…system originates in the midbrain ventral tegmental area (VTA) and projects to the nucleus accumbens (NAc) and prefrontal cortex (PFC); it is believed that this pathway is essential for both drug reward and relapse to drug-seeking behavior (Swanson, 1982; Wise, 1996; Lüscher and Malenka, 2011).”
Wattanathorn, J., & Sutalangka, C. (2014) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2014/937601 · Cited by 40
“In addition, several lines of evidence have demonstrated that dentate gyrus of the hippocampus received the dopaminergic projection form substantia nigra (A9) [35, 36] and ventral tegmental area (A10), a structure nearby substantia nigra, via mesolimbic”
BackgroundParker, N. F., Baidya, A., Cox, J., Haetzel, L. M., Zhukovskaya, A., Murugan, M., Engelhard, B., Goldman, M. S., & Witten, I. B. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110756 · Cited by 41
“…with dense dopaminergic inputs from the midbrain (Brog et al., 1993; Do-Monte et al., 2017; Groenewegen et al., 1980; Hunnicutt et al., 2016; Otis et al., 2017; Phillipson and Griffiths, 1985; Poulin et al., 2018; Reed et al., 2018; Swanson, 1982; Wright and Groenewegen, 1995; Zhu et al., 2016).”
BackgroundHeydendael, W., & Jacobson, L. (2009) · Brain Research · doi:10.1016/j.brainres.2009.06.082 · Cited by 40
Wang, J., Carnicella, S., Ahmadiantehrani, S., He, D., Barak, S., Kharazia, V., Hamida, S. B., Zapata, A. G., Shippenberg, T. S., & Dorit Ron, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3909-10.2010 · Cited by 39
“In addition to projecting to the NAc, VTA DA neurons also project to the PFC (Swanson, 1982).”
BackgroundInfluentialA versatile system for the neuronal subtype specific expression of lentiviral vectors
Tolu, S., Avale, M. E., Nakatani, H., Pons, S., Parnaudeau, S., Tronche, F., Vogt, A., Monyer, H., Vogel, R., de Chaumont, F., et al. (2009) · The FASEB Journal · doi:10.1096/fj.09-139790 · Cited by 40
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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