Role of Projections from Ventral Medial Prefrontal Cortex to Nucleus Accumbens Shell in Context-Induced Reinstatement of Heroin Seeking
Open accessAbstract
In humans, exposure to contexts previously associated with heroin use can provoke relapse. In rats, exposure to heroin-paired contexts after extinction of drug-reinforced responding in different contexts reinstates heroin seeking. This effect is attenuated by inhibition of glutamate or dopamine transmission in nucleus accumbens shell, or inactivation of ventral medial prefrontal cortex (mPFC). Here, we used an anatomical asymmetrical disconnection procedure to demonstrate that an interaction between glutamatergic projections from ventral mPFC to accumbens shell and local dopamine D 1 postsynaptic receptors contributes to context-induced reinstatement of heroin seeking. We also combined the marker of neuronal activity, Fos, with the retrograde tracer Fluoro-Gold to assess activation in this pathway during context-induced reinstatement. Rats were trained to self-administer heroin for 12 d; drug infusions were paired with a discrete tone–light cue. Lever pressing was subsequently extinguished in a nondrug-associated context in the presence of the discrete cue. Rats were then tested in the heroin- or extinction-associated contexts under extinction conditions. Injections of muscimol + baclofen into ventral mPFC in one hemisphere and D 1-family receptor antagonist SCH 23390 into the contralateral or ipsilateral accumbens shell decreased context-induced reinstatement. Unilateral injections of muscimol + baclofen into ventral mPFC or SCH 23390 into the accumbens shell had no effect. Context-induced reinstatement was associated with increased Fos expression in ventral mPFC neurons, including those projecting to accumbens shell, with higher double-labeling in the ipsilateral projection than in the contralateral projection. Our results demonstrate that activation of glutamatergic projections from ventral mPFC to accumbens shell, previously implicated in inhibition of cocaine relapse, promotes heroin relapse.
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?
Performance on conditional discrimination tasks is dependent upon the intact functioning of the nucleus accumbens.
“Previous animal studies have revealed that performance on conditional discrimination tasks is dependent upon the intact functioning of the nucleus accumbens [64, 65].”
From Linking haploinsufficiency of the autism- and schizophrenia-associated gene Cyfip1 with striatal-limbic-cortical network dysfunction and cognitive inflexibility (2024) · cites this paper as [65]
The Introduction and Results address the accumbens shell’s role in context-induced reinstatement of heroin seeking, not performance on conditional discrimination tasks. Searches for “conditional discrimination tasks” and “nucleus accumbens lesions conditional discrimination performance” found no passage in our copy addressing the claimed task dependence; page numbers were not available. (LLM, conf=0.73)
Experimental — accuracy not yet measured
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
Expression of c- <i>fos</i> Protein in Brain: Metabolic Mapping at the Cellular Level
Sagar, S. M., Sharp, F. R., & Curran, T. (1988) · Science · doi:10.1126/science.3131879 · Cited by 1,925 · see citing works
Heroin and cocaine intravenous self-administration in rats: Mediation by separate neural systems
Ettenberg, A., Pettit, H. O., Bloom, F. E., & Koob, G. F. (1982) · Psychopharmacology · doi:10.1007/bf00428151 · Cited by 563 · see citing works
Everitt, B. J., Morris, K. A., O'Brien, A., & Robbins, T. W. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90145-e · Cited by 507 · see citing works
Mesocorticolimbic Glutamatergic Pathway
