Afferents to the GABAergic tail of the ventral tegmental area in the rat

Kaufling, Jennifer; Veinante, Pierre; Pawlowski, Sophie A.; Freund‐Mercier, Marie‐Jose; Barrot, Michel

doi:10.1002/cne.21983

Cited by 347Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeurological disorders and treatments

Afferents to the GABAergic tail of the ventral tegmental area in the rat

Kaufling, Jennifer, Veinante, Pierre, Pawlowski, Sophie A., Freund‐Mercier, Marie‐Jose, Barrot, Michel·2009·Journal of Comparative Neurology

DOI 10.1002/cne.21983

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Abstract

We previously showed that chronic psychostimulant exposure induces the transcription factor DeltaFosB in γ‐aminobutyric acid (GABA)ergic neurons of the caudal tier of the ventral tegmental area (VTA). This subregion was defined as the tail of the VTA (tVTA). In the present study, we showed that tVTA can also be visualized by analyzing FosB/DeltaFosB response following acute cocaine injection. This induction occurs in GABAergic neurons, as identified by glutamic acid decarboxylase (GAD) expression. To characterize tVTA further, we mapped its inputs by using the retrograde tracers Fluoro‐Gold or cholera toxin B subunit. Retrogradely labeled neurons were observed in the medial prefrontal cortex, the lateral septum, the ventral pallidum, the bed nucleus of the stria terminalis, the substantia innominata, the medial and lateral preoptic areas, the lateral and dorsal hypothalamic areas, the lateral habenula, the intermediate layers of the superior colliculus, the dorsal raphe, the periaqueductal gray, and the mesencephalic and pontine reticular formation. Projections from the prefrontal cortex, the hypothalamus, and the lateral habenula to the tVTA were also shown by using the anterograde tracer biotinylated dextran amine (BDA). We showed that the central nucleus of the amygdala innervates the anterior extent of the VTA but not the tVTA. Moreover, the tVTA mainly receives non‐aminergic inputs from the dorsal raphe and the locus coeruleus. Although the tVTA has a low density of dopaminergic neurons, its afferents are mostly similar to those targeting the rest of the VTA. This suggests that the tVTA can be considered as a VTA subregion despite its caudal location. J. Comp. Neurol. 513:597–621, 2009. © 2009 Wiley‐Liss, Inc.

