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Fosb in the Nucleus Accumbens Regulates Food- Reinforced Instrumental Behavior and Motivation

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Fosb in the Nucleus Accumbens Regulates Food- Reinforced Instrumental Behavior and Motivation 9196 • The Journal of Neuroscience, September 6, 2006 • 26(36):9196–9204 Behavioral/Systems/Cognitive ⌬FosB in the Nucleus Accumbens Regulates Food- Reinforced Instrumental Behavior and Motivation Peter Olausson,1 J. David Jentsch,2 Natalie Tronson,1 Rachel L. Neve,3 Eric J. Nestler,4 and Jane R. Taylor1 1Department of Psychiatry, Division of Molecular Psychiatry, Yale University School of Medicine, New Haven, Connecticut 06508, 2Department of Psychology, University of California, Los Angeles, California 90095, 3Department of Psychiatry, Harvard Medical School, McLean Hospital, Belmont, Massachusetts 02178, and 4Department of Psychiatry and Center for Basic Neuroscience, The University of Texas Southwestern Medical Center, Dallas, Texas 75390 Alterations in motivation have been implicated in the pathophysiology of several psychiatric disorders, including substance abuse and depression. Repeated exposure to drugs of abuse or stress is known to persistently induce the transcription factor ⌬FosB in the nucleus accumbens (NAc) and dorsal striatum, effects hypothesized to contribute to neuroadaptations in dopamine-regulated signaling. Little is known, however, about the specific involvement of ⌬FosB in dysregulation of appetitively motivated behaviors. We show here that inducible overexpression of ⌬FosB in NAc and dorsal striatum of bitransgenic mice, or specifically in the NAc core of rats by use of viral- mediated gene transfer, enhanced food-reinforced instrumental performance and progressive ratio responding. Very similar behavioral effects were found after previous repeated exposure to cocaine, amphetamine, MDMA [(ϩ)-3,4-methylenedioxymethamphetamine], or nico- tine in rats. These results reveal the powerful regulation of motivational processes by ⌬FosB, and provide evidence that drug-induced alterations in gene expression via induction of ⌬FosB within the NAc core may play a critical role in the impact of motivational influences on instrumental behavior. Key words: addiction; psychostimulant; reinforcement; dopamine; gene expression; transcription factors Introduction The performance of instrumental responses is a necessary Repeated drug exposure causes temporally dynamic alterations component of drug-taking behavior that can become dysregu- in gene transcription that produce lasting neuroadaptations lated or inflexible as the transition to addiction progresses within the nucleus accumbens (NAc) (Nestler, 2004). This brain (Jentsch and Taylor, 1999; Berke and Hyman, 2000; Berridge and region plays a critical role in both drug and natural reinforcement Robinson, 2003; Everitt and Robbins, 2005). The NAc is involved processes (Kelley and Berridge, 2002), although little is known in multiple aspects of instrumental behavior with relevance for about the transcription factors that impact on behavior moti- addiction (Balleine and Killcross, 1994; Corbit et al., 2001; de vated by nondrug, appetitive reinforcers such as food. ⌬FosB is a Borchgrave et al., 2002; Di Ciano and Everitt, 2004b; Everitt and transcription factor activated within the NAc and dorsal striatum Robbins, 2005). It is therefore likely that drug-induced neuroad- by chronic drug exposure (Konradi et al., 1994; Nye et al., 1995; aptations within the NAc could affect performance of instrumen- Chen et al., 1997; Pich et al., 1997; Shaw-Lutchman et al., 2003) tal actions. Indeed, chronic cocaine exposure enhances sucrose- and compulsive wheel-running (Werme et al., 2002). It is also reinforced instrumental performance (Miles et al., 2004) and induced in these regions by several forms of chronic stress (Per- manipulations thought to block neuroplasticity within the NAc rotti et al., 2004). The enhancement of drug reinforcement pro- core, including inhibition of PKA (protein kinase A) or protein cesses associated with induction of striatal ⌬FosB is well estab- synthesis, interfere with food-rewarded instrumental responses lished (Kelz et al., 1999; Colby et al., 2003; Zachariou et al., 2006). (Baldwin et al., 2002a; Hernandez et al., 2002). The NAc core also The consequences of elevated ⌬FosB levels in these regions on mediates the motivational impact of conditioned influences on instrumental behavior motivated by natural reinforcers are, how- instrumental behavior (Parkinson et al., 1999; Corbit et al., 2001; ever, not known. Hall et al., 2001; Di Ciano and Everitt, 2004a; Ito et al., 2004), providing a neurobiological substrate whereby ⌬FosB induction Received March 15, 2006; revised June 23, 2006; accepted Aug. 2, 2006. might powerfully affect instrumental performance and motiva- This work was supported by grants from the National