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Incubation of craving and fear: behavioral and neuronal mechanisms
Yavin Shaham
Branch Chief
Behavioral Neuroscience Branch, IRP-NIDA, NIH
Using a rat model of drug relapse and craving, we previously found time-dependent increases in
cue-induced cocaine seeking after withdrawal from the drug, suggesting that cocaine craving
incubates over time. In this lecture, I will summarize results from studies on the generality of this
incubation phenomenon to other drugs and non-drugs rewards and to fear conditioning in a rat model
of delayed-onset PTSD. I will then summarize results for a series of studies on the neuronal
mechanisms of incubation of drug craving.
Selected references
Grimm JW, Hope B, Wise RA, Shaham Y (2001) Incubation of cocaine craving after withdrawal. Nature 412:141142
Grimm JW, Lu L, Hayashi T, Su TP, Hope BT, Shaham Y (2003) Time dependent increases in brain-derived
neurotrophic factor (BDNF) protein levels within the mesolimbic dopamine system following withdrawal from
cocaine: implications for incubation of cocaine craving. The Journal of Neuroscience 23:742-747
Lu L, Dempsey J, Liu S, Bossert J, Shaham Y (2004) A single infusion of BDNF into the ventral tegmental area
induces long-lasting potentiation of cocaine-seeking after withdrawal. The Journal of Neuroscience 24:16041611
Lu L, Hope BT, Dempsey J, Liu S, Bossert JM, Shaham Y (2005) Central amygdala ERK signaling pathway is
critical to incubation of cocaine craving. Nature Neuroscience 8:212-219
Lu L, Uejima JL, Gray SM, Bossert JM, Shaham Y (2007) Systemic and central amygdala injections of the
mGluR2/3 agonist LY379268 attenuate the expression of incubation of cocaine craving. Biological Psychiatry
61:591-598
Conrad KL, Tseng K, Uejima J, Reimers J, Heng L, Shaham Y, Marinelli M, Wolf ME (2008, July) Formation of
accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454:118-121
YG, Li FQ, Wang, XY, Wu P, Zhao M, Xu CM, Shaham Y, Lu L (2008) Central amygdala ERK signaling pathway
is critical to incubation of opiate craving. The Journal of Neuroscience 28:13248-13257
Pickens CL, Golden SA, Adams-Deutsch T, Nair SG, Shaham Y (2009) Long-lasting incubation of conditioned
fear in rats. Biological Psychiatry 65:881-886
Koya E, Uejima J, Wihbey K, Bossert JM, Hope BT, Shaham Y (2009) Role of ventral medial prefrontal cortex in
incubation of cocaine craving. Neuropharmacology 56(S1):117-185
Lu L, Wang X, Wu P, Zhao M, Morales M, Harvey BK, Hoffer BJ, Shaham Y (2009) Role of ventral tegmental
area GDNF in incubation of cocaine craving. Biological Psychiatry 66:137-145
Bedi G, Marrone GF, Preston KL, Epstein DH, Heishman SJ, King AC, Shaham Y, de Wit H (2011) Incubation of
cue-induced cigarette craving during abstinence in human smokers. Biological Psychiatry 69:708-711
Pickens CL, Airavaara M, Theberge F, Fanous S, Hope BT, Shaham Y (2011) Neurobiology of incubation of drug
craving. Trends in Neuroscience 34:411-420
Fanous S, Goldart EM, Schrama R, Theberge FR, Bossert JM, Shaham Y, Hope BT (2012) Role of orbitofrontal
cortex neuronal ensembles in the expression of incubation of heroin craving. The Journal of Neuroscience
32:11600-11609
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