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GABAergic inputs to the VTA come from a list of regions including substantia nigra pars reticulata, nucleus accumbens, ventral pallidum/globus pallidus, laterodorsal tegmentum, pedunculopontine nuclei, diagonal band of Broca, bed nucleus of the stria terminalis, and rostromedial tegmental nucleus.
“GABAergic inputs arrive at the VTA from the substantia nigra pars reticulata, nucleus accumbens, ventral pallidum/globus pallidus, laterodorsal tegmentum, pedunculopontine nuclei, diagonal band of Broca, bed nucleus of the stria terminalis, and the caudal tip of the VTA, termed the rostromedial tegmental nucleus (RMTg) (Geisler and Zahm 2005; Jhou et al. 2009; Kaufling et al. 2009).”
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Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396 · see citing works
Input-specific control of reward and aversion in the ventral tegmental area
Lammel, S., Lim, B. K., Ran, C., Huang, K. W., Betley, M. J., Tye, K. M., Deisseroth, K., & Malenka, R. C. (2012) · Nature · doi:10.1038/nature11527 · Cited by 1,300 · see citing works
The habenula: from stress evasion to value-based decision-making
Hikosaka, O. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2866 · Cited by 955 · see citing works
Cortico-Basal Ganglia Reward Network: Microcircuitry
Sesack, S. R., & Grace, A. A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.93 · Cited by 985 · see citing works
Reward and aversion in a heterogeneous midbrain dopamine system
Lammel, S., Lim, B. K., & Malenka, R. C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.019 · Cited by 804 · see citing works
Dopamine system dysregulation in major depressive disorders
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The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses.
Jhou, T. C., Fields, H. L., Baxter, M. G., Saper, C. B., & Holland, P. C. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.001 · Cited by 696 · see citing works
Synaptic potentiation onto habenula neurons in the learned helplessness model of depression
Li, B., Piriz, J., Mirrione, M., Chung, C., Proulx, C. D., Schulz, D., Henn, F., & Malinow, R. (2011) · Nature · doi:10.1038/nature09742 · Cited by 634 · see citing works
GABA Neurons of the VTA Drive Conditioned Place Aversion
Tan, K. R., Yvon, C., Turiault, M., Mirzabekov, J. J., Doehner, J., Labouèbe, G., Deisseroth, K. A., Tye, K. M., & Lüscher, C. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.015 · Cited by 635 · see citing works
How Addictive Drugs Disrupt Presynaptic Dopamine Neurotransmission
Sulzer, D. L. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.010 · Cited by 573 · see citing works
A Neural Circuit Mechanism for Encoding Aversive Stimuli in the Mesolimbic Dopamine System
de Jong, J. W., Afjei, S. A., Dorocic, I. P., Peck, J. R., Liu, C. J., Kim, C. K., Tian, L., Deisseroth, K. A., & Lammel, S. (2018) · Neuron · doi:10.1016/j.neuron.2018.11.005 · Cited by 506 · see citing works
Circuits and functions of the lateral habenula in health and in disease
Hu, H., Cui, Y., & Yang, Y. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0292-4 · Cited by 471 · see citing works
Reward processing by the lateral habenula in normal and depressive behaviors
Proulx, C. D., Hikosaka, O., & Malinow, R. (2014) · Nature Neuroscience · doi:10.1038/nn.3779 · Cited by 461 · see citing works
Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory
Ikemoto, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.001 · Cited by 454 · see citing works
Negative Reward Signals from the Lateral Habenula to Dopamine Neurons Are Mediated by Rostromedial Tegmental Nucleus in Primates
Hong, S., Jhou, T. C., Smith, M., Saleem, K. S., & Hikosaka, O. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.1384-11.2011 · Cited by 390 · see citing works
Nucleus Accumbens Subnuclei Regulate Motivated Behavior via Direct Inhibition and Disinhibition of VTA Dopamine Subpopulations
Yang, H., de Jong, J. W., Tak, Y., Peck, J., Bateup, H. S., & Lammel, S. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.022 · Cited by 407 · see citing works
Pavlovian to instrumental transfer: a neurobehavioural perspective.
Holmes, N. M., Marchand, A., & Coutureau, E. (2010) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.03.007 · Cited by 327 · see citing works
Neuronal circuits underlying acute morphine action on dopamine neurons
Jalabert, M., Bourdy, R., Courtin, J., Veinante, P., Manzoni, O. J., Barrot, M., & Georges, F. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105418108 · Cited by 303 · see citing works
Self-citation
Molecular characterization of the subnuclei in rat habenula
Aizawa, H., Kobayashi, M. S., Tanaka, S., Fukai, T., & Okamoto, H. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23167 · Cited by 288 · see citing works
Lateral habenula in the pathophysiology of depression
Yang, Y., Wang, H., Hu, J., & Hu, H. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.024 · Cited by 254 · see citing works
Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain
Brinschwitz, K., Dittgen, A., Madai, V. I., Lommel, R., Geisler, S., & Veh, R. W. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.03.050 · Cited by 240 · see citing works
Identification of the Zebrafish Ventral Habenula As a Homolog of the Mammalian Lateral Habenula
Amo, R., Aizawa, H., Takahoko, M., Kobayashi, M. S., Takahashi, R., Aoki, T., & Okamoto, H. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3690-09.2010 · Cited by 236 · see citing works
Separate GABA Afferents to Dopamine Neurons Mediate Acute Action of Opioids, Development of Tolerance, and Expression of Withdrawal
Matsui, A., Jarvie, B. C., Robinson, B. G., Hentges, S. T., & Williams, J. T. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.030 · Cited by 237 · see citing works