Yamaguchi, T., Wang, H.-L., Li, X., Ng, T. H., & Morales, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1598-11.2011 · Cited by 332 · see citing works
Self-citationPrefrontal cortex AMPA receptor plasticity is crucial for cue-induced relapse to heroin-seeking
Van den Oever, M. C., Goriounova, N. A., Wan Li, K., Van der Schors, R. C., Binnekade, R., Schoffelmeer, A. N. M., Mansvelder, H. D., Smit, A. B., Spijker, S., & De Vries, T. J. (2008) · Nature Neuroscience · doi:10.1038/nn.2165 · Cited by 206 · see citing works
Anderson, S. M., Bari, A. A., & Pierce, R. C. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1298-5 · Cited by 178 · see citing works
Lasseter, H. C., Wells, A. M., Xie, X., & Fuchs, R. A. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.209 · Cited by 72 · see citing works
Flagged first, then by citations
Research works printed but not linked: 76
- Alvarez-Jaimes L Polis I Parsons LH 2008 Attenuation of cue-induced heroin-seeking behavior by cannabinoid CB1 antagonist infusions into the nucleus accumbens core and prefrontal cortex, but not basolateral amygdala Neuropsychopharmacology 33 2483 2493 18059440
- Anderson SM Schmidt HD Pierce RC 2006 Administration of the D2 dopamine receptor antagonist sulpiride into the shell, but not the core, of the nucleus accumbens attenuates cocaine priming-induced reinstatement of drug seeking Neuropsychopharmacology 31 1452 1461 16205775
- Badiani A Belin D Epstein D Calu D Shaham Y 2011 Opiate versus psychostimulant addiction: the differences do matter Nat Rev Neurosci 12 685 700 21971065 PMC3721140
- Beckstead RM 1979 An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat J Comp Neurol 184 43 62 762282
- Belin D Everitt BJ 2008 Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum Neuron 57 432 441 18255035
- Bossert JM Liu SY Lu L Shaham Y 2004 A role of ventral tegmental area glutamate in contextual cue-induced relapse to heroin seeking J Neurosci 24 10726 10730 15564590 PMC6730135
- Bossert JM Gray SM Lu L Shaham Y 2006a Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking Neuropsychopharmacology 31 2197 2209 16341024 PMC1570155
- Bossert JM Poles GC Sheffler-Collins SI Ghitza UE 2006b The mGluR2/3 agonist LY379268 attenuates context- and discrete cue-induced reinstatement of sucrose seeking but not sucrose self-administration in rats Behav Brain Res 173 148 152 16834996
- Bossert JM Poles GC Wihbey KA Koya E Shaham Y 2007 Differential effects of blockade of dopamine D1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues J Neurosci 27 12655 12663 18003845 PMC2117350
- Bossert JM Wihbey KA Pickens CL Nair SG Shaham Y 2009 Role of dopamine D(1)-family receptors in dorsolateral striatum in context-induced reinstatement of heroin seeking in rats Psychopharmacology 206 51 60 19506837 PMC3145155
- Bossert JM Stern AL Theberge FR Cifani C Koya E Hope BT Shaham Y 2011 Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin Nat Neurosci 14 420 422 21336273 PMC3077927
- Bouton ME Bolles RC 1979 Role of conditioned contextual stimuli in reinstatement of extinguished fear J Exp Psychol Anim Behav Process 5 368 378 528893
- Capriles N Rodaros D Sorge RE Stewart J 2003 A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats Psychopharmacology (Berl) 168 66 74 12442201
- Carr DB Sesack SR 1998 Callosal terminals in the rat prefrontal cortex: synaptic targets and association with GABA-immunoreactive structures Synapse 29 193 205 9635889
- Celentano M Caprioli D Dipasquale P Cardillo V Nencini P Gaetani S Badiani A 2009 Drug context differently regulates cocaine versus heroin self-administration and cocaine- versus heroin-induced Fos mRNA expression in the rat Psychopharmacology 204 349 360 19169671
- Crombag H Bossert JM Koya E Shaham Y 2008 Context-induced relapse to drug seeking: a review Trans R Soc Lond B: Biol Sci 363 3233 3243 PMC2607323 18640922
- Crombag HS Shaham Y 2002 Renewal of drug seeking by contextual cues after prolonged extinction in rats Behav Neurosci 116 169 173 11895178
- Crombag HS Jedynak JP Redmond K Robinson TE Hope BT 2002 Locomotor sensitization to cocaine is associated with increased Fos expression in the accumbens, but not in the caudate Behav Brain Res 136 455 462 12429408
- Curran T Morgan JI 1995 Fos: an immediate-early transcription factor in neurons J Neurobiol 26 403 412 7775973
- Diergaarde L de Vries W Raaso H Schoffelmeer AN De Vries TJ 2008 Contextual renewal of nicotine seeking in rats and its suppression by the cannabinoid-1 receptor antagonist Rimonabant (SR141716A) Neuropharmacology 55 712 716 18588903
- Divac I Mogensen J 1990 Long-term retrograde labelling of neurons Brain Res 524 339 341 1705466
- Ferino F Thierry AM Saffroy M Glowinski J 1987 Interhemispheric and subcortical collaterals of medial prefrontal cortical neurons in the rat Brain Res 417 257 266 2443214
- Floresco SB 2007 Dopaminergic regulation of limbic-striatal interplay J Psychiatry Neurosci 32 400 411 18043763 PMC2077353
- Floresco SB Seamans JK Phillips AG 1997 Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay J Neurosci 17 1880 1890 9030646 PMC6573377
- Fuchs RA Ramirez DR Bell GH 2008 Nucleus accumbens shell and core involvement in drug context-induced reinstatement of cocaine seeking in rats Psychopharmacology 200 545 556 18597075 PMC2613506
- Fuchs RA Evans KA Parker MC See RE 2004 Differential involvement of the core and shell subregions of the nucleus accumbens in conditioned cue-induced reinstatement of cocaine seeking in rats Psychopharmacology 176 459 465 15138757
- Fuchs RA Eaddy JL Su ZI Bell GH 2007 Interactions of the basolateral amygdala with the dorsal hippocampus and dorsomedial prefrontal cortex regulate drug context-induced reinstatement of cocaine-seeking in rats Eur J Neurosci 26 487 498 17650119
- Fuchs RA Evans KA Ledford CC Parker MP Case JM Mehta RH See RE 2005 The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats Neuropsychopharmacology 30 296 309 15483559
- Gaffan D Murray EA Fabre-Thorpe M 1993 Interaction of the amygdala with the frontal lobe in reward memory Eur J Neurosci 5 968 975 8281307
- Ghazizadeh A Ambroggi F Odean N Fields HL 2012 Prefrontal cortex mediates extinction of responding by two distinct neural mechanisms in accumbens shell J Neurosci 32 726 737 22238108 PMC6621084
- Goldman-Rakic PS 1999 The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia Biol Psychiatry 46 650 661 10472417
- Grace AA Floresco SB Goto Y Lodge DJ 2007 Regulation of firing of dopaminergic neurons and control of goal-directed behaviors Trends Neursoci 30 220 227 17400299
- Groenewegen HJ Vermeulen-Van der Zee E te Kortschot A Witter MP 1987 Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin Neuroscience 23 103 120 3683859
- Groenewegen HJ Wright CI Beijer AV Voorn P 1999 Convergence and segregation of ventral striatal inputs and outputs Ann N Y Acad Sci 877 49 63 10415642
- Hamlin AS Newby J McNally GP 2007 The neural correlates and role of D1 dopamine receptors in renewal of extinguished alcohol-seeking Neuroscience 146 525 536 17360123
- Ikemoto S Qin M Liu ZH 2005 The functional divide for primary reinforcement of D-amphetamine lies between the medial and lateral ventral striatum: is the division of the accumbens core, shell, and olfactory tubercle valid? J Neurosci 25 5061 5065 15901788 PMC1360206
- Insausti R Herrero MT Witter MP 1997 Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents Hippocampus 7 146 183 9136047
- Jay TM Witter MP 1991 Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin J Comp Neurol 313 574 586 1783682
- Karreman M Moghaddam B 1996 The prefrontal cortex regulates the basal release of dopamine in the limbic striatum: an effect mediated by ventral tegmental area J Neurochem 66 589 598 8592128
- Koya E Uejima JL Wihbey KA Bossert JM Hope BT Shaham Y 2009a Role of ventral medial prefrontal cortex in incubation of cocaine craving Neuropharmacology 56 Suppl 1 177 185 18565549 PMC2635336
- Koya E Golden SA Harvey BK Guez-Barber DH Berkow A Simmons DE Bossert JM Nair SG Uejima JL Marin MT Mitchell TB Farquhar D Ghosh SC Mattson BJ Hope BT 2009b Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization Nat Neurosci 12 1069 1073 19620976 PMC2752202
- LaLumiere RT Kalivas PW 2008 Glutamate release in the nucleus accumbens core is necessary for heroin seeking J Neurosci 28 3170 3177 18354020 PMC6670700
- Lasseter HC Xie X Ramirez DR Fuchs RA 2010 Sub-region specific contribution of the ventral hippocampus to drug context-induced reinstatement of cocaine-seeking behavior in rats Neuroscience 171 830 839 20870011 PMC2987272
- Lu L Grimm JW Dempsey J Shaham Y 2004 Cocaine seeking over extended withdrawal periods in rats: different time courses of responding induced by cocaine cues versus cocaine priming over the first 6 months Psychopharmacology 176 101 108 15071719
- Lupinsky D Moquin L Gratton A 2010 Interhemispheric regulation of the medial prefrontal cortical glutamate stress response in rats J Neurosci 30 7624 7633 20519537 PMC6632388
- Marchant NJ Furlong TM McNally GP 2010 Medial dorsal hypothalamus mediates the inhibition of reward seeking after extinction J Neurosci 30 14102 11415 20962231 PMC6634760
- McFarland K Kalivas PW 2001 The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior J Neurosci 21 8655 8663 11606653 PMC6762812
- McFarland K Davidge SB Lapish CC Kalivas PW 2004 Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior J Neurosci 24 1551 1560 14973230 PMC6730472
- McLaughlin J See RE 2003 Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats Psychopharmacology (Berl) 168 57 65 12845418
- Mello NK Negus SS 1996 Preclinical evaluation of pharmacotherapies for treatment of cocaine and opioid abuse using drug self-administration procedures Neuropsychopharmacology 14 375 424 8726752
- Millan EZ Furlong TM McNally GP 2010 Accumbens shell-hypothalamus interactions mediate extinction of alcohol seeking J Neurosci 30 4626 4635 20357113 PMC6632314
- Millan EZ Marchant NJ McNally GP 2011 Extinction of drug seeking Behav Brain Res 217 454 462 21073904
- Miller CA Marshall JF 2005 Altered Fos expression in neural pathways underlying cue-elicited drug seeking in the rat Eur J Neurosci 21 1385 1393 15813948
- Morales M Wang SD 2002 Differential composition of 5-hydroxytryptamine3 receptors synthesized in the rat CNS and peripheral nervous system J Neurosci 22 6732 6741 12151552 PMC6758137
- Morales M Criado JR Sanna PP Henriksen SJ Bloom FE 1998 Acute ethanol induces c-fos immunoreactivity in GABAergic neurons of the central nucleus of the amygdala Brain Res 798 333 336 9666163
- Nair SG Navarre BM Cifani C Pickens CL Bossert JM Shaham Y 2011 Role of dorsal medial prefrontal cortex dopamine D1-family receptors in relapse to high-fat food seeking induced by the anxiogenic drug yohimbine Neuropsychopharmacology 36 497 510 20962767 PMC3005956
- O’Brien CP Childress AR Mclellan TA Ehrman R 1992 Classical conditioning in drug dependent humans Ann N Y Acad Sci 654 400 415 1632593
- O’Donnell P 2003 Dopamine gating of forebrain neural ensembles Eur J Neurosci 17 429 435 12581161
- Paxinos G Watson C 2005 The rat brain in stereotaxic coordinates 5 Amsterdam Elsevier Academic Press
- Peters J LaLumiere RT Kalivas PW 2008 Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats J Neurosci 28 6046 6053 18524910 PMC2585361
- Peters J Kalivas PW Quirk GJ 2009 Extinction circuits for fear and addiction overlap in prefrontal cortex Learn Mem 16 279 288 19380710 PMC4527308
- Peters J Vallone J Laurendi K Kalivas PW 2007 Opposing roles for the ventral prefrontal cortex and the basolateral amygdala on the spontaneous recovery of cocaine-seeking in rats Psychopharmacology 18066533
- Rogers JL Ghee S See RE 2008 The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse Neuroscience 151 579 588 18061358 PMC2238688
- Schmidt ED Voorn P Binnekade R Schoffelmeer AN De Vries TJ 2005 Differential involvement of the prelimbic cortex and striatum in conditioned heroin and sucrose seeking following long-term extinction Eur J Neurosci 22 2347 2356 16262673
- Schmued LC Fallon JH 1986 Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties Brain Res 377 147 154 2425899
- Sesack SR Deutch AY Roth RH Bunney BS 1989 Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin J Comp Neurol 290 213 242 2592611
- Setlow B Holland PC Gallagher M 2002 Disconnection of the basolateral amygdala complex and nucleus accumbens impairs appetitive pavlovian second-order conditioned responses Behav Neurosci 116 267 275 11996312
- Shalev U Grimm JW Shaham Y 2002 Neurobiology of relapse to heroin and cocaine seeking: a review Pharmacol Rev 54 1 42 11870259
- Shalev U Robarts P Shaham Y Morales M 2003 Selective induction of c-Fos immunoreactivity in the prelimbic cortex during reinstatement of heroin seeking induced by acute food deprivation in rats Behav Brain Res 145 79 88 14529807
- Thierry AM Gioanni Y Degenetais E Glowinski J 2000 Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics Hippocampus 10 411 419 10985280
- Vertes RP 2004 Differential projections of the infralimbic and prelimbic cortex in the rat Synapse 51 32 58 14579424
- Weiss F Maldonado-Vlaar CS Parsons LH Kerr TM Smit DL Ben-Shahar O 2000 Control of cocaine-seeking behavior by drug-associated stimuli in rats: effects on recovery of extinguished operant-responding and extracellular dopamine levels in amygdala and nucleus accumbens Proc Natl Acad Sci (USA) 97 4321 4326 10760299 PMC18240
- Wikler A 1973 Dynamics of drug dependence. Implications of a conditioning theory for research and treatment Arch Gen Psychiatry 28 611 616 4700675
- Wilson CJ 1986 Postsynaptic potentials evoked in spiny neostriatal projection neurons by stimulation of ipsilateral and contralateral neocortex Brain Res 367 201 213 3008920
- You ZB Tzschentke TM Brodin E Wise RA 1998 Electrical stimulation of the prefrontal cortex increases cholecystokinin, glutamate, and dopamine release in the nucleus accumbens: an in vivo microdialysis study in freely moving rats J Neurosci 18 6492 5000 9698337 PMC6793204
- Zironi I Burattini C Aicardi G Janak PH 2006 Context is a trigger for relapse to alcohol Behav Brain Res 167 150 155 16256214
Cited by
Sorted by citations
Hiser, J., & Koenigs, M. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.030 · Cited by 972 · see citing works
Scofield, M. D., Heinsbroek, J. A., Gipson, C. D., Kupchik, Y. M., Spencer, S., Smith, A. C. W., Roberts-Wolfe, D., & Kalivas, P. W. (2016) · Pharmacological Reviews · doi:10.1124/pr.116.012484 · Cited by 598 · see citing works
The nucleus accumbens: a comprehensive review
Salgado, S., & Kaplitt, M. G. (2015) · Stereotactic and Functional Neurosurgery · doi:10.1159/000368279 · Cited by 489 · see citing works
Bossert, J. M., Marchant, N. J., Calu, D. J., & Shaham, Y. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3120-y · Cited by 453 · see citing works
Self-citationPrefrontal cortex output circuits guide reward seeking through divergent cue encoding
Otis, J. M., Namboodiri, V. M. K., Matan, A. M., Voets, E. S., Mohorn, E. P., Kosyk, O., McHenry, J. A., Robinson, J. E., Resendez, S. L., Rossi, M. A., et al. (2017) · Nature · doi:10.1038/nature21376 · Cited by 412 · see citing works
Ma, Y.-Y., Lee, B. R., Wang, X., Guo, C., Liu, L., Cui, R., Lan, Y., Balcita-Pedicino, J. J., Wolf, M. E., Sesack, S. R., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.023 · Cited by 344 · see citing works
Self-citationPrefrontal cortical control of a brainstem social behavior circuit
Franklin, T. B., Silva, B. A., Perova, Z., Marrone, L., Masferrer, M. E., Zhan, Y., Kaplan, A., Greetham, L., Verrechia, V., Halman, A., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4470 · Cited by 231 · see citing works
Optogenetic dissection of medial prefrontal cortex circuitry
Riga, D., Matos, M. R., Glas, A., Smit, A. B., Spijker, S., & Van den Oever, M. C. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00230 · Cited by 208 · see citing works
Going and stopping: dichotomies in behavioral control by the prefrontal cortex
Gourley, S. L., & Taylor, J. R. (2016) · Nature Neuroscience · doi:10.1038/nn.4275 · Cited by 195 · see citing works
Furlong, T. M., Jayaweera, H. K., Balleine, B. W., & Corbit, L. H. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3707-13.2014 · Cited by 186 · see citing works
Venniro, M., Caprioli, D., Zhang, M., Whitaker, L. R., Zhang, S., Warren, B. L., Cifani, C., Marchant, N. J., Yizhar, O., Bossert, J. M., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.024 · Cited by 162 · see citing works
Self-citationKim, C. K., Ye, L., Jennings, J. H., Pichamoorthy, N., Tang, D. D., Yoo, A.-C. W., Ramakrishnan, C., & Deisseroth, K. (2017) · Cell · doi:10.1016/j.cell.2017.07.020 · Cited by 145 · see citing works
Zhang, Y., Kahng, M. W., Elkind, J. A., Weir, V. R., Hernandez, N. S., Stein, L. M., & Schmidt, H. D. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-019-0531-4 · Cited by 92 · see citing works
Wendler, E., Gaspar, J. C. C., Ferreira, T. L., Barbiero, J. K., Andreatini, R., Vital, M. A. B. F., Blaha, C. D., Winn, P., & Da Cunha, C. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.11.009 · Cited by 65 · see citing works
Haddon, J. E., Titherage, D., Heckenast, J. R., Carter, J., Owen, M. J., Hall, J., Wilkinson, L. S., & Jones, M. W. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02969-x · Cited by 6 · see citing works
“Previous animal studies have revealed that performance on conditional discrimination tasks is dependent upon the intact functioning of the nucleus accumbens [64, 65].”
Background
- Authors
- Bossert, J. M., Stern, A. L., Theberge, F. R. M., Marchant, N. J., Wang, H.-L., Morales, M., & Shaham, Y.
- Affiliations
- National Institutes of Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-04-04
- Volume
- 32
- Issue
- 14
- Pages
- 4982-4991
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3335169
- OpenAlex
- W2147272801
- Cited by
- 223
- References
- 7
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 4 · 2023: 11 · 2022: 15 · 2021: 12 · 2020: 20 · 2019: 20 · 2018: 18 · 2017: 22 · 2016: 15 · 2015: 21 · 2014: 24 · 2013: 20 · 2012: 11
- FWCI
- 10.02
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- U.S. Department of Health and Human Services
- National Institutes of Health
- National Institute on Drug Abuse (ZIADA000434)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- heroin seeking, heroin relapse, ventromedial prefrontal cortex, nucleus accumbens shell, glutamatergic projections, dopamine D1 receptor, self-administration, extinction, Fos expression, muscimol, baclofen, SCH 23390, opioid use disorder
- MeSH terms
- Animals, Extinction, Psychological, Heroin Dependence, Male, Nerve Net, Neural Pathways, Nucleus Accumbens, Self Administration, Behavior, Addictive, Prefrontal Cortex, Rats, Long-Evans, Rats
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
