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Meal schedule influences food restriction-induced locomotor sensitization to methamphetamine

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Abstract

Rationale

Traditional protocols for inducing sensitization to psychostimulants use an intermittent or “binge”-like drug administration, and binge eating behavior is comorbid with drug abuse in humans. Food restriction increases the reinforcing properties and self-administration of many drugs of abuse.

Objective

The present study tested the hypotheses that (1) food restriction induces sensitization to the locomotor stimulation observed in response to methamphetamine and (2) a binge-like feeding schedule during food restriction produces increased sensitization compared to equally restricted mice fed in three daily meals.

Methods

Male DBA/2J mice were fed ad libitum or were food restricted to either an 8% or 16% loss of body weight. Additionally, the food-restricted mice were divided into two groups that were fed in either one meal (binge) or three equal-sized meals (meal). After the reduced body weight was stable, mice were tested for locomotor activity following saline and methamphetamine (1 mg/kg) injections.

Results

Both 16% body weight loss groups exhibited sensitization to methamphetamine. Opposite to our hypothesis, the 8% meal but not the 8% binge food-restricted group demonstrated locomotor sensitization. Serum corticosterone levels were significantly higher in the meal-fed groups when compared to the binge- and ad libitum-fed groups.

Conclusions

These results support a role for feeding schedule and plasma corticosterone levels in food restriction-induced enhancement of the effects of methamphetamine.

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References

  • Avena NM, Hoebel BG (2003) A diet promoting sugar dependency causes behavioral cross-sensitization to a low dose of amphetamine. Neuroscience 122:17–20

    Article  PubMed  CAS  Google Scholar 

  • Baladi MG, France CP (2009) High fat diet and food restriction differentially modify the behavioral effects of quinpirole and raclopride in rats. Eur J Pharmacol 610:55–60

    Article  PubMed  CAS  Google Scholar 

  • Bauco P, Wise RA (1997) Synergistic effects of cocaine with lateral hypothalamic brain stimulation reward: lack of tolerance or sensitization. J Pharmacol Exp Ther 283:1160–1167

    PubMed  CAS  Google Scholar 

  • Bell SM, Stewart RB, Thompson SC, Meisch RA (1997) Food-deprivation increases cocaine-induced conditioned place preference and locomotor activity in rats. Psychopharmacology (Berl) 131:1–8

    Article  CAS  Google Scholar 

  • Bjijou Y, Stinus L, Le Moal M, Cador M (1996) Evidence for selective involvement of dopamine D1 receptors of the ventral tegmental area in the behavioral sensitization induced by intra-ventral tegmental area injections of D-amphetamine. J Pharmacol Exp Ther 277:1177–1187

    PubMed  CAS  Google Scholar 

  • Borgland SL, Malenka RC, Bonci A (2004) 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

    Article  PubMed  CAS  Google Scholar 

  • Broocks A, Schweiger U, Pirke KM (1990) Hyperactivity aggravates semistarvation-induced changes in corticosterone and triiodothyronine concentrations in plasma but not luteinizing hormone and testosterone levels. Physiol Behav 48:567–569

    Article  PubMed  CAS  Google Scholar 

  • Cabeza de Vaca S, Carr KD (1998) Food restriction enhances the central rewarding effect of abused drugs. J Neurosci 18:7502–7510

    PubMed  CAS  Google Scholar 

  • Campbell UC, Carroll ME (2001) Effects of ketoconazole on the acquisition of intravenous cocaine self-administration under different feeding conditions in rats. Psychopharmacology (Berl) 154:311–318

    Article  CAS  Google Scholar 

  • Carr KD, Kim GY, Cabeza de Vaca S (2001) Rewarding and locomotor-activating effects of direct dopamine receptor agonists are augmented by chronic food restriction in rats. Psychopharmacology (Berl) 154:420–428

    Article  CAS  Google Scholar 

  • Carr KD, Tsimberg Y, Berman Y, Yamamoto N (2003) Evidence of increased dopamine receptor signaling in food-restricted rats. Neuroscience 119:1157–1167