The inhibitory influence of the lateral habenula on midbrain dopamine cells: Ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus
Balcita‐Pedicino, J. J., Omelchenko, N., Bell, R., & Sesack, S. R. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22561 · Cited by 236 · see citing works
Basal ganglia circuit loops, dopamine and motivation: a review and enquiry
Ikemoto, S., Yang, C., & Tan, A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.018 · Cited by 226 · see citing works
VTA GABA Neurons at the Interface of Stress and Reward
Bouarab, C., Thompson, B. V., & Polter, A. M. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00078 · Cited by 224 · see citing works
Chronic Stress Induces Activity, Synaptic, and Transcriptional Remodeling of the Lateral Habenula Associated with Deficits in Motivated Behaviors
Cerniauskas, I., Winterer, J., de Jong, J. W., Lukacsovich, D., Yang, H., Khan, F., Peck, J. R., Obayashi, S. K., Lilascharoen, V., Lim, B. K., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.005 · Cited by 187 · see citing works
Braking Dopamine Systems: A New GABA Master Structure for Mesolimbic and Nigrostriatal Functions
Barrot, M., Sesack, S. R., Georges, F. E., Pistis, M., Hong, S., & Jhou, T. C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3370-12.2012 · Cited by 215 · see citing works
Self-citation
The Habenulo-Raphe Serotonergic Circuit Encodes an Aversive Expectation Value Essential for Adaptive Active Avoidance of Danger
Amo, R., Fredes, F., Kinoshita, M., Aoki, R., Aizawa, H., Agetsuma, M., Aoki, T., Shiraki, T., Kakinuma, H., Matsuda, M., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.035 · Cited by 207 · see citing works
A new control center for dopaminergic systems: pulling the VTA by the tail
Bourdy, R., & Barrot, M. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.06.007 · Cited by 208 · see citing works
Self-citation
Cocaine Drives Aversive Conditioning via Delayed Activation of Dopamine-Responsive Habenular and Midbrain Pathways
Jhou, T. C., Good, C. H., Rowley, C. S., Xu, S., Wang, H., Burnham, N. W., Hoffman, A. F., Lupica, C. R., & Ikemoto, S. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3634-12.2013 · Cited by 198 · see citing works
The lateral habenula in addiction and depression: an anatomical, synaptic and behavioral overview
Lecca, S., Meye, F. J., & Mameli, M. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12480 · Cited by 196 · see citing works
Opioid-Sensitive GABA Inputs from Rostromedial Tegmental Nucleus Synapse onto Midbrain Dopamine Neurons
Matsui, A., & Williams, J. T. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4570-11.2011 · Cited by 191 · see citing works
Surprise! Neural correlates of Pearce–Hall and Rescorla–Wagner coexist within the brain
Roesch, M. R., Esber, G. R., Li, J., Daw, N. D., & Schoenbaum, G. M. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07986.x · Cited by 186 · see citing works
Inhibitory Inputs from Rostromedial Tegmental Neurons Regulate Spontaneous Activity of Midbrain Dopamine Cells and Their Responses to Drugs of Abuse
Lecca, S., Melis, M., Luchicchi, A., Muntoni, A. L., & Pistis, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.302 · Cited by 185 · see citing works
Nicotine Withdrawal
McLaughlin, I., Dani, J. A., & De Biasi, M. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/978-3-319-13482-6_4 · Cited by 173 · see citing works
“…accumbens, ventral pallidum/globus pallidus, laterodorsal tegmentum, pedunculopontine nuclei, diagonal band of Broca, bed nucleus of the stria terminalis, and the caudal tip of the VTA, termed the rostromedial tegmental nucleus (RMTg) (Geisler and Zahm 2005; Jhou et al. 2009; Kaufling et al. 2009).”
Background
An update on the connections of the ventral mesencephalic dopaminergic complex
Yetnikoff, L., Lavezzi, H. N., Reichard, R. A., & Zahm, D. S. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.010 · Cited by 172 · see citing works
Efferent Pathways of the Mouse Lateral Habenula
Quina, L. A., Tempest, L., Ng, L., Harris, J. A., Ferguson, S. M., Jhou, T. C., & Turner, E. E. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23662 · Cited by 165 · see citing works
Increased CRF signalling in a ventral tegmental area-interpeduncular nucleus-medial habenula circuit induces anxiety during nicotine withdrawal
Zhao-Shea, R., DeGroot, S. R., Liu, L., Vallaster, M., Pang, X.-Y., Su, Q., Gao, G., Rando, O. J., Martin, G. E., George, O., et al. (2015) · Nature Communications · doi:10.1038/ncomms7770 · Cited by 166 · see citing works
Translating the habenula-from rodents to humans
Boulos, L.-J., Darcq, E., & Kieffer, B. L. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.06.003 · Cited by 164 · see citing works
Serotonergic modulation of the activity of mesencephalic dopaminergic systems: Therapeutic implications
Deurwaerdère, P. D., & Giovanni, G. D. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.03.004 · Cited by 164 · see citing works
The Lateral Habenula Circuitry: Reward Processing and Cognitive Control
Baker, P. M., Jhou, T. C., Li, B., Matsumoto, M., Mizumori, S. J. Y., Stephenson‐Jones, M., & Vicentic, A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2350-16.2016 · Cited by 156 · see citing works
Effects of Drugs of Abuse on Putative Rostromedial Tegmental Neurons, Inhibitory Afferents to Midbrain Dopamine Cells
Lecca, S., Melis, M., Luchicchi, A., Ennas, M. G., Castelli, M. P., Muntoni, A. L., & Pistis, M. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.190 · Cited by 158 · see citing works
Dynamic regulation of midbrain dopamine neuron activity: intrinsic, synaptic, and plasticity mechanisms
Morikawa, H., & Paladini, C. A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.023 · Cited by 150 · see citing works
