The nucleus accumbens shell in reinstatement and extinction of drug seeking.
addiction
circuit
corticostriatal
relapse
striatum
Journal
The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110
Informations de publication
Date de publication:
08 2019
08 2019
Historique:
received:
13
04
2018
revised:
05
07
2018
accepted:
17
07
2018
pubmed:
26
7
2018
medline:
1
7
2020
entrez:
26
7
2018
Statut:
ppublish
Résumé
The contexts where drugs are self-administered have important control over relapse and extinction of drug-seeking behavior. The nucleus accumbens shell (AcbSh) is essential to this contextual control over drug-seeking behavior. It has been consistently implicated in both the expression of context-induced reinstatement and the expression of extinction, across a variety of drug classes and other rewards. Here, we review the evidence linking AcbSh to the extinction and reinstatement of drug seeking. We consider whether this dual role can be linked to known heterogeneities in AcbSh cell types, their major afferents, and their major efferents. We show that although these heterogeneities are each important and can determine extinction vs. reinstatement, they do not seem adequate to explain the body of findings from the behavioral literature. Rather, we suggest that this functional specialization of AcbSh may be more profitably viewed in terms of the segregation and compartmentalization of AcbSh channels.
Substances chimiques
Ethanol
3K9958V90M
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2014-2022Subventions
Organisme : National Health and Medical Research Council
ID : GNT1098436
Pays : International
Organisme : National Health and Medical Research Council
ID : GNT1138062
Pays : International
Informations de copyright
© 2018 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
Références
Al-Hasani, R., McCall, J.G., Shin, G., Gomez, A.M., Schmitz, G.P., Bernardi, J.M., Pyo, C.O., Park, S.I. et al. (2015) Distinct subpopulations of nucleus accumbens dynorphin neurons drive aversion and reward. Neuron, 87, 1063-1077.
Badiani, A., Belin, D., Epstein, D.H., Calu, D.J. & Shaham, Y. (2011) Opiate versus psychostimulant addiction: the differences do matter. Nat. Rev. Neurosci., 12, 685-700.
Basso, A.M. & Kelley, A.E. (1999) Feeding induced by GABAA receptor stimulation within the nucleus accumbens shell: regional mapping and characterization of macronutrient and taste preference. Behav. Neurosci., 113, 324-336.
Beier, K.T., Steinberg, E.E., DeLoach, K.E., Xie, S., Miyamichi, K., Schwarz, L., Gao, X.J., Kremer, E.J. et al. (2015) Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping. Cell, 162, 622-634.
Berendse, H.W., Galis-de Graaf, Y. & Groenewegen, H.J. (1992) Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. Comp. Neurol., 316, 314-347.
Bertran-Gonzalez, J., Herve, D., Girault, J.-A. & Valjent, E.J. (2010) What is the degree of segregation between striatonigral and striatopallidal projections? Front. Neuroanat., 4, 1-9.
Bocklisch, C., Pascoli, V., Wong, J.C.Y., House, D.R.C., Yvon, C., de Roo, M., Tan, K.R., Lüscher, C. (2013) Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science, 341, 1521-1525.
Bolam, J.P., Hanley, J.J., Booth, P.A. & Bevan, M.D. (2000) Synaptic organisation of the basal ganglia. J. Anat., 196, 527-542.
Bossert, J.M., Liu, S.Y., 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.
Bossert, J.M., Gray, S.M., Lu, L. & Shaham, Y. (2006) Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking. Neuropsychopharmacology, 31, 2197-2209.
Bossert, J.M., Poles, G.C., Wihbey, K.A., 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.
Bossert, J.M., Stern, A.L., Theberge, F.R.M., Cifani, C., Koya, E., Hope, B.T. & Shaham, Y. (2011) Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nat. Neurosci., 14, 420-422.
Bossert, J.M., Stern, A.L., Theberge, F.R.M., Marchant, N.J., Wang, H.L., Morales, M. & Shaham, Y. (2012) Role of projections from ventral medial prefrontal cortex to nucleus accumbens shell in context-induced reinstatement of heroin seeking. J. Neurosci., 32, 4982-4991.
