Synaptic plasticity and addiction (original) (raw)

• Ramón y Cajal, S. La fine structure des centres nerveux. Proc. R. Soc. Lond. 55, 444–468 (1894).
  Article Google Scholar
• Bliss, T. V. P. & Lomo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331–356 (1973). The initial, now classic, description of LTP in the hippocampus.
  Article CAS PubMed PubMed Central Google Scholar
• Malenka, R. C. & Bear, M. F. LTP and LTD: an embarrassment of riches. Neuron 44, 5–21 (2004).
  Article CAS PubMed Google Scholar
• Foeller, E. & Feldman, D. E. Synaptic basis for developmental plasticity in somatosensory cortex. Curr. Opin. Neurobiol. 14, 89–95 (2004).
  Article CAS PubMed Google Scholar
• Hyman, S. E. & Malenka, R. C. Addiction and the brain: the neurobiology of compulsion and its persistence. Nature Rev. Neurosci. 2, 695–703 (2001).
  Article CAS Google Scholar
• Kalivas, P. W. & Volkow, N. D. The neural basis of addiction: a pathology of motivation and choice. Am. J. Psychiatry 162, 1403–1413 (2005).
  Article PubMed Google Scholar
• Montague, P. R., Hyman, S. E. & Cohen, J. D. Computational roles for dopamine in behavioural control. Nature 431, 760–767 (2004).
  Article CAS PubMed Google Scholar
• Hyman, S. E., Malenka, R. C. & Nestler, E. J. Neural mechanisms of addiction: the role of reward–related learning and memory. Annu. Rev. Neurosci. 29, 565–598 (2006).
  Article CAS PubMed Google Scholar
• Kauer, J. A. Learning mechanisms in addiction: synaptic plasticity in the ventral tegmental area as a result of exposure to drugs of abuse. Annu. Rev. Physiol. 66, 447–475 (2004).
  Article CAS PubMed Google Scholar
• Kelley, A. E. Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44, 161–179 (2004).
  Article CAS PubMed Google Scholar
• Badiani, A. & Robinson, T. E. Drug-induced neurobehavioral plasticity: the role of environmental context. Behav. Pharmacol. 15, 327–339 (2004).
  Article CAS PubMed Google Scholar
• Kitamura, O., Wee, S., Specio, S. E., Koob, G. F. & Pulvirenti, L. Escalation of methamphetamine self-administration in rats: a dose-effect function. Psychopharmacology (Berl) 186, 48–53 (2006).
  Article CAS Google Scholar
• Morris, R. G. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur. J. Neurosci. 23, 2829–2846 (2006).
  Article CAS PubMed Google Scholar
• Schenk, S., Valadez, A., Worley, C. M. & McNamara, C. Blockade of the acquisition of cocaine self-administration by the NMDA antagonist MK-801 (dizocilpine). Behav. Pharmacol. 4, 652–659 (1993).
  CAS PubMed Google Scholar
• Kalivas, P. W. & Alesdatter, J. E. Involvement of NMDA receptor stimulation in the ventral tegmental area and amygdala in behavioral sensitization to cocaine. J. Pharmacol. Exp. Ther. 267, 486–495 (1993).
  CAS PubMed Google Scholar
• Harris, G. C., Wimmer, M., Byrne, R. & Aston-Jones, G. Glutamate-associated plasticity in the ventral tegmental area is necessary for conditioning environmental stimuli with morphine. Neuroscience 129, 841–847 (2004).
  Article CAS PubMed Google Scholar
• Harris, G. C. & Aston-Jones, G. Critical role for ventral tegmental glutamate in preference for a cocaine-conditioned environment. Neuropsychopharmacology 28, 73–76 (2003).
  Article CAS PubMed Google Scholar
• Karler, R., Calder, L. D., Chaudhry, I. A. & Turkanis, S. A. Blockade of “reverse tolerance” to cocaine and amphetamine by MK-801. Life Sciences 45, 599–606 (1989).
  Article CAS PubMed Google Scholar
• Jeziorski, M., White, F. J. & Wolf, M. E. MK-801 prevents the development of behavioral sensitization during repeated morphine administration. Synapse 16, 137–147 (1994).