Dopamine and addiction: what have we learned from 40 years of research
Solinas, M., Belujon, P., Fernagut, P., Jaber, M., & Thiriet, N. (2018) · Journal of Neural Transmission · doi:10.1007/s00702-018-1957-2 · Cited by 155 · see citing works
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
Genetic dissection of the zebrafish habenula, a possible switching board for selection of behavioral strategy to cope with fear and anxiety
Okamoto, H., Agetsuma, M., & Aizawa, H. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20913 · Cited by 142 · see citing works
Ethanol Action on Dopaminergic Neurons in the Ventral Tegmental Area
Morikawa, H., & Morrisett, R. A. (2010) · International review of neurobiology · doi:10.1016/s0074-7742(10)91008-8 · Cited by 139 · see citing works
Glial Dysfunction in the Mouse Habenula Causes Depressive-Like Behaviors and Sleep Disturbance
Cui, W., Mizukami, H., Yanagisawa, M., Aida, T., Nomura, M., Isomura, Y., Takayanagi, R., Ozawa, K., Tanaka, K., & Aizawa, H. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1465-14.2014 · Cited by 139 · see citing works
Learning shapes the aversion and reward responses of lateral habenula neurons
Wang, D., Li, Y., Feng, Q., Guo, Q., Zhou, J., & Luo, M. (2017) · eLife · doi:10.7554/elife.23045 · Cited by 141 · see citing works
PostnatalSim1Deficiency Causes Hyperphagic Obesity and ReducedMc4randOxytocinExpression
Tolson, K. P., Gemelli, T., Gautron, L., Elmquist, J. K., Zinn, A. R., & Kublaoui, B. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5444-09.2010 · Cited by 137 · see citing works
Differential projections from the lateral habenula to the rostromedial tegmental nucleus and ventral tegmental area in the rat
Gonçalves, L., Sego, C., & Metzger, M. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22787 · Cited by 134 · see citing works
Neuronal and Nonneuronal Cholinergic Structures in the Mouse Gastrointestinal Tract and Spleen
Gautron, L., Rutkowski, J. M., Burton, M. D., Wei, W., Wan, Y., & Elmquist, J. (2013) · The Journal of comparative neurology · doi:10.1002/cne.23376 · Cited by 123 · see citing works
The forgotten insular cortex: Its role on recognition memory formation
Bermúdez‐Rattoni, F. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.01.001 · Cited by 138 · see citing works
Optogenetic dissection of neural circuits underlying emotional valence and motivated behaviors
Nieh, E. H., Kim, S., Namburi, P., & Tye, K. M. (2012) · Brain Research · doi:10.1016/j.brainres.2012.11.001 · Cited by 129 · see citing works
Neuronal Nicotinic Acetylcholine Receptors: Common Molecular Substrates of Nicotine and Alcohol Dependence
Hendrickson, L. M., Guildford, M. J., & Tapper, A. R. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00029 · Cited by 132 · see citing works
Conditional viral tracing reveals that steroidogenic factor 1-positive neurons of the dorsomedial subdivision of the ventromedial hypothalamus project to autonomic centers of the hypothalamus and hindbrain
Lindberg, D., Chen, P., & Li, C. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23338 · Cited by 125 · see citing works
Lateral habenula and the rostromedial tegmental nucleus innervate neurochemically distinct subdivisions of the dorsal raphe nucleus in the rat
Sego, C., Gonçalves, L., Lima, L. B., Furigo, I. C., Donato, J., & Metzger, M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23533 · Cited by 126 · see citing works
Reward-centricity and attenuated aversions: an adolescent phenotype emerging from studies in laboratory animals
Doremus-Fitzwater, T. L., & Spear, L. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.015 · Cited by 125 · see citing works
Neurocircuitry of drug reward
Ikemoto, S., & Bonci, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.031 · Cited by 122 · see citing works
The Evolving Understanding of Dopamine Neurons in the Substantia Nigra and Ventral Tegmental Area
Gantz, S. C., Ford, C., Morikawa, H., & Williams, J. T. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021317-121615 · Cited by 122 · see citing works
Phylogeny and Ontogeny of the Habenular Structure
eAizawa, H., Amo, R., & Okamoto, H. (2011) · Frontiers in Neuroscience · doi:10.3389/fnins.2011.00138 · Cited by 119 · see citing works
Nicotinic, glutamatergic and dopaminergic synaptic transmission and plasticity in the mesocorticolimbic system: Focus on nicotine effects
Pistillo, F., Clementi, F., Zoli, M., & Gotti, C. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.10.002 · Cited by 113 · see citing works
Control of the Nigrostriatal Dopamine Neuron Activity and Motor Function by the Tail of the Ventral Tegmental Area
Bourdy, R., Sánchez-Catalán, M. J., Kaufling, J., Balcita‐Pedicino, J. J., Freund‐Mercier, M. J., Veinante, P., Sesack, S. R., Georges, F. E., & Barrot, M. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.129 · Cited by 113 · see citing works
Self-citation
Nicotine-Mediated Activation of Dopaminergic Neurons in Distinct Regions of the Ventral Tegmental Area
Zhao-Shea, R., Liu, L., Soll, L. G., Improgo, M. R., Meyers, E. E., McIntosh, J. M., Grady, S. R., Marks, M. J., Gardner, P. D., & Tapper, A. R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.240 · Cited by 113 · see citing works
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 112 · see citing works
Self-citation
Glutamate and GABA in lateral hypothalamic mechanisms controlling food intake
Stanley, B. G., Urstadt, K. R., Charles, J. R., & Kee, T. W. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.04.046 · Cited by 108 · see citing works
Opioid Modulation of Ventral Pallidal Afferents to Ventral Tegmental Area Neurons
Hjelmstad, G. O., Xia, Y., Margolis, E. B., & Fields, H. L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0178-13.2013 · Cited by 106 · see citing works