Bossert, J.M., Adhikary, S., St Laurent, R., Marchant, N.J., Wang, H.-L., Morales, M. & Shaham, Y. (2016) Role of projections from ventral subiculum to nucleus accumbens shell in context-induced reinstatement of heroin seeking in rats. Psychopharmacology, 233, 1991-2004.
Bouton, M.E. & Todd, T.P. (2014) A fundamental role for context in instrumental learning and extinction. Behav. Process., 104, 13-19.
Bouyer, J.J., Park, D.H., Joh, T.H. & Pickel, V.M. (1984) Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res., 302, 267-275.
Britt, J.P., Benaliouad, F., Mcdevitt, R.A., Stuber, G.D., Wise, R.A. & Bonci, A. (2012) Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron, 76, 790-803.
Brog, J.S., Salyapongse, A., Deutch, A.Y. & Zahm, D.S. (1993) The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J. Comp. Neurol., 338, 255-278.
Brown, M.T.C., Tan, K.R., O'Connor, E.C., Nikonenko, I., Muller, D. & Luscher, C. (2012) Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature, 492, 452-456.
Canteras, N.S., Simerly, R.B. & Swanson, L.W. (1992) Connections of the posterior nucleus of the amygdala. J. Comp. Neurol., 324, 143-179.
Castro, D.C. & Berridge, K.C. (2014) Opioid hedonic hotspot in nucleus accumbens shell: mu, delta, and kappa maps for enhancement of sweetness “liking” and “wanting”. J. Neurosci., 34, 4239-4250.
Castro, D.C., Terry, R.A. & Berridge, K.C. (2016) Orexin in rostral hotspot of nucleus accumbens enhances sucrose liking and intake but scopolamine in caudal shell shifts liking toward disgust and fear. Neuropsychopharmacology, 41, 2101-2111.
Chaudhri, N., Sahuque, L.L., Cone, J.J. & Janak, P.H. (2008) Reinstated ethanol-seeking in rats is modulated by environmental context and requires the nucleus accumbens core. Eur. J. Neurosci., 28, 2288-2298.
Chaudhri, N., Sahuque, L.L. & Janak, P.H. (2009) Ethanol seeking triggered by environmental context is attenuated by blocking dopamine D1 receptors in the nucleus accumbens core and shell in rats. Psychopharmacology, 207, 303-314.
Cho, Y.T., Ernst, M. & Fudge, J.L. (2013) Cortico-amygdala-striatal circuits are organized as hierarchical subsystems through the primate amygdala. J. Neurosci., 33, 14017-14030.
Christie, M.J., Summers, R.J., Stephenson, J.A., Cook, C.J. & Beart, P.M. (1987) Excitatory amino acid projections to the nucleus accumbens septi in the rat: a retrograde transport study utilizing D[3H]aspartate and [3H]GABA. Neuroscience, 22, 425-439.
Ciccocioppo, R., Sanna, P.P. & Weiss, F. (2001) Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D(1) antagonists. Proc. Nat. Acad. Sci. USA, 98, 1976-1981.
Creed, M., Pascoli, V.J. & Luscher, C. (2015) Refining deep brain stimulation to emulate optogenetic treatment of synaptic pathology. Science, 347, 659-664.
Crombag, H.S. & Shaham, Y. (2002) Renewal of drug seeking by contextual cues after prolonged extinction in rats. Behav. Neurosci., 116, 169-173.
Crombag, H.S., Grimm, J.W. & Shaham, Y. (2002) Effect of dopamine receptor antagonists on renewal of cocaine seeking by reexposure to drug-associated contextual cues. Neuropsychopharmacology, 27, 1006-1015.
Cruz, F.C., Babin, K.R., Leao, R.M., Goldart, E.M., Bossert, J.M., Shaham, Y. & Hope, B.T. (2014) Role of nucleus accumbens shell neuronal ensembles in context-induced reinstatement of cocaine-seeking. J. Neurosci., 34, 7437-7446.
Dayas, C.V., Liu, X., Simms, J.A. & Weiss, F. (2007) Distinct patterns of neural activation associated with ethanol seeking: effects of naltrexone. Biol. Psychiatry, 61, 979-989.