  Article CAS PubMed Google Scholar
• Kim, H. S., Park, W. K., Jang, C. G. & Oh, S. Inhibition by MK-801 of cocaine-induced sensitization, conditioned place preference, and dopamine-receptor supersensitivity in mice. Brain. Res. Bull. 40, 201–207 (1996).
  Article CAS PubMed Google Scholar
• Tzschentke, T. M. & Schmidt, W. J. N-methyl-D-aspartic acid-receptor antagonists block morphine-induced conditioned place preference in rats. Neurosci. Lett. 193, 37–40 (1995).
  Article CAS PubMed Google Scholar
• Kalivas, P. W. & Stewart, J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res. Rev. 16, 223–244 (1991).
  Article CAS PubMed Google Scholar
• Robinson, T. E. & Berridge, K. C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Rev. 18, 247–291 (1993).
  Article CAS PubMed Google Scholar
• Tong, Z. Y., Overton, P. G. & Clark, D. Chronic administration of (+)-amphetamine alters the reactivity of midbrain dopaminergic neurons to prefrontal cortex stimulation in the rat. Brain Res. 674, 63–74 (1995).
  Article CAS PubMed Google Scholar
• Wolf, M. E. The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog. Neurobiology 54, 1–42 (1998).
  Article Google Scholar
• Everitt, B. J. & Wolf, M. E. Psychomotor stimulant addiction: a neural systems perspective. J. Neurosci. 22, 3312–3320 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Kalivas, P. W. Glutamate systems in cocaine addiction. Curr. Opin. Pharmacol. 4, 23–29 (2004).
  Article CAS PubMed Google Scholar
• Baler, R. D. & Volkow, N. D. Drug addiction: the neurobiology of disrupted self-control. Trends Mol. Med. 12, 559–566 (2006).
  Article CAS PubMed Google Scholar
• Malenka, R. C. & Nicoll, R. A. Long-term potentiation — a decade of progress? Science 285, 1870–1874 (1999).
  Article CAS PubMed Google Scholar
• Lynch, M. A. Long-term potentiation and memory. Physiol. Rev. 84, 87–136 (2004).
  Article CAS PubMed Google Scholar
• Yuste, R. & Bonhoeffer, T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24, 1071–1089 (2001).
  Article CAS PubMed Google Scholar
• Matsuzaki, M., Honkura, N., Ellis-Davies, G. C. & Kasai, H. Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761–766 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Lau, C. G. & Zukin, R. S. (2007). NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nature Rev. Neurosci. 8, 413–426.
  Article CAS Google Scholar
• Nicoll, R. A. & Schmitz, D. Synaptic plasticity at hippocampal mossy fibre synapses. Nature Rev. Neurosci. 6, 863–876 (2005).
  Article CAS Google Scholar
• Yeckel, M. F., Kapur, A. & Johnston, D. Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nature Neurosci. 2, 625–633 (1999).
  Article CAS PubMed Google Scholar
• Contractor, A., Rogers, C., Maron, C., Henkemeyer, M., Swanson, G. T. & Heinemann S. F. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296, 1864–1869 (2002).
  Article CAS PubMed Google Scholar
• Castillo, P. E., Schoch, S., Schmitz, F., Sudhof, T. C. & Malenka, R. C. RIM1α is required for presynaptic long-term potentiation. Nature 415, 327–330 (2002).
  Article CAS PubMed Google Scholar
• Castillo, P. E. et al. Rab3A is essential for mossy fibre long-term potentiation in the hippocampus. Nature 388, 590–593 (1997).
  Article CAS PubMed Google Scholar
• Carroll, R. C., Beattie, E. C., von Zastrow, M. & Malenka, R. C. Role of AMPA receptor endocytosis in synaptic plasticity. Nature Rev. Neurosci. 2, 315–324 (2001).
  Article CAS Google Scholar
• Selig, D. K., Hjelmstad, G. O., Herron, C., Nicoll, R. A. & Malenka, R. C. Independent mechanisms for long-term depression of AMPA and NMDA responses. Neuron 15, 417–426 (1995).