Sources of input to the rostromedial tegmental nucleus, ventral tegmental area, and lateral habenula compared: A study in rat
Yetnikoff, L., Cheng, A. Y., Lavezzi, H. N., Parsley, K. P., & Zahm, D. S. (2015) · Journal of Comparative Neurology · doi:10.1002/cne.23797 · Cited by 101 · see citing works
Lateral Habenular Burst Firing as a Target of the Rapid Antidepressant Effects of Ketamine
Cui, Y., Hu, S., & Hu, H. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2018.12.002 · Cited by 105 · see citing works
Individual neurons in the rat lateral habenular complex project mostly to the dopaminergic ventral tegmental area or to the serotonergic raphe nuclei
Bernard, R., & Veh, R. W. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23080 · Cited by 103 · see citing works
Expression of mu opioid receptor in dorsal diencephalic conduction system: New insights for the medial habenula
Gardon, O., Faget, L. C., Chung, P. C. S., Matifas, A., Massotte, D., & Kieffer, B. L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.053 · Cited by 101 · see citing works
Progress in understanding mood disorders: optogenetic dissection of neural circuits
Lammel, S., Tye, K. M., & Warden, M. R. (2014) · Genes, Brain and Behavior · doi:10.1111/gbb.12049 · Cited by 98 · see citing works
Multiplexed neurochemical signaling by neurons of the ventral tegmental area
Barker, D. J., Root, D. H., Zhang, S., & Morales, M. (2016) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2015.12.016 · Cited by 99 · see citing works
Turning a Negative into a Positive: Ascending GABAergic Control of Cortical Activation and Arousal
Brown, R. E., & McKenna, J. T. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00135 · Cited by 89 · see citing works
Error-Related Functional Connectivity of the Habenula in Humans
Ide, J. S., & Li, C. R. (2011) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2011.00025 · Cited by 89 · see citing works
Cocaine Evokes Projection-Specific Synaptic Plasticity of Lateral Habenula Neurons
Maroteaux, M. J., & Mameli, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2405-12.2012 · Cited by 92 · see citing works
Persistent Adaptations in Afferents to Ventral Tegmental Dopamine Neurons after Opiate Withdrawal
Kaufling, J., & Aston‐Jones, G. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0715-15.2015 · Cited by 89 · see citing works
Self-citation
Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat
Hahn, J. D., & Swanson, L. W. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23064 · Cited by 87 · see citing works
Review of the cytology and connections of the lateral habenula, an avatar of adaptive behaving
Zahm, D. S., & Root, D. H. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.004 · Cited by 91 · see citing works
Habenula-Induced Inhibition of Midbrain Dopamine Neurons Is Diminished by Lesions of the Rostromedial Tegmental Nucleus
Brown, P. L., Palacorolla, H., Brady, D. L., Riegger, K. E., Elmer, G. I., & Shepard, P. D. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1353-16.2016 · Cited by 90 · see citing works
Habenula cholinergic neurons regulate anxiety during nicotine withdrawal via nicotinic acetylcholine receptors
Pang, X.-Y., Liu, L., Ngolab, J., Zhao-Shea, R., McIntosh, J. M., Gardner, P. D., & Tapper, A. R. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.03.039 · Cited by 84 · see citing works
Identifying the efferent projections of leptin‐responsive neurons in the dorsomedial hypothalamus using a novel conditional tracing approach
Gautron, L., Lazarus, M., Scott, M. M., Saper, C. B., & Elmquist, J. K. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22323 · Cited by 82 · see citing works
Fos After Single and Repeated Self-Administration of Cocaine and Saline in the Rat: Emphasis on the Basal Forebrain and Recalibration of Expression
Zahm, D. S., Becker, M. L., Freiman, A. J., Strauch, S., DeGarmo, B., Geisler, S., Meredith, G. E., & Marinelli, M. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.149 · Cited by 81 · see citing works
Neural Substrates and Circuits of Drug AddictionPreprint
Feltenstein, M. W., See, R. E., & Fuchs, R. A. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a039628 · Cited by 88 · see citing works
Dopamine D 4 Receptor Excitation of Lateral Habenula Neurons via Multiple Cellular Mechanisms
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Afferent and efferent connections of the interpeduncular nucleus with special reference to circuits involving the habenula and raphe nuclei
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γ-Aminobutyric Acid Cells with Cocaine-Induced ΔFosB in the Ventral Tegmental Area Innervate Mesolimbic Neurons
Kaufling, J., Veinante, P., Pawlowski, S. A., Freund‐Mercier, M. J., & Barrot, M. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.08.001 · Cited by 73 · see citing works
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Pharmacological recruitment of the GABAergic tail of the ventral tegmental area by acute drug exposure
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The GABAergic tail of the ventral tegmental area (a new control center of the dopaminergic system)
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ΔFosB accumulates in a GABAergic cell population in the posterior tail of the ventral tegmental area after psychostimulant treatment
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DeltaFosB accumulates in a GABAergic cell population in the posterior tail of the ventral tegmental area after psychostimulant treatment
Perrotti, L. I., Bolaños, C. A., Choi, K. H., Russo, S. J., Edwards, S., Ulery, P. G., Wallace, D. L., Self, D. W., Nestler, E. J., & Barrot, M. (2005) · HAL · Cited by 13 · see citing works
Self-citation