Diergaarde, L., de Vries, W., Raasø, H., Schoffelmeer, A.N.M. & De Vries, T.J. (2008) Contextual renewal of nicotine seeking in rats and its suppression by the cannabinoid-1 receptor antagonist Rimonabant (SR141716A). Neuropharmacology, 55, 712-716.
Edwards, N.J., Tejeda, H.A., Pignatelli, M., Zhang, S., Mcdevitt, R.A., Wu, J., Bass, C.E., Bettler, B. et al. (2017) Circuit specificity in the inhibitory architecture of the VTA regulates cocaine-induced behavior. Nat. Neurosci., 20, 438-448.
Faget, L., Osakada, F., Duan, J., Ressler, R., Johnson, A.B., Proudfoot, J.A., Yoo, J.H., Callaway, E.M. et al. (2016) Afferent inputs to neurotransmitter-defined cell types in the ventral tegmental area. Cell Rep., 15, 2796-2808.
Faure, A., Reynolds, S.M., Richard, J.M. & Berridge, K.C. (2008) Mesolimbic dopamine in desire and dread: enabling motivation to be generated by localized glutamate disruptions in nucleus accumbens. J. Neurosci., 28, 7184-7192.
Floresco, S.B., Todd, C.L. & Grace, A.A. (2001) Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J. Neurosci., 21, 4915-4922.
Floresco, S.B., McLaughlin, R.J. & Haluk, D.M. (2008) Opposing roles for the nucleus accumbens core and shell in cue-induced reinstatement of food-seeking behavior. Neuroscience, 154, 877-884.
Fuchs, R.A., Evans, K.A., Parker, M.C. & See, R.E. (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.
Fuchs, R.A., Ramirez, D.R. & Bell, G.H. (2008) Nucleus accumbens shell and core involvement in drug context-induced reinstatement of cocaine seeking in rats. Psychopharmacology, 200, 545-556.
Gibson, G.D., Prasad, A.A., Jean-Richard Dit Bressel, P., Yau, J.O.-Y., Millan, E.Z., Campbell, E.J., Lim, J., Marchant, N.J. et al. (2018). Distinct accumbens shell output pathways promote versus prevent relapse to alcohol seeking. Neuron, 98, 512-520.
Groenewegen, H.J. & Berendse, H.W. (1994) The specificity of the “nonspecific” midline and intralaminar thalamic nuclei. Trends Neurosci., 17, 52-57.
Groenewegen, H.J., Berendse, H.W. & Haber, S.N. (1993) Organisation of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience, 57, 113-142.
Groenewegen, H.J., Wright, C.I. & Beijer, A.V. (1996) The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog. Brain Res., 107, 485-511.
Groenewegen, H.J., Wright, C.I., Beijer, A.V.J. & Voorn, P. (1999) Convergence and segregation of ventral striatal inputs and outputs. Ann. N. Y. Acad. Sci., 877, 49-63.
Guercio, L.A., Schmidt, H.D. & Pierce, R.C. (2015) Deep brain stimulation of the nucleus accumbens shell attenuates cue-induced reinstatement of both cocaine and sucrose seeking in rats. Behav. Brain Res., 281, 125-130.
Hamlin, A.S., Blatchford, K.E. & McNally, G.P. (2006) Renewal of an extinguished instrumental response: neural correlates and the role of D1 dopamine receptors. Neuroscience, 143, 25-38.
Hamlin, A.S., Newby, J. & McNally, G.P. (2007) The neural correlates and role of D1 dopamine receptors in renewal of extinguished alcohol-seeking. Neuroscience, 146, 525-536.
Hamlin, A.S., Clemens, K.J. & McNally, G.P. (2008) Renewal of extinguished cocaine-seeking. Neuroscience, 151, 659-670.
Hamlin, A.S., Clemens, K.J., Choi, E.A. & McNally, G.P. (2009) Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking. Eur. J. Neurosci., 29, 802-812.
Harris, G.C., Wimmer, M. & Aston-Jones, G. (2005) A role for lateral hypothalamic orexin neurons in reward seeking. Nature, 437, 556-559.
Heimer, L., Zahm, D.S., Churchill, L. & Kalivas, P.W. (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience, 41, 89-125.