  Article CAS PubMed Google Scholar
• Morishita, W., Marie, H. & Malenka, R. C. Distinct triggering and expression mechanisms underlie LTD of AMPA and NMDA synaptic responses. Nature Neurosci. 8, 1043–1050 (2005).
  Article CAS PubMed Google Scholar
• Ito, M. Long-term depression. Annu. Rev. Neurosci. 12, 85–102 (1989).
  Article CAS PubMed Google Scholar
• Pfeiffer, B. E. & Huber, K. M. Current advances in local protein synthesis and synaptic plasticity. J. Neurosci. 26, 7147–7150 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Wilson, R. I. & Nicoll, R. A. Endocannabinoid signaling in the brain. Science 296, 678–682 (2002).
  Article CAS PubMed Google Scholar
• Chevaleyre, V., Takahashi, K. A. & Castillo, P. E. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu. Rev. Neurosci. 29, 37–76 (2006).
  Article CAS PubMed Google Scholar
• Chevaleyre, V. et al. Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1α. Neuron 54, 801–812 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Turrigiano, G. G. & Nelson, S. B. Homeostatic plasticity in the developing nervous system. Nature Rev. Neurosci. 5, 97–107 (2004).
  Article CAS Google Scholar
• Wierenga, C. J., Ibata, K. & Turrigiano, G. G. Postsynaptic expression of homeostatic plasticity at neocortical synapses. J. Neurosci. 25, 2895–2905 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Stellwagen, D. & Malenka, R. C. Synaptic scaling mediated by glial TNF-α. Nature 440, 1054–1059 (2006).
  Article CAS PubMed Google Scholar
• Di Chiara, G. & Imperato, A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl Acad. Sci. USA 85, 5274–5278 (1980).
  Article Google Scholar
• Omelchenko, N. & Sesack, S. R. Glutamate synaptic inputs to ventral tegmental area neurons in the rat derive primarily from subcortical sources. Neuroscience 146, 1259–1274 (2007).
  Article CAS PubMed Google Scholar
• Carr, D. B. & Sesack, S. R. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J. Neurosci. 20, 3864–3873 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Overton, P. G., Richards, C. D., Berry, M. S. & Clark, D. Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons. Neuroreport 10, 221–226 (1999).
  Article CAS PubMed Google Scholar
• Bonci, A. & Malenka, R. C. Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J. Neurosci. 19, 3723–3730 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Mansvelder, H. D. & McGehee, D. S. Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27, 349–357 (2000).
  Article CAS PubMed Google Scholar
• Liu, Q. S., Pu, L. & Poo, M. M. Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons. Nature 437, 1027–1031 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Jones, S., Kornblum, J. L. & Kauer, J. A. Amphetamine blocks long-term synaptic depression in the ventral tegmental area. J. Neurosci. 20, 5575–5580 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Thomas, M. T., Malenka, R. C. & Bonci, A. Modulation of long-term depression by dopamine in the mesolimbic system. J. Neurosci. 20, 5581–5586 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Bellone, C. & Luscher, C. mGluRs induce a long-term depression in the ventral tegmental area that involves a switch of the subunit composition of AMPA receptors. Eur. J. Neurosci. 21, 1280–1288 (2005).
  Article PubMed Google Scholar
• Ungless, M. A., Whistler, J. L., Malenka, R. C. & Bonci, A. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411, 583–587 (2001).
  Article CAS PubMed Google Scholar
• Saal, D., Dong, Y., Bonci, A. & Malenka, R. C. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37, 577–582 (2003).
  Article CAS PubMed Google Scholar
• Faleiro, L. J., Jones, S. & Kauer, J. A. Rapid synaptic plasticity of glutamatergic synapses on dopamine neurons in the ventral tegmental area in response to acute amphetamine injection. Neuropsychopharmacology 29, 2115–2125 (2004). References 60–62 demonstrate that in vivo administration of different classes of drugs of abuse, as well as acute stress, elicit LTP at excitatory synapses on midbrain dopamine neurons.
  Article CAS PubMed Google Scholar
• Marinelli, M. & Piazza, P. V. Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur. J. Neurosci. 16, 387–394 (2002).
  Article PubMed Google Scholar
• Wallace, B. C. Psychological and environmental determinants of relapse in crack cocaine smokers. J. Subst. Abuse Treat. 6, 95–106 (1989).