Institute on Drug Abuse, the National Institute of Mental tion for appetitive reinforcers such as food, water, or drugs of Health, and the National Institute of Alcohol Abuse and Alcoholism. We gratefully acknowledge the valuable assis- tanceofDiljaKrueger,DrewKiraly,Dr.RalphDiLeone,RobertSears,andDr.JonathanHommelattheDepartmentof abuse. Psychiatry, Yale University. We are also grateful to Dr. Jennifer Quinn and Dr. Paul Hitchcott for providing helpful Here, we investigated the effects of ⌬FosB on food-motivated comments on this manuscript. instrumental behavior using two complementary genetic ap- Correspondence should be addressed to Jane R. Taylor, Department of Psychiatry, Division of Molecular Psychi- proaches: (1) inducible overexpression of ⌬FosB within the NAc atry, Yale University School of Medicine, Ribicoff Research Facilities, Connecticut Mental Health Center, 34 Park and dorsal striatum of bitransgenic mice (NSE-tTA ϫ TetOp- Street, New Haven, CT 06508. E-mail: [email protected]. ⌬ ⌬ DOI:10.1523/JNEUROSCI.1124-06.2006 FosB) and (2) overexpression of FosB in the NAc core specif- Copyright © 2006 Society for Neuroscience 0270-6474/06/269196-09$15.00/0 ically by use of viral-mediated gene transfer in rats. We also eval- Olausson et al. • ⌬FosB in NAc Regulates Motivation J. Neurosci., September 6, 2006 • 26(36):9196–9204 • 9197 uated whether previous repeated exposure to cocaine, am- The vectors driving expression of either HSV-LacZ, coding for the con- phetamine, (ϩ)-3,4-methylenedioxymethamphetamine (MDMA), trol protein ␤-galactosidase, or HSV-⌬FosB, coding for ⌬FosB, were or nicotine, under conditions reported to increase ⌬FosB, would subsequently infused into the NAc core according to the experimental enhance food-reinforced instrumental responding and/or moti- protocol. vation using a progressive ratio schedule, as has been shown for drug-reinforced self-administration (Horger et al., 1990, 1992; Experimental procedure Piazza et al., 1990; Vezina et al., 2002; Miles et al., 2004). Our Outline. Experiment 1 examined the effects of previous repeated drug results demonstrate persistent effects of ⌬FosB on instrumental exposure on food-reinforced instrumental performance and progressive ratio responding. Rats were randomly divided into five experimental behavior and suggest that this transcription factor may act in the groups (n ϭ 9–10/group). These groups received twice daily injections NAc core as a regulator of motivational function. (intraperitoneally; at 9:00 A.M. and 5:00 P.M.) with saline or one of the following drugs: nicotine, 0.35 mg/kg; MDMA, 2.5 mg/kg; cocaine, 15 Materials and Methods mg/kg; or amphetamine, 2.5 mg/kg for 15 consecutive days. The doses Animals and animal care were selected based on our previously published data (Taylor and Experimentally naive Sprague Dawley rats were acquired from Charles Jentsch, 2001; Olausson et al., 2003), and the drug-induced locomotor River Laboratories (Wilmington, MA). Male bitransgenic 11A mice were stimulation was monitored on treatment days 1 and 15. After5dof derived from a cross between homozygous transgenic mice expressing a withdrawal, animals were trained on instrumental responding for 10 neuron-specific enolase (NSE)-tTA tetracycline transactivator protein consecutive days and subsequently tested on progressive ratio respond- (line A) and mice expressing TetOp (tetracycline-responsive promoter)- ⌬ ing on the next day. Two animals were excluded from the statistical FosB (line 11); the parental lines were maintained on an outbred mixed analysis because they did not acquire the instrumental response, making background (50% ICR and 50% C57BL6 ϫ SJL) (Chen et al., 1998; Kelz ⌬ no more than one active lever response on each of the three final training et al., 1999). These bitransgenic 11A mice express FosB only when: (1) sessions. both transgenes are present in the same cell, and (2) the transcriptional Experiments 2 and 3 examined the effects of inducible striatal overex- activation by tTA is not inhibited by the presence of tetracycline antibi- pression of ⌬FosB in bitransgenic mice on instrumental performance otics such as doxycycline. The administration of doxycycline to these ⌬ and responding on a progressive ratio of reinforcement. The inducible mice can thus exert a temporal control over the expression of FosB and overexpression of ⌬FosB in these mice has previously been demonstrated be used to prevent the expression during development; indeed, doxycy- to mimic the effects of repeated drug exposure in the locomotor activity cline administration is associated with no detectable leak expression of ⌬ and conditioned place preference paradigms (Kelz et al., 1999; Zachariou FosB (Chen et al., 1998; Kelz et al., 1999). Moreover, the 11A line of et al., 2006). These mice can provide critical information about the con- bitransgenic mice were chosen for the present
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