Heimer, L., Alheid, G.F., de Olmos, J.S., Groenewegen, H.J., Haber, S.N., Harlan, R.E. & Zahm, D.S. (1997) The accumbens: beyond the core-shell dichotomy. J. Neuropsychiatry Clin. Neurosci., 9, 354-381.
Humphries, M.D. & Prescott, T.J. (2010) The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. Prog. Neurobiol., 90, 385-417.
Ikemoto, S. (2002) Ventral striatal anatomy of locomotor activity induced by cocaine, D-amphetamine, dopamine and D1/D2 agonists. Neuroscience, 113, 939-955.
Ikemoto, S. (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev., 56, 27-78.
Ikemoto, S., Qin, M. & Liu, Z.-H. (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.
Jupp, B., Krivdic, B., Krstew, E. & Lawrence, A.J. (2011) The orexin1 receptor antagonist SB-334867 dissociates the motivational properties of alcohol and sucrose in rats. Brain Res., 1391, 54-59.
Kallupi, M., de Guglielmo, G., Cannella, N., Li, H.W., Caló, G., Guerrini, R., Ubaldi, M., Renger, J.J. et al. (2012) Hypothalamic neuropeptide S receptor blockade decreases discriminative cue-induced reinstatement of cocaine seeking in the rat. Psychopharmacology, 226, 347-355.
Kelley, A.E. & Swanson, C.J. (1997) Feeding induced by blockade of AMPA and kainate receptors within the ventral striatum: a microinfusion mapping study. Behav. Brain Res., 89, 107-113.
Khoo, S.Y.S., Gibson, G.D., Prasad, A.A. & McNally, G.P. (2017) How contexts promote and prevent relapse to drug seeking. Genes Brain Behav., 16, 185-204.
Kravitz, A.V., Freeze, B.S., Parker, P.R.L., Kay, K., Thwin, M.T., Deisseroth, K. & Kreitzer, A.C. (2010) Regulation of parkinsonian motor behaviors by optogenetic control of basal ganglia circuitry. Nature, 466, 622-626.
Kufahl, P.R., Zavala, A.R., Singh, A., Thiel, K.J., Dickey, E.D., Joyce, J.N. & Neisewander, J.L. (2009) c-Fos expression associated with reinstatement of cocaine-seeking behavior by response-contingent conditioned cues. Synapse, 63, 823-835.
Kupchik, Y.M., Brown, R.M., Heinsbroek, J.A., Lobo, M.K., Schwatrz, D.J. & Kalivas, P.W. (2015) Coding the direct/indirect pathways by D1 and D2 receptors is not valid for accumbens projections. Nat. Neurosci., 18, 1230-1232.
Lacroix, F., Pettorelli, A., Maddux, J.-M.N., Heidari-Jam, A. & Chaudhri, N. (2017) Varenicline reduces context-induced relapse to alcohol-seeking through actions in the nucleus accumbens. Neuropsychopharmacology, 42, 1037-1048.
LaLumiere, R.T., Smith, K.C. & Kalivas, P.W. (2012) Neural circuit competition in cocaine-seeking: roles of the infralimbic cortex and nucleus accumbens shell. Eur. J. Neurosci., 35, 614-622.
Lammel, S., Lim, B.K., Ran, C., Huang, K.W., Betley, M.J., Tye, K.M., Deisseroth, K., Malenka, R.C. (2013) Input-specific control of reward and aversion in the ventral tegmental area. Nature, 491, 212-217.
Li, S.S.Y. & McNally, G.P. (2015a) A role of nucleus accumbens dopamine receptors in the nucleus accumbens core, but not shell, in fear prediction error. Behav. Neurosci., 129, 450-456.
Li, S.S.Y. & McNally, G.P. (2015b) Selecting danger signals: dissociable roles of nucleus accumbens shell and core glutamate in predictive fear learning. Eur. J. Neurosci., 41, 1515-1523.
Lindvall, O. & Björklund, A. (1974) The organization of the ascending catecholamine neuron systems in the rat brain as revealed by the glyoxylic acid fluorescence method. Acta Physiol. Scand. Suppl., 412, 1-48.
Luo, A.H., Tahsili-Fahadan, P., Wise, R.A., Lupica, C.R. & Aston-Jones, G. (2011) Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science, 333, 353-357.