  Article CAS PubMed Google Scholar
• Stewart, J. Stress and relapse to drug seeking: studies in laboratory animals shed light on mechanisms and sources of long-term vulnerability. Am. J. Addict. 12, 1–17 (2003).
  Article CAS PubMed Google Scholar
• Piazza, P. V. & Le Moal, M. The role of stress in drug self-administration. Trends Pharmacol. Sci. 19, 67–74 (1998).
  Article CAS PubMed Google Scholar
• Dong, Y. et al. Cocaine-induced potentiation of synaptic strength in dopamine neurons: behavioral correlates in GluRA(−/−) mice. Proc. Natl Acad. Sci. USA 101, 14282–14287 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Malinow, R. & Malenka, R. C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103–126 (2002).
  Article CAS PubMed Google Scholar
• Carlezon Jr, W. A. et al. Sensitization to morphine induced by viral-mediated gene transfer. Science 277, 812–814 (1997). Demonstration that viral-mediated expression of GluR1 in the ventral tegmental area enhances the locomotor stimulatory and rewarding actions of morphine.
  Article CAS Google Scholar
• Borgland, S. L., Malenka, R. C. & Bonci, A. Acute and chronic cocaine-induced potentiation of synaptic strength in the ventral tegmental area: electrophysiological and behavioral correlates in individual rats. J. Neurosci. 24, 7482–7490 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Neisewander, J. L. et al. Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J. Neurosci. 20, 798–805 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Pu, L., Liu, Q. S. & Poo, M. M. BDNF-dependent synaptic sensitization in midbrain dopamine neurons after cocaine withdrawal. Nature Neurosci. 9, 605–607 (2006).
  Article CAS PubMed Google Scholar
• Lu, L., Dempsey, J., Liu, S. Y., Bossert, J. M. & Shaham, Y. A single infusion of brain-derived neurotrophic factor into the ventral tegmental area induces long-lasting potentiation of cocaine seeking after withdrawal. J. Neurosci. 24, 1604–1611 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Liu, S. J. & Zukin, R. S. Ca2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 30, 126–134 (2007).
  Article CAS PubMed Google Scholar
• Carlezon Jr, W. A. & Nestler, E. J. Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci. 25, 610–615 (2002).
  Article Google Scholar
• Ju, W. et al. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nature Neurosci. 7, 244–253 (2004).
  Article CAS PubMed Google Scholar
• Clem, R. L. & Barth, A. Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49, 663–670 (2006).
  Article CAS PubMed Google Scholar
• Plant, K. et al. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nature Neurosci. 9, 602–604 (2006).
  Article CAS PubMed Google Scholar
• Adesnik, H. & Nicoll, R. A. Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J. Neurosci. 27, 4598–4602 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Bagal, A. A., Kao, J. P., Tang, C. M. & Thompson, S. M. Long-term potentiation of exogenous glutamate responses at single dendritic spines. Proc. Natl Acad. Sci. USA 102, 14434–14439 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Bellone, C. & Luscher, C. Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nature Neurosci. 9, 636–641 (2006).
  Article CAS PubMed Google Scholar
• Mameli, M., Balland, B., Lujan, R. & Luscher, C. Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science 317, 530–533 (2007). References 81 and 82 present evidence that a novel form of mGluR-LTD reverses the cocaine-induced LTP at excitatory synapses on ventral tegmental area dopamine cells.
  Article CAS PubMed Google Scholar
• de Lecea, L. et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl Acad. Sci. USA 95, 322–327 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Sakurai, T. et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573–585 (1998).
  Article CAS PubMed Google Scholar
• Harris, G. C. & Aston-Jones, G. Arousal and reward: a dichotomy in orexin function. Trends Neurosci. 29, 571–577 (2006).
  Article CAS PubMed Google Scholar
• Fadel, J. & Deutch, A. Y. Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience 111, 379–387 (2002).
  Article CAS PubMed Google Scholar
• Baldo, B. A., Daniel, R. A., Berridge, C. W. & Kelley, A. E. Overlapping distributions of orexin/hypocretin- and dopamine-β-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. J. Comp. Neurol. 464, 220–237 (2003).
  Article PubMed Google Scholar
• Boutrel, B. Hypocretins: between desire and needs. toward the understanding of a new hypothalamic brain pathway involved in motivation and addiction. Med. Sci. (Paris) 22, 573–575 (2006).
  Article Google Scholar
• Harris, G. C., Wimmer, M. & Aston-Jones, G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437, 556–559 (2005). Demonstration that orexin neurons in the lateral hypothalamus play a key role in the reinstatement of drug-seeking behaviour at least in part due to actions of orexin A in the ventral tegmental area.
  Article CAS PubMed Google Scholar
• Narita, M. et al. Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J. Neurosci. 26, 398–405 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Borgland, S. L., Taha, S. A., Sarti, F., Fields, H. L. & Bonci, A. Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49, 589–601 (2006). Demonstration that orexin A enhances NMDAR-mediated synaptic currents in ventral tegmental area (VTA) dopamine neurons and that its actions in the VTA are required for behavioural sensitization to cocaine.
  Article CAS PubMed Google Scholar
• Schilstrom, B. et al. Cocaine enhances NMDA receptor-mediated currents in ventral tegmental area cells via dopamine D5 receptor-dependent redistribution of NMDA receptors. J. Neurosci. 26, 8549–8558 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Yim, C. Y. & Mogenson, G. J. Electrophysiological studies of neurons in the ventral tegmental area of Tsai. Brain Res. 181, 301–313 (1980).
  Article CAS PubMed Google Scholar
• Johnson, S. W. & North, R. A. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 12, 483–488 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Mansvelder, H. D., Keath, J. R. & McGehee, D. S. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33, 905–919 (2002).
  Article CAS PubMed Google Scholar
• Nugent, F. S., Penick, E. C. & Kauer, J. A. Opioids block long-term potentiation of inhibitory synapses. Nature 446, 1086–1090 (2007). Demonstration of LTP of inhibitory synapses on ventral tegmental area dopamine neurons due to a long-lasting enhancement of GABA release triggered by NMDAR-dependent release of nitric oxide from the dopamine neurons. Exposure to morphine in vivo blocks this LTP by interrupting the signalling from nitric oxide to guanylate cyclase.
  Article CAS PubMed Google Scholar
• Martin, M., Chen, B. T., Hopf, F. W., Bowers, M. S. & Bonci, A. Cocaine self-administration selectively abolishes LTD in the core of the nucleus accumbens. Nature Neurosci. 9, 868–869 (2006).
  Article CAS PubMed Google Scholar
• Cardinal, R. N. & Everitt, B. J. Neural and psychological mechanisms underlying appetitive learning: links to drug addiction. Curr. Opin. Neurobiol. 14, 156–162 (2004).
  Article CAS PubMed Google Scholar
• Kalivas, P. W., Volkow, N. & Seamans, J. Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron 45, 647–650 (2005).
  Article CAS PubMed Google Scholar
• Pierce, R. C. & Kumaresan, V. The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse? Neurosci. Biobehav. Rev. 30, 215–238 (2006).
  Article CAS PubMed Google Scholar
• Kombian, S. B. & Malenka, R. C. Simultaneous LTP of non-NMDA- and LTD of NMDA-receptor-mediated responses in the nucleus accumbens. Nature 368, 242–246 (1994).
  Article CAS PubMed Google Scholar
• Schramm, N. L., Egli, R. E. & Winder, D. G. LTP in the mouse nucleus accumbens is developmentally regulated. Synapse 45, 213–219 (2002).
  Article CAS PubMed Google Scholar
• Yao, W. D. et al. Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 41, 625–638 (2004).
  Article CAS PubMed Google Scholar
• Robbe, D., Kopf, M., Remaury, A., Bockaert, J. & Manzoni, O. J. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl Acad. Sci. USA 99, 8384–8388 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hoffman, A. F., Oz, M., Caulder, T. & Lupica, C. R. Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure. J. Neurosci. 23, 4815–4820 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Brebner, K. et al. Nucleus accumbens long-term depression and the expression of behavioral sensitization. Science 310, 1340–1343 (2005).
  Article CAS PubMed Google Scholar
• Thomas, M. J., Beurrier, C., Bonci, A. & Malenka, R. C. Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nature Neurosci. 4, 1217–1223 (2001). References 106 and 107 demonstrate that in animals, which had previously been exposed to cocaine to elicit sensitization, a single subsequent dose of cocaine elicits LTD at excitatory synapses in the nucleus accumbens and that preventing this LTD in vivo prevents the expression of behavioral sensitization.
  Article CAS PubMed Google Scholar
• Schramm-Sapyta, N. L., Olsen, C. M. & Winder, D. G. Cocaine self-administration reduces excitatory responses in the mouse nucleus accumbens shell. Neuropsychopharmacology 31, 1444–1451 (2006).
  Article CAS PubMed Google Scholar
• Kourrich, S., Rothwell, P., Klug, J. & Thomas, M. Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J. Neurosci. 27, 7921–7928 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Robinson, T. E. & Kolb, B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47, S33–S46 (2004).
  Article CAS Google Scholar
• Boudreau, A. C. & Wolf, M. E. Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J. Neurosci. 25, 9144–9151 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Pierce, R. C., Bell, K., Duffy, P. & Kalivas, P. W. Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J. Neurosci. 16, 1550–1560 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Cornish, J. L. & Kalivas, P. W. Glutamate transmission in the nucleus accumbens mediates relapse in cocaine addiction. J. Neurosci. 20, RC89 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Fourgeaud, L. et al. A single in vivo exposure to cocaine abolishes endocannabinoid-mediated long-term depression in the nucleus accumbens. J. Neurosci. 24, 6939–6945 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Mato, S. et al. A single in vivo exposure to δ9THC blocks endocannabinoid-mediated synaptic plasticity. Nature Neurosci. 7, 585–596 (2004). References 114 and 115 demonstrate that a single in vivo dose of cocaine or THC abolishes endocannabinoid-mediated LTD in the nucleus accumbens.
  Article CAS PubMed Google Scholar
• Mato, S., Robbe, D., Puente, N., Grandes, P. & Manzoni, O. J. Presynaptic homeostatic plasticity rescues long-term depression after chronic δ9-tetrahydrocannabinol exposure. J. Neurosci. 25, 11619–11627 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Goto, Y. & Grace, A. A. Dopamine-dependent interactions between limbic and prefrontal cortical plasticity in the nucleus accumbens: disruption by cocaine sensitization. Neuron 47, 255–266 (2005).
  Article CAS PubMed Google Scholar
• Baker, D. A. et al. Neuroadaptations in cystine-glutamate exchange underlie cocaine relapse. Nature Neurosci. 6, 743–749 (2003).
  Article CAS PubMed Google Scholar
• Szumlinski, K. K., Kalivas, P. W. & Worley, P. F. Homer proteins: implications for neuropsychiatric disorders. Curr. Opin. Neurobiol. 16, 251–257 (2006).
  Article CAS PubMed Google Scholar
• Sutton, M. A. et al. Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour. Nature 421, 70–75 (2003).
  Article CAS PubMed Google Scholar
• Kelz, M. B. et al. Expression of the transcription factor δFosB in the brain controls sensitivity to cocaine. Nature 401, 272–276 (1999).
  Article CAS PubMed Google Scholar
• Todtenkopf, M. S. et al. Brain reward regulated by AMPA receptor subunits in nucleus accumbens shell. J. Neurosci. 26, 11665–11669 (2006). References 120–122 demonstrate that expression of AMPA receptor subunits in the nucleus accumbens influence cocaine-induced behaviours as well as the rewarding impact of electrical stimulation in the medial forebrain bundle.
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, X. F., Hu, X. T. & White, F. J. Whole-cell plasticity in cocaine withdrawal: reduced sodium currents in nucleus accumbens neurons. J. Neurosci. 18, 488–498 (1998).
  Article PubMed PubMed Central Google Scholar
• Hu, X. T., Basu, S. & White, F. J. Repeated cocaine administration suppresses HVA-Ca2+ potentials and enhances activity of K+ channels in rat nucleus accumbens neurons. J. Neurophysiol. 92, 15971–15977 (2004).
  Article Google Scholar
• Dong, Y. et al. CREB modulates excitability of nucleus accumbens neurons. Nature Neurosci. 9, 475–477 (2006).
  Article CAS PubMed Google Scholar
• Tsankova, N., Renthal, W., Kumar, A. & Nestler, E. J. Epigenetic regulation in psychiatric disorders. Nature Rev. Neurosci. 8, 355–367 (2007).
  Article CAS Google Scholar
• Delfs, J. M., Zhu, Y., Druhan, J. P. & Aston-Jones, G. Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion. Nature 403, 430–434 (2000).
  Article CAS PubMed Google Scholar
• Walker, J. R., Ahmed, S. H., Gracy, K. N. & Koob, G. F. Microinjections of an opiate receptor antagonist into the bed nucleus of the stria terminalis suppress heroin self-administration in dependent rats. Brain Res. 854, 85–92 (2000).
  Article CAS PubMed Google Scholar
• Weitlauf, C., Egli, R. E., Grueter, B. A. & Winder, D. G. High-frequency stimulation induces ethanol-sensitive long-term potentiation at glutamatergic synapses in the dorsolateral bed nucleus of the stria terminalis. J. Neurosci. 24, 5741–5747 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Dumont, E. C., Mark, G. P., Mader, S. & Williams, J. T. Self-administration enhances excitatory synaptic transmission in the bed nucleus of the stria terminalis. Nature Neurosci. 8, 413–414 (2005). Demonstration that self-administration of cocaine potentiates excitatory synaptic transmission in the bed nucleus of the stria terminalis, but that passive administration of cocaine or food does not.
  Article CAS PubMed Google Scholar
• Grueter, B. A. et al. Extracellular-signal regulated kinase 1-dependent metabotropic glutamate receptor 5-induced long-term depression in the bed nucleus of the stria terminalis is disrupted by cocaine administration. J. Neurosci. 26, 3210–3219 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Sigurdsson, T., Doyere, V., Cain, C. K. & LeDoux, J. E. Long-term potentiation in the amygdala: a cellular mechanism of fear learning and memory. Neuropharmacology 52, 215–227 (2007).
  Article CAS PubMed Google Scholar
• Childress, A. R. et al. Limbic activation during cue-induced cocaine craving. Am. J. Psychiatry 156, 11–18 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Fu, Y. et al. Long-term potentiation (LTP) in the central amygdala (CeA) is enhanced after prolonged withdrawal from chronic cocaine and requires CRF1 receptors. J. Neurophysiol. 97, 937–941 (2007).
  Article CAS PubMed Google Scholar
• Richter, R. M. & Weiss, F. In vivo CRF release in rat amygdala is increased during cocaine withdrawal in self-administering rats. Synapse 32, 254–261 (1999).
  Article CAS PubMed Google Scholar
• Pollandt, S. et al. Cocaine withdrawal enhances long-term potentiation induced by corticotropin-releasing factor at central amygdala glutamatergic synapses via CRF, NMDA receptors and PKA. Eur. J. Neurosci. 24, 1733–1743 (2006).
  Article PubMed Google Scholar
• Gong, S. et al. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917–925 (2003).
  Article CAS PubMed Google Scholar
• Kreitzer, A. C. & Malenka, R. C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445, 643–647 (2007).
  Article CAS PubMed Google Scholar
• Day, M. et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nature Neurosci. 9, 251–259 (2006).
  Article CAS PubMed Google Scholar
• Lee, K. W. et al. Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc. Natl Acad. Sci. USA 103, 3399–4304 (2006). References 138–140 use BAC transgenic mice to demonstrate cell specific modifications of medium spiny neuron synapses in the dorsal and ventral striatum following in vivo manipulations.
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, F. et al. Multimodal fast optical interrogation of neural circuitry. Nature 446, 633–639 (2007).
  Article CAS PubMed Google Scholar
• Zhang, F., Aravanis, A. M, Adamantidis, A., de Lecea, L. & Deisseroth, K. Circuit-breakers: optical technologies for probing neural signals and systems. Nature Rev. Neurosci. 8, 577–581 (2007).
  Article CAS Google Scholar
• Schultz W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259–288 (2007).
  Article CAS PubMed Google Scholar