Authors: Kaufling, J., Veinante, P., Pawlowski, S. A., Freund‐Mercier, M., & Barrot, M.
Affiliations: Centre National de la Recherche Scientifique (FR)
Corresponding author: Barrot, Michel
ORCID: Kaufling, Jennifer
Veinante, Pierre
Barrot, Michel
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 2009-02-20
Volume: 513
Issue: 6
Pages: 597-621
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.21983
OpenAlex: W1995790991
Cited by: 347
References: 86
Citations by year: 2026: 9 · 2025: 8 · 2024: 17 · 2023: 11 · 2022: 11 · 2021: 15 · 2020: 32 · 2019: 21 · 2018: 20 · 2017: 20 · 2016: 29 · 2015: 22 · 2014: 27 · 2013: 25 · 2012: 24
FWCI: 10.92
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
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 › Neurology › Neurological disorders and treatments
Keywords: ventral tegmental area, GABAergic neurons, afferent projections, ΔFosB, glutamic acid decarboxylase, cocaine, medial prefrontal cortex, lateral habenula, dorsal raphe nucleus, locus coeruleus, central amygdala, ventral pallidum, bed nucleus of the stria terminalis, substantia innominata, preoptic area, hypothalamus, superior colliculus, periaqueductal gray, reticular formation, dopaminergic neurons
MeSH terms: Animals, Cocaine, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Male, Neurons, Gene Expression, Proto-Oncogene Proteins c-fos, Rats, Sprague-Dawley, Ventral Tegmental Area, Rats

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Afferents to the GABAergic tail of the ventral tegmental area in the rat

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