Mahler, S.V. & Aston-Jones, G.S. (2012) Fos activation of selective afferents to ventral tegmental area during cue-induced reinstatement of cocaine seeking in rats. J. Neurosci., 32, 13309-13325.
Mahler, S.V., Vazey, E.M., Beckley, J.T., Keistler, C.R., McGlinchey, E.M., Kaufling, J., Wilson, S.P., Deisseroth, K. et al. (2014) Designer receptors show role for ventral pallidum input to ventral tegmental area in cocaine seeking. Nat. Neurosci., 17, 577-585.
Marchant, N.J., Hamlin, A.S. & McNally, G.P. (2009) Lateral hypothalamus is required for context-induced reinstatement of extinguished reward seeking. J. Neurosci., 29, 1331-1342.
Marchant, N.J., Rabei, R., Kaganovsky, K., Caprioli, D., Bossert, J.M., Bonci, A. & Shaham, Y. (2014) A critical role of lateral hypothalamus in context-induced relapse to alcohol seeking after punishment-imposed abstinence. J. Neurosci., 34, 7447-7457.
Marchant, N.J., Kaganovsky, K., Shaham, Y. & Bossert, J.M. (2015) Role of corticostriatal circuits in context-induced reinstatement of drug-seeking. Brain Res., 1628, 219-232.
Marchant, N.J., Campbell, E.J., Whitaker, L.R., Harvey, B.K., Kaganovsky, K., Adhikary, S., Hope, B.T., Heins, R.C. et al. (2016) Role of ventral subiculum in context-induced relapse to alcohol seeking after punishment-imposed abstinence. J. Neurosci., 36, 3281-3294.
Martínez-Rivera, F.J., Rodríguez-Romaguera, J., Lloret-Torres, M.E., Do-monte, F.H., Quirk, G.J. & Barreto-Estrada, J.L. (2016) Bidirectional modulation of extinction of drug seeking by deep brain stimulation of the ventral striatum DBS of ventral striatum and extinction of drug seeking. Biol. Psychiatry, 80, 682-690.
Matamales, M., Bertran-Gonzalez, J., Salomon, L., Degos, B., Deniau, J.-M., Valjent, E., Hervé, D., Girault, J.A. (2009) Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS One, 4, e4770.
McFarland, K. & Kalivas, P.W. (2001) The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J. Neurosci., 21, 8655-8663.
McFarland, K., Davidge, S.B., Lapish, C.C. & Kalivas, P.W. (2004) Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J. Neurosci., 24, 1551-1560.
Meredith, G.E., Pennartz, C.M.A. & Groenewegen, H.J. (1993) The cellular framework for chemical signalling in the nucleus accumbens. Prog. Neurobiol., 99, 3-24.
Meredith, G.E., Baldo, B.A., Andrezjewski, M.E. & Kelley, A.E. (2008) The structural basis for mapping behavior onto the ventral striatum and its subdivisions. Brain Struct. Funct., 213, 17-27.
Millan, E.Z. & McNally, G.P. (2011) Accumbens shell AMPA receptors mediate expression of extinguished reward seeking through interactions with basolateral amygdala. Learn. Mem., 18, 414-421.
Millan, E.Z. & McNally, G.P. (2012) Cocaine- and amphetamine-regulated transcript in the nucleus accumbens shell attenuates context-induced reinstatement of alcohol seeking. Behav. Neurosci., 126, 690-698.
Millan, E.Z., Furlong, T.M. & McNally, G.P. (2010) Accumbens shell-hypothalamus interactions mediate extinction of alcohol seeking. J. Neurosci., 30, 4626-4635.
Millan, E.Z., Reese, R.M., Grossman, C.D., Chaudhri, N. & Janak, P.H. (2015) Nucleus accumbens and posterior amygdala mediate cue-triggered alcohol seeking and suppress behavior during the omission of alcohol-predictive cues. Neuropsychopharmacology, 15, 2555-2565.
Mogenson, G.J., Jones, D.L. & Yim, C.Y. (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol., 14, 69-97.
Müller, U.J., Sturm, V., Voges, J., Heinze, H.-J., Galazky, I., Heldmann, M., Scheich, H., Bogerts, B. (2009) Successful treatment of chronic resistant alcoholism by deep brain stimulation of nucleus accumbens: first experience with three cases. Pharmacopsychiatry, 42, 288-291.
Nieh, E.H., Matthews, G.A., Allsop, S.A., Presbrey, K.N., Leppla, C.A., Wichmann, R., Neve, R., Wildes, C.P. et al. (2015) Decoding neural circuits that control compulsive sucrose seeking. Cell, 160, 528-541.
O'Connor, E.C., Kremer, Y., Lefort, S., Harada, M., Pascoli, V., Rohner, C. & Luscher, C. (2015) Accumbal D1R neurons projecting to lateral hypothalamus authorize feeding. Neuron, 88, 553-564.
O'Donnell, P. & Grace, A.A. (1994) Tonic D2-mediated attenuation of cortical excitation in nucleus accumbens neurons recorded in vitro. Brain Res., 634, 105-112.
Parsons, M.P., Li, S. & Kirouac, G.J. (2007) Functional and anatomical connection between the paraventricular nucleus of the thalamus and dopamine fibers of the nucleus accumbens. J. Comp. Neurol., 500, 1050-1063.
Peciña, S. & Berridge, K.C. (2005) Hedonic hot spot in nucleus accumbens shell: where do mu-opioids cause increased hedonic impact of sweetness? J. Neurosci., 25, 11777-11786.
Perry, C.J. & McNally, G.P. (2013a) μ-Opioid receptors in the nucleus accumbens shell mediate context-induced reinstatement (renewal) but not primed reinstatement of extinguished alcohol seeking. Behav. Neurosci., 127, 535-543.
Perry, C.J. & McNally, G.P. (2013b) A role for the ventral pallidum in context-induced and primed reinstatement of alcohol seeking. Eur. J. Neurosci., 38, 2762-2773.
Peters, J., LaLumiere, R.T. & Kalivas, P.W. (2008) Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. J. Neurosci., 28, 6046-6053.
Plaza-Zabala, A., Flores, A.F., Martín-García, E., Saravia, R., Maldonado, R. & Berrendero, F. (2013) A role for hypocretin/orexin receptor-1 in cue-induced reinstatement of nicotine-seeking behavior. Neuropsychopharmacology, 38, 1724-1736.
Prasad, A.A. & McNally, G.P. (2016) Ventral pallidum output pathways in context-induced reinstatement of alcohol seeking. J. Neurosci., 36, 11716-11726.
Reynolds, S.M. & Berridge, K.C. (2002) Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste “liking”/‘disliking’ reactions, place preference/avoidance, and fear. J. Neurosci., 22, 7308-7320.
Reynolds, S.M. & Berridge, K.C. (2003) Glutamate motivational ensembles in nucleus accumbens: rostrocaudal shell gradients of fear and feeding. Eur. J. Neurosci., 17, 2187-2200.
Rocha, A. & Kalivas, P.W. (2010) Role of the prefrontal cortex and nucleus accumbens in reinstating methamphetamine seeking. Eur. J. Neurosci., 31, 903-909.
Rogers, J.L., Ghee, S. & See, R.E. (2008) The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse. Neuroscience, 151, 579-588.
Rubio, F.J., Liu, Q.R., Li, X., Cruz, F.C., Leao, R.M., Warren, B.L., Kambhampati, S., Babin, K.R. et al. (2015) Context-induced reinstatement of methamphetamine seeking is associated with unique molecular alterations in fos-expressing dorsolateral striatum neurons. J. Neurosci., 35, 5625-5639.
Sano, H. & Yokoi, M. (2007) Striatal medium spiny neurons terminate in a distinct region in the lateral hypothalamic area and do not directly innervate orexin/hypocretin- or melanin-concentrating hormone-containing neurons. J. Neurosci., 27, 6948-6955.
Sartor, G.C. & Aston-Jones, G.S. (2012) A septal-hypothalamic pathway drives orexin neurons, which is necessary for conditioned cocaine preference. J. Neurosci., 32, 4623-4631.
Schmeichel, B.E. & Berridge, C.W. (2013) Amphetamine acts within the lateral hypothalamic area to elicit affectively neutral arousal and reinstate drug-seeking. Intl. J. Neuropsychopharm., 17, 63-75.
Self, D.W., Choi, K.-H., Simmons, D., Walker, J.R. & Smagula, C.S. (2004) Extinction training regulates neuroadaptive responses to withdrawal from chronic cocaine self-administration. Learn. Mem., 11, 648-657.
Shin, R., Qin, M., Liu, Z.-H. & Ikemoto, S. (2008) Intracranial self-administration of MDMA into the ventral striatum of the rat: differential roles of the nucleus accumbens shell, core, and olfactory tubercle. Psychopharmacology, 198, 261-270.
Smith, R.J., Lobo, M.K., Spencer, S. & Kalivas, P.W. (2013) Cocaine-induced adaptations in D1 and D2 accumbens projection neurons (a dichotomy not necessarily synonymous with direct and indirect pathways). Curr. Opin. Neurobiol., 23, 546-552.
Sutton, M.A., Schmidt, E.F., Choi, K.-H., Schad, C.A., Whisler, K., Simmons, D., Karanian, D.A., Monteggia, L.M. et al. (2003) Extinction-induced upregulation in AMPA receptors reduces cocaine- seeking behavior. Nature, 421, 70-74.
Tang, X.C., McFarland, K., Cagle, S. & Kalivas, P.W. (2005) Cocaine-induced reinstatement requires endogenous stimulation of mu-opioid receptors in the ventral pallidum. J. Neurosci., 25, 4512-4520.
Thompson, R.H. & Swanson, L.W. (2010) Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc. Nat. Acad. Sci. USA, 107, 15235-15239.
Todd, T.P. (2013) Mechanisms of renewal after the extinction of instrumental behavior. J. Exp. Psychol. Anim. Behav. Process., 39, 193-207.
Todd, T.P., Vurbic, D. & Bouton, M.E. (2014) Behavioral and neurobiological mechanisms of extinction in Pavlovian and instrumental learning. Neurobiol. Learn. Mem., 108, 52-64.
Vassoler, F.M., Schmidt, H.D., Gerard, M.E., Famous, K.R., Ciraulo, D.A., Kornetsky, C., Knapp, C.M., Pierce, R.C. (2008) Deep brain stimulation of the nucleus accumbens shell attenuates cocaine priming-induced reinstatement of drug seeking in rats. J. Neurosci., 28, 8735-8739.
Voorn, P., Vanderschuren, L.J.M.J., Groenewegen, H.J., Robbins, T.W. & Pennartz, C.M.A. (2004) Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci., 27, 468-474.
Watabe-Uchida, M., Zhu, L., Ogawa, S.K., Vamanrao, A. & Uchida, N. (2012) Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron, 74, 858-873.
Xia, Y., Driscoll, J.R., Wilbrecht, L., Margolis, E.B., Fields, H.L. & Hjelmstad, G.O. (2011) Nucleus accumbens medium spiny neurons target non-dopaminergic neurons in the ventral tegmental area. J. Neurosci., 31, 7811-7816.
Xie, X., Lasseter, H.C., Ramirez, D.R., Ponds, K.L., Wells, A.M. & Fuchs, R.A. (2011) Subregion-specific role of glutamate receptors in the nucleus accumbens on drug context-induced reinstatement of cocaine-seeking behavior in rats. Addict. Biol., 17, 287-299.
Yang, H., de Jong, J.W., Tak, Y., Peck, J., Bateup, H.S. & Lammel, S. (2018) Nucleus accumbens subnuclei regulate motivated behavior via direct inhibition and disinhibition of VTA dopamine subpopulations. Neuron, 97, 434-449.
Zahm, D.S. & Heimer, L. (1990) Two transpallidal pathways originating in the rat nucleus accumbens. J. Comp. Neurol., 302, 437-446.
Zhao, Y., Dayas, C.V., Aujla, H., Baptista, M.A.S., Martin-Fardon, R. & Weiss, F. (2006) Activation of group II metabotropic glutamate receptors attenuates both stress and cue-induced ethanol-seeking and modulates c-fos expression in the hippocampus and amygdala. J. Neurosci., 26, 9967-9974.
Zhou, H., Xu, J. & Jiang, J. (2011) Deep brain stimulation of nucleus accumbens on heroin-seeking behaviors: a case report. Biol. Psychiatry, 69, e41-e42.