    Article  PubMed  CAS  Google Scholar 

  • Carroll ME, Meisch RA (1981) Determinants of increased drug self-administration due to food deprivation. Psychopharmacology (Berl) 74:197–200

    Article  CAS  Google Scholar 

  • Carroll ME, France CP, Meisch RA (1979) Food deprivation increases oral and intravenous drug intake in rats. Science 205:319–321

    Article  PubMed  CAS  Google Scholar 

  • Carroll ME, France CP, Meisch RA (1981) Intravenous self-administration of etonitazene, cocaine and phencyclidine in rats during food deprivation and satiation. J Pharmacol Exp Ther 217:241–247

    PubMed  CAS  Google Scholar 

  • Collins GT, Calinski DM, Newman AH, Grundt P, Woods JH (2008) Food restriction alters N′-propyl-4,5,6,7-tetrahydrobenzothiazole-2,6-diamine dihydrochloride (pramipexole)-induced yawning, hypothermia, and locomotor activity in rats: evidence for sensitization of dopamine D2 receptor-mediated effects. J Pharmacol Exp Ther 325:691–697

    Article  PubMed  CAS  Google Scholar 

  • Davis C, Carter JC (2009) Compulsive overeating as an addiction disorder. A review of theory and evidence. Appetite 53:1–8

    Article  PubMed  Google Scholar 

  • Deroche V, Piazza PV, Casolini P, Le Moal M, Simon H (1993) Sensitization to the psychomotor effects of amphetamine and morphine induced by food restriction depends on corticosterone secretion. Brain Res 611:352–356

    Article  PubMed  CAS  Google Scholar 

  • Donny EC, Caggiula AR, Mielke MM, Jacobs KS, Rose C, Sved AF (1998) Acquisition of nicotine self-administration in rats: the effects of dose, feeding schedule, and drug contingency. Psychopharmacology (Berl) 136:83–90

    Article  CAS  Google Scholar 

  • Gallo PV, Weinberg J (1981) Corticosterone rhythmicity in the rat: interactive effects of dietary restriction and schedule of feeding. J Nutr 111:208–218

    PubMed  CAS  Google Scholar 

  • Holderness CC, Brooks-Gunn J, Warren MP (1994) Co-morbidity of eating disorders and substance abuse review of the literature. Int J Eat Disord 16:1–34

    Article  PubMed  CAS  Google Scholar 

  • Honma KI, Honma S, Hiroshige T (1983) Critical role of food amount for prefeeding corticosterone peak in rats. Am J Physiol 245:R339–R344

    PubMed  CAS  Google Scholar 

  • Honma KI, Honma S, Hiroshige T (1984) Feeding-associated corticosterone peak in rats under various feeding cycles. Am J Physiol 246:R721–R726

    PubMed  CAS  Google Scholar 

  • Kamens HM, Burkhart-Kasch S, McKinnon CS, Li N, Reed C, Phillips TJ (2005) Sensitivity to psychostimulants in mice bred for high and low stimulation to methamphetamine. Genes Brain Behav 4:110–125

    PubMed  CAS  Google Scholar 

  • Klebanov S, Diais S, Stavinoha WB, Suh Y, Nelson JF (1995) Hyperadrenocorticism, attenuated inflammation, and the life-prolonging action of food restriction in mice. J Gerontol A Biol Sci Med Sci 50:B78–B82

    Article  PubMed  CAS  Google Scholar 

  • Lindblom J, Johansson A, Holmgren A, Grandin E, Nedergård C, Fredriksson R, Schiöth HB (2006) Increased mRNA levels of tyrosine hydroxylase and dopamine transporter in the VTA of male rats after chronic food restriction. Eur J Neurosci 23:180–186

    Article  PubMed  Google Scholar 

  • Macenski MJ, Meisch RA (1999) Cocaine self-administration under conditions of restricted and unrestricted food access. Exp Clin Psychopharmacