Identification of Brain Nuclei Implicated in Cocaine-Primed Reinstatement of Conditioned Place Preference: A Behaviour Dissociable from Sensitization
Open accessAbstract
Relapse prevention represents the primary therapeutic challenge in the treatment of drug addiction. As with humans, drug-seeking behaviour can be precipitated in laboratory animals by exposure to a small dose of the drug (prime). The aim of this study was to identify brain nuclei implicated in the cocaine-primed reinstatement of a conditioned place preference (CPP). Thus, a group of mice were conditioned to cocaine, had this place preference extinguished and were then tested for primed reinstatement of the original place preference. There was no correlation between the extent of drug-seeking upon reinstatement and the extent of behavioural sensitization, the extent of original CPP or the extinction profile of mice, suggesting a dissociation of these components of addictive behaviour with a drug-primed reinstatement. Expression of the protein product of the neuronal activity marker c-fos was assessed in a number of brain regions of mice that exhibited reinstatement (R mice) versus those which did not (NR mice). Reinstatement generally conferred greater Fos expression in cortical and limbic structures previously implicated in drug-seeking behaviour, though a number of regions not typically associated with drug-seeking were also activated. In addition, positive correlations were found between neural activation of a number of brain regions and reinstatement behaviour. The most significant result was the activation of the lateral habenula and its positive correlation with reinstatement behaviour. The findings of this study question the relationship between primed reinstatement of a previously extinguished place preference for cocaine and behavioural sensitization. They also implicate activation patterns of discrete brain nuclei as differentiators between reinstating and non-reinstating mice.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Activation of the habenula in animal models of cocaine addiction has been associated with relapse to drug taking upon cue exposure.
“Indeed, activation of the habenula, in animal models of cocaine addiction, has been associated with relapse to drug taking upon cue exposure (153,154).”
From Obesity and addiction: Neurobiological overlaps (2013) · cites this paper as [154]
In animal models of cocaine or heroin addiction, activation of the lateral habenula is associated with relapse.
“Indeed, activation of the lateral habenula, in animal models of cocaine or heroin addiction, has been associated with relapse (108,109).”
From The Addictive Dimensionality of Obesity (2013) · cites this paper as [109]
Activation of the habenula in cocaine addicted subjects has been associated with behavioral relapse to drug taking upon cue exposure.
“Indeed, activation of the habenula, in cocaine addicted subjects, has been associated with behavioral relapse to drug taking upon cue exposure (Brown et al 2011;Zhang et al 2005).”
From Food and Drug Reward: Overlapping Circuits in Human Obesity and Addiction (2011) · cites this paper as Brown et al 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
The neural basis of drug craving: An incentive-sensitization theory of addiction
Robinson, T. (1993) · Brain Research Reviews · doi:10.1016/0165-0173(93)90013-p · Cited by 7,346 · see citing works
The Neural Basis of Addiction: A Pathology of Motivation and Choice
Kalivas, P. W., & Volkow, N. D. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.8.1403 · Cited by 2,757 · see citing works
Morgan, J., & Curran, T. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.002225 · Cited by 2,689 · see citing works
The reinstatement model of drug relapse: history, methodology and major findings
Shaham, Y., Shalev, U., Lu, L., de Wit, H., & Stewart, J. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1224-x · Cited by 1,615 · see citing works
The psychology and neurobiology of addiction: an incentive–sensitization view
Robinson, T. E., & Berridge, K. C. (2000) · Addiction · doi:10.1046/j.1360-0443.95.8s2.19.x · Cited by 1,507 · see citing works
The use of c-fos as a metabolic marker in neuronal pathway tracing
Dragunow, M., & Faull, R. (1989) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(89)90150-7 · Cited by 1,416 · see citing works
A role for lateral hypothalamic orexin neurons in reward seeking
Harris, G. C., Wimmer, M., & Aston-Jones, G. (2005) · Nature · doi:10.1038/nature04071 · Cited by 1,311 · see citing works
Lateral habenula as a source of negative reward signals in dopamine neurons
Matsumoto, M., & Hikosaka, O. (2007) · Nature · doi:10.1038/nature05860 · Cited by 1,292 · see citing works
Tzschentke, T. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00060-4 · Cited by 1,254 · see citing works
Graybiel, A. M., Moratalla, R., & Robertson, H. A. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.17.6912 · Cited by 957 · see citing works
The role of ventromedial prefrontal cortex in the recovery of extinguished fear
Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06225.2000 · Cited by 957 · cited 1× · see citing works
“These data are challenged by studies which implicate the infralimbic cortex in the extinguished response and hence the inhibition of cocaine-seeking [49,50,51,52].”
BackgroundActivation of memory circuits during cue-elicited cocaine craving.
Grant, S., London, E. D., Newlin, D. B., Villemagne, V. L., Liu, X., Contoreggi, C., Phillips, R. L., Kimes, A. S., & Margolin, A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.12040 · Cited by 936 · see citing works
Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology
Watson, R. E., Wiegand, S. J., Clough, R. W., & Hoffman, G. E. (1986) · Peptides · doi:10.1016/0196-9781(86)90076-8 · Cited by 933 · see citing works
The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior
McFarland, K., & Kalivas, P. W. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-21-08655.2001 · Cited by 905 · see citing works
Herrera, D., & Robertson, H. A. (1996) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00021-4 · Cited by 713 · see citing works
Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure
Epstein, D., Preston, K., Stewart, J., & Shaham, Y. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0529-6 · Cited by 634 · see citing works
Markou, A., Weiss, F., Gold, L. H., Caine, S. B., Schulteis, G., & Koob, G. F. (1993) · Psychopharmacology · doi:10.1007/bf02244907 · Cited by 551 · see citing works
Infralimbic Prefrontal Cortex Is Responsible for Inhibiting Cocaine Seeking in Extinguished Rats
Peters, J., LaLumiere, R. T., & Kalivas, P. W. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1045-08.2008 · Cited by 537 · see citing works
Limbic and Motor Circuitry Underlying Footshock-Induced Reinstatement of Cocaine-Seeking Behavior
McFarland, K., Davidge, S. B., Lapish, C. C., & Kalivas, P. W. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4177-03.2004 · Cited by 524 · see citing works
Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior
Boutrel, B., Kenny, P. J., Specio, S. E., Martin-Fardon, R., Markou, A., Koob, G. F., & de Lecea, L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507480102 · Cited by 520 · see citing works
Cocaine induces striatal c-fos-immunoreactive proteins via dopaminergic D1 receptors.
Young, S., Porrino, L. J., & Iadarola, M. J. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.4.1291 · Cited by 497 · see citing works
Hope, B. T., Kosofsky, B. E., Hyman, S. E., & Nestler, E. J. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5764 · Cited by 474 · see citing works
Psychological stress, drug-related cues and cocaine craving
Sinha, R., Fuse, T., Aubin, L.-R., & O'Malley, S. S. (2000) · Psychopharmacology · doi:10.1007/s002130000499 · Cited by 463 · see citing works
Neisewander, J. L., Baker, D. L., Fuchs, R. A., Tran-Nguyen, L. T. L., Palmer, A., & Marshall, J. F. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-02-00798.2000 · Cited by 438 · see citing works
Habenula: crossroad between the basal ganglia and the limbic system
Hikosaka, O., Sesack, S. R., Lecourtier, L., & Shepard, P. D. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3463-08.2008 · Cited by 432 · see citing works
The orexin system regulates alcohol-seeking in rats
Lawrence, A. J., Cowen, M. S., Yang, H., Chen, F., & Oldfield, B. (2006) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706789 · Cited by 392 · see citing works
Self-citationStress, vulnerability and adult alcohol relapse.
Brown, S. A., Vik, P. W., Patterson, T. L., Grant, I., & Schuckit, M. A. (1995) · Journal of Studies on Alcohol · doi:10.15288/jsa.1995.56.538 · Cited by 380 · see citing works
Wagner, F. A. (2002) · American Journal of Epidemiology · doi:10.1093/aje/155.10.918 · Cited by 380 · see citing works
Ciccocioppo, R., Sanna, P. P., & Weiss, F. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.4.1976 · Cited by 371 · see citing works
Comer, S. D., Sullivan, M. A., Yu, E., Rothenberg, J. L., Kleber, H. D., Kampman, K., Dackis, C., & O’Brien, C. P. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.2.210 · Cited by 348 · see citing works
Erb, S. M., & Stewart, J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-j0006.1999 · Cited by 347 · see citing works
Vries, T. J. D., Schoffelmeer, A. N. M., Binnekade, R., Mulder, A. H., & Vanderschuren, L. J. M. J. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00368.x · Cited by 332 · see citing works
Mueller, D. T., & Stewart, J. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00239-4 · Cited by 324 · see citing works
Cocaine dependence: a disease of the brain’s reward centers
Dackis, C. A., & O’Brien, C. P. (2001) · Journal of Substance Abuse Treatment · doi:10.1016/s0740-5472(01)00192-1 · Cited by 322 · see citing works
Leri, F., Flores, J., Rodaros, D., & Stewart, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05713.2002 · Cited by 292 · see citing works
Salmaso, N., Rodaros, D., Stewart, J., & Erb, S. (2001) · Psychopharmacology · doi:10.1007/s002130000642 · Cited by 291 · see citing works
Brown, E., Robertson, G. S., & Fibiger, H. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-10-04112.1992 · Cited by 288 · see citing works
Takagishi, M., & Chiba, T. (1991) · Brain Research · doi:10.1016/0006-8993(91)91677-s · Cited by 284 · see citing works
Neurobiology of relapse to heroin and cocaine seeking: An update and clinical implications
Bossert, J. M., Ghitza, U. E., Lü, L., Epstein, D. H., & Shaham, Y. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.09.030 · Cited by 271 · see citing works
Neurobiological mechanisms of the reinstatement of drug-conditioned place preference
Aguilar, M. A., Rodríguez‐Arias, M., & Miñarro, J. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.08.002 · Cited by 270 · see citing works
Lapse, Relapse and Survival among Opiate Addicts after Treatment
Gossop, M., Green, L., Phillips, G., & Bradley, B. P. (1989) · The British Journal of Psychiatry · doi:10.1192/bjp.154.3.348 · Cited by 230 · see citing works
Rogers, J. L., Ghee, S. M., & See, R. E. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.10.012 · Cited by 204 · see citing works
Drugs of abuse and immediate-early genes in the forebrain
Harlan, R. E., & Garcia, M. M. (1998) · Molecular Neurobiology · doi:10.1007/bf02741385 · Cited by 198 · see citing works
Shaham, Y., & Stewart, J. (1996) · Psychopharmacology · doi:10.1007/bf02246022 · Cited by 194 · see citing works
Orbitomedial prefrontal cortical projections to hypothalamus in the rat
Floyd, N. S., Price, J. L., Ferry, A. T., Keay, K. A., & Bandler, R. J. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1105 · Cited by 175 · see citing works
Renewal of extinguished cocaine-seeking
Hamlin, A. S., Clemens, K. J., & McNally, G. P. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.11.018 · Cited by 164 · see citing works
Sanchez, C. J., Bailie, T. M., Wu, W.-R., Li, N., & Sorg, B. A. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00078-2 · Cited by 160 · see citing works
Distinct Patterns of Neural Activation Associated with Ethanol Seeking: Effects of Naltrexone
Dayas, C. V., Liu, X., Simms, J. A., & Weiss, F. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.07.034 · Cited by 152 · see citing works
The Lateral Habenula:No Longer Neglected
Geisler, S., & Trimble, M. (2008) · CNS Spectrums · doi:10.1017/s1092852900016710 · Cited by 149 · see citing works
Conditioned craving and arousal in cocaine addiction: a preliminary report.
Childress, A. R., Ehrman, R. N., McLellan, A. T., & O'Brien, C. P. (1988) · PubMed · Cited by 138 · see citing works
Crawford, C. A., McDougall, S. A., Bolaños, C. A., Hall, S. E., & Berger, S. P. (1995) · Psychopharmacology · doi:10.1007/bf02245810 · Cited by 130 · see citing works
Franklin, T. R., & Druhan, J. P. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00071.x · Cited by 126 · see citing works
Pharmacological validation of a new animal model of alcoholism
Spanagel, R., & Hölter, S. M. (2000) · Journal of Neural Transmission · doi:10.1007/s007020070068 · Cited by 126 · see citing works
Rhodes, S. E. V., & Killcross, S. (2004) · Learning & Memory · doi:10.1101/lm.79704 · Cited by 119 · see citing works
Parker, L. A., & McDonald, R. V. (2000) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(00)00222-7 · Cited by 117 · see citing works
Medial preoptic area/anterior hypothalamus and sexual motivation
Paredes, R. G. (2003) · Scandinavian Journal of Psychology · doi:10.1111/1467-9450.00337 · Cited by 115 · see citing works
Lü, L., Liu, D., & Ceng, X. (2001) · European Journal of Pharmacology · doi:10.1016/s0014-2999(01)00840-8 · Cited by 98 · see citing works
Brain mechanisms of aggressive behavior: an updated review.
Adams, D. B. (2006) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.09.004 · Cited by 97 · see citing works
Kufahl, P. R., Zavala, A. R., Singh, A., Thiel, K. J., Dickey, E. D., Joyce, J. N., & Neisewander, J. L. (2009) · Synapse · doi:10.1002/syn.20666 · Cited by 96 · see citing works
Zavala, A. R., Weber, S. M., Rice, H. J., Alleweireldt, A. T., & Neisewander, J. L. (2003) · Brain Research · doi:10.1016/s0006-8993(03)03452-8 · Cited by 90 · see citing works
Conditioned fear stimuli reinstate cocaine-induced conditioned place preference
Sanchez, C. J., & Sorg, B. A. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02638-5 · Cited by 81 · see citing works
Lesions of rat infralimbic cortex enhance renewal of extinguished appetitive Pavlovian responding
Rhodes, S. E., & Killcross, A. S. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05486.x · Cited by 80 · see citing works
Relapse Prevention: An Emerging Technology for Promoting Long-Term Drug Abstinence
DeJong, W. (1994) · International Journal of the Addictions · doi:10.3109/10826089409047904 · Cited by 79 · see citing works
Hrabovszky, E., Halász, J., Meelis, W., Kruk, M. R., Liposits, Z., & Haller, J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.03.042 · Cited by 78 · see citing works
Self-stimulation of the habenular complex in the rat.
Sutherland, R. J., & Nakajima, S. (1981) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077833 · Cited by 77 · see citing works
Zavala, A. R., Biswas, S., Harlan, R. E., & Neisewander, J. L. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.12.038 · Cited by 77 · see citing works
Biała, G., & Budzyńska, B. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.03.017 · Cited by 67 · see citing works
Medial prefrontal cortical integration of psychological stress in rats
McDougall, S. J., Widdop, R. E., & Lawrence, A. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03707.x · Cited by 65 · see citing works
Self-citationBrown, R. M., Short, J. L., Cowen, M. S., Ledent, C. A., & Lawrence, A. J. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.72 · Cited by 60 · see citing works
Self-citationProgress in the science of addiction
O'Brien, C. P. (1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.9.1195 · Cited by 52 · see citing works
Zhang, F., Zhou, W., Liu, H., Zhu, H., Tang, S., Lai, M., & Yang, G. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.06.008 · Cited by 51 · see citing works
McPherson, C. S., & Lawrence, A. J. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705005845 · Cited by 44 · see citing works
Self-citationElectrolytic lesions of the habenula attenuate brain stimulation reward
Morissette, M.-C., & Boye, S. M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.08.021 · Cited by 43 · see citing works
Bilbao, A., Parkitna, J. M. R., Engblom, D., Perreau‐Lenz, S., Sanchis‐Segura, C., Schneider, M., Konopka, W., Westphal, M., Breen, G. D., Desrivières, S., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803959105 · Cited by 43 · see citing works
Font, L., Miquel, M., & Aragón, C. M. G. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.026 · Cited by 37 · see citing works
Acute cocaine effects on stereotypy and defense: an ethoexperimental approach
Blanchard, R. J., Hebert, M. A., Dulloog, L., Kaawaloa, N., Nishimura, O., & Blanchard, D. C. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00019-0 · Cited by 36 · see citing works
Dorsal diencephalic self-stimulation: A movable electrode mapping study.
Vachon, M. P., & Miliaressis, E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.6.981 · Cited by 35 · see citing works
Cruz, F. C., Marin, M. T., & Planeta, C. S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.10.019 · Cited by 34 · see citing works
CONDITIONING MECHANISMS IN DRUG DEPENDENCE
O’Brien, C. P., Childress, A. R., Ehrman, R. N., Robbins, S. J., & McLellan, A. T. (1992) · Clinical Neuropharmacology · doi:10.1097/00002826-199201001-00036 · Cited by 32 · see citing works
Hebert, M. A., Blanchard, D. C., & Blanchard, R. J. (1999) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(98)00255-x · Cited by 30 · see citing works
Dorsal diencephalic self-stimulation: A movable electrode mapping study.
Vachon, M. P., & Miliaressis, E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.6.981 · Cited by 28 · see citing works
Lateral hypothalamus dopamine D1-like receptors and glucose-conditioned flavor preferences in rats
Touzani, K., Bodnar, R. J., & Sclafani, A. J. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.06.006 · Cited by 27 · see citing works
Neurochemistry Underlying Relapse to Opiate Seeking Behaviour
Brown, R. M., & Lawrence, A. J. (2009) · Neurochemical Research · doi:10.1007/s11064-009-9967-y · Cited by 18 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Obesity and addiction: Neurobiological overlaps
Volkow, N. D., Wang, G. ‐., Tomasi, D., & Baler, R. D. (2013) · Obesity Reviews · doi:10.1111/j.1467-789x.2012.01031.x · Cited by 800 · see citing works
Addiction circuitry in the human brain
Volkow, N. D., Wang, G.-J., Fowler, J. S., & Tomasi, D. (2012) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134625 · Cited by 592 · see citing works
Food and Drug Reward: Overlapping Circuits in Human Obesity and Addiction
Volkow, N. D., Wang, G. J., Fowler, J. S., Tomasi, D., & Baler, R. (2011) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2011_169 · Cited by 525 · see citing works
The Addictive Dimensionality of Obesity
Volkow, N. D., Wang, G.-J., Tomasi, D., & Baler, R. D. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.12.020 · Cited by 380 · see citing works
Pain and suicidality: Insights from reward and addiction neuroscience
Elman, I., Borsook, D., & Volkow, N. D. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.06.003 · Cited by 220 · see citing works
Unbalanced neuronal circuits in addiction
Volkow, N. D., Wang, G.-J., Tomasi, D. G., & Baler, R. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.002 · Cited by 219 · 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
Addiction science: Uncovering neurobiological complexity
Volkow, N. D., & Baler, R. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.007 · Cited by 194 · see citing works
Shifted pallidal co-release of GABA and glutamate in habenula drives cocaine withdrawal and relapse
Meye, F. J., Soiza-Reilly, M., Smit, T., Diana, M. A., Schwarz, M. K., & Mameli, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4334 · Cited by 173 · 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
The role of the habenula in drug addiction
Velasquez, K. M., Molfese, D. L., & Salas, R. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00174 · Cited by 155 · see citing works
The thalamus in drug addiction: from rodents to humans
Huang, A., Mitchell, J. A., Haber, S. N., Nelly Alia-klein, A., & Goldstein, R. Z. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0028 · Cited by 116 · see citing works
Wright, K. N., Hollis, F., Duclot, F., Dossat, A. M., Strong, C. E., Francis, T. C., Mercer, R., Feng, J., Dietz, D., Lobo, M. K., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.5227-14.2015 · Cited by 103 · see citing works
Guzmán, M. S., Jaeger, X. D., Raulic, S., Souza, I. A., Li, A. X., Schmid, S., Menon, R. S., Gainetdinov, R. R., Caron, M. G., Bartha, R., et al. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001194 · Cited by 94 · see citing works
Meyer, P., Ma, S. T., & Robinson, T. E. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2429-7 · Cited by 93 · 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
The habenula in psychiatric disorders: More than three decades of translational investigation
Fakhoury, M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.010 · Cited by 90 · see citing works
James, M. H., Charnley, J. L., Flynn, J. R., Smith, D. W., & Dayas, C. V. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.047 · Cited by 77 · see citing works
Nair, S. G., Strand, N. S., & Neumaier, J. F. (2012) · Brain Research · doi:10.1016/j.brainres.2012.10.011 · Cited by 72 · see citing works
The Role of the Medial Habenula Cholinergic System in Addiction and Emotion-Associated Behaviors
Lee, H. W., Yang, S. H., Kim, J. Y., & Kim, H. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00100 · Cited by 69 · see citing works
Hong, S., & Hikosaka, O. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00778 · Cited by 63 · see citing works
Chesworth, R., Brown, R. M., Kim, J. H., & Lawrence, A. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068371 · Cited by 53 · see citing works
Self-citationCastilla‐Ortega, E., Blanco, E., Serrano, A., de Guevara‐Miranda, D. L., Pedraz, M., Estivill‐Torrús, G., Pavón, F. J., de Fonseca, F. R., & Santín, L. J. (2015) · Addiction Biology · doi:10.1111/adb.12248 · Cited by 47 · see citing works
Lax, E., Friedman, A., Croitoru, O., Sudai, E., Ben‐Moshe, H., Redlus, L., Sasson, E., Blumenfeld‐Katzir, T., Assaf, Y., & Yadid, G. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.06.034 · Cited by 40 · see citing works
Effects of acupuncture on stress-induced relapse to cocaine-seeking in rats
Yoon, S. S., Yang, E. J., Lee, B. H., Jang, E. Y., Kim, H. Y., Choi, S., Steffensen, S. C., & Yang, C. H. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2683-3 · Cited by 39 · see citing works
Information processing in the vertebrate habenula
Fore, S., Palumbo, F., Pelgrims, R., & Yaksi, E. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.08.019 · Cited by 35 · see citing works
Madsen, H. B., Brown, R. M., Short, J. L., & Lawrence, A. J. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.225219 · Cited by 34 · see citing works
Self-citationLateral habenula deep brain stimulation for personalized treatment of drug addiction
Yadid, G., Gispan, I. H., & Lax, E. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00806 · Cited by 31 · see citing works
Koob, G. F., Kandel, D. B., Baler, R., & Volkow, N. D. (2023) · Springer eBooks · doi:10.1007/978-3-030-42825-9_29-1 · Cited by 31 · see citing works
Moreno‐Gómez‐Toledano, R., Arenas, M. I., González-Martínez, C., Olea‐Herrero, N., Reventún, P., Nunzio, M. D., Sánchez, S. G., Arilla, E., Saura, M., & Bosch, R. J. (2020) · Scientific Reports · doi:10.1038/s41598-020-73636-6 · Cited by 28 · see citing works
mGlu5 and adenosine A2A receptor interactions regulate the conditioned effects of cocaine
Brown, R. M., Duncan, J. R., Stagnitti, M. R., Ledent, C. A., & Lawrence, A. J. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114571100126x · Cited by 25 · see citing works
Self-citationRogg, M., Yasuda‒Yamahara, M., Abed, A., Dinse, P., Helmstädter, M., Conzelmann, A.-C., Frimmel, J., Sellung, D., Biniossek, M. L., Kretz, O., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-15844-1 · Cited by 24 · see citing works
Montesinos, J., Castilla‐Ortega, E., Sánchez‐Marín, L., Montagud‐Romero, S., Araos, P. F., Pedraz, M., Porras-Perales, Ó., García‐Marchena, N., Serrano, A., Suárez, J., et al. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107840 · Cited by 24 · see citing works
Clough, S. J., Hutchinson, A. J., Hudson, R. L., & Dubocovich, M. L. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.04.049 · Cited by 23 · see citing works
Lateral habenula cannabinoid CB1 receptor involvement in drug-associated impulsive behavior
Zapata, A. G., & Lupica, C. R. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108604 · Cited by 22 · see citing works
Adenosine 2 A receptors modulate reward behaviours for methamphetamine
Chesworth, R., Brown, R. M., Kim, J. H., Ledent, C. A., & Lawrence, A. J. (2015) · Addiction Biology · doi:10.1111/adb.12225 · Cited by 19 · see citing works
Self-citationKim, J. H., Lavan, D., Chen, N. A., Flores, C., Cooper, H. M., & Lawrence, A. J. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3187-5 · Cited by 19 · see citing works
Self-citationScheller, K. J., Williams, S. J., Lawrence, A. J., & Djouma, E. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.03.004 · Cited by 19 · see citing works
Self-citationAllosteric modulation of muscarinic receptors in alcohol and substance use disorders
Walker, L. C., & Lawrence, A. J. (2020) · Advances in pharmacology · doi:10.1016/bs.apha.2020.01.003 · Cited by 18 · see citing works
Self-citationLucke-Wold, B. P. (2011) · PubMed · Cited by 17 · see citing works
Puhl, M. D., Berg, A., Bechtholt, A. J., & Coyle, J. T. (2015) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.115.223099 · Cited by 17 · see citing works
Nair, S. G., Smirnov, D. S., Estabrook, M. M., Chisholm, A. D., Silva, P. R., & Neumaier, J. F. (2020) · Addiction Biology · doi:10.1111/adb.12865 · Cited by 17 · see citing works
Liu, Q., Zhang, M., Qin, W., Wang, Y., Li, Y., Li, J., Li, J., Lawrence, A. J., & Liang, J. (2012) · Brain Research · doi:10.1016/j.brainres.2012.03.027 · Cited by 17 · see citing works
Self-citationAshby, C. R., Rice, O. V., Heidbreder, C. A., & Gardner, E. L. (2015) · Synapse · doi:10.1002/syn.21820 · Cited by 14 · see citing works
HMG-CoA synthase 2 drives brain metabolic reprogramming in cocaine exposure
Shao, X., Tang, Y., Long, H., Gu, H., Zhang, J., Deng, P., Zhao, Y., & Cen, X. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.10.001 · Cited by 13 · see citing works
Koob, G. F., Kandel, D. B., Baler, R., & Volkow, N. D. (2015) · Wiley eBooks · doi:10.1002/9781118753378.ch22 · Cited by 13 · see citing works
Buffalari, D. M., & Rinaman, L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.017 · Cited by 12 · see citing works
Wickens, R. H., Quartarone, S. E., & Beninger, R. J. (2016) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000283 · Cited by 12 · see citing works
Guerin, A. A., Zbukvic, I., Luikinga, S. J., Drummond, K. D., Lawrence, A. J., Madsen, H. B., & Kim, J. H. (2020) · Developmental Psychobiology · doi:10.1002/dev.22017 · Cited by 12 · see citing works
Self-citationOrexin Receptor Targets for Anti-Relapse Medication Development in Drug Addiction
Zhou, L., Sun, W., & See, R. E. (2011) · Pharmaceuticals · doi:10.3390/ph4060804 · Cited by 11 · see citing works
Addiction Circuitry in the Human Brain
Volkow, N. D., Wang, G., Fowler, J. S., & Tomasi, D. G. (2015) · FOCUS The Journal of Lifelong Learning in Psychiatry · doi:10.1176/appi.focus.130306 · Cited by 11 · see citing works
You, I., Hong, S., Ma, S., Nguyen, T., Kwon, S., Lee, S., & Jang, C. (2019) · Journal of Psychopharmacology · doi:10.1177/0269881119864943 · Cited by 10 · see citing works
Gill, K. E., Reynolds, A. R., Prendergast, M., & Akins, C. K. (2016) · Experimental and Clinical Psychopharmacology · doi:10.1037/pha0000070 · Cited by 8 · see citing works
Orsini, C., Bonito-Oliva, A., Montanari, C., Conversi, D., & Cabib, S. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.06.021 · Cited by 7 · see citing works
Cullity, E. R., Guerin, A. A., Madsen, H. B., Perry, C. J., & Kim, J. H. (2021) · Neuroanatomy and Behaviour · doi:10.35430/nab.2021.e24 · Cited by 7 · see citing works
Nguyen, A. T. M., Quach, T. V. B., Kotha, P., Chien, S.-Y., MacDonald, I. J., Lane, H., Tu, C., Lin, J., & Chen, Y. (2021) · Scientific Reports · doi:10.1038/s41598-021-93014-0 · Cited by 6 · see citing works
Gakare, S. G., & Ugale, R. R. (2023) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000728 · Cited by 4 · see citing works
A method for evaluating cocaine-induced social preference in rats
Dingess, P. M., Deters, M. J., Darling, R. A., Yarborough, E. A., & Brown, T. E. (2017) · Journal of Biological Methods · doi:10.14440/jbm.2017.145 · Cited by 3 · see citing works
Koob, G. F., Kandel, D. B., Baler, R., & Volkow, N. D. (2024) · Springer eBooks · doi:10.1007/978-3-030-51366-5_29 · Cited by 1 · see citing works
Matzeu, A., Flores‐Ramirez, F. J., & Martin‐Fardon, R. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-823453-2.00012-6 · Cited by 1 · see citing works
Neural mechanisms of MK-801 induced sensitisation
Lefevre, E. M. (2016) · The University of Queensland · doi:10.14264/uql.2016.911 · Cited by 1 · see citing works
Mu opioid receptors in the habenula : dissecting reward and aversion in addiction
Boulos, L. (2017) · HAL · doi:10.70675/4ec6ce3az48cbz4a77za34ezb8b76b41f629 · Cited by 1 · see citing works
The Effects of Binge-Like Sucrose Consumption on the Mesolimbic Reward Pathway in the Brain
Shariff, M. R. (2017) · Queensland University of Technology · doi:10.5204/thesis.eprints.107900
Xie, Q., Namba, M. D., Dasari, R., Buck, L. A., Side, C. M., Goldberg, S. L., Park, K., Jackson, J. G., Giacometti, L. L., & Barker, J. M. (2025) · Psychopharmacology · doi:10.1007/s00213-025-06849-0
Pérez-Berlanga, J. M., Pérez-Cano, A. M., Ávila‐Gámiz, F., Gómez-Roldán, M. D. C., Santín, L. J., & de Guevara‐Miranda, D. L. (2026) · Behavioural Brain Research · doi:10.1016/j.bbr.2026.116528
Gill, K. E. (2015) · UKnowledge (University of Kentucky)
- Authors
- Brown, R. M., Short, J. L., & Lawrence, A. J.
- Affiliations
- The University of Melbourne (AU)
- Corresponding author
- Lawrence, Andrew John
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-12-29
- Volume
- 5
- Issue
- 12
- Pages
- e15889
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3012115
- OpenAlex
- W2093084898
- Cited by
- 69
- References
- 83
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 3 · 2021: 3 · 2020: 4 · 2019: 3 · 2018: 1 · 2017: 9 · 2016: 6 · 2015: 8 · 2014: 4 · 2013: 11 · 2012: 6
- FWCI
- 3.23
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- State Government of Victoria
- National Health and Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- cocaine, reinstatement, conditioned place preference, drug-seeking behavior, relapse, drug sensitization, lateral habenula, Fos expression, neuronal activation, extinction, addiction
- MeSH terms
- Animals, Behavior, Animal, Brain, Cell Nucleus, Cocaine, Conditioning, Psychological, Conditioning, Operant, Immunohistochemistry, Male, Neurons, Reinforcement, Psychology, Behavior, Addictive, Proto-Oncogene Proteins c-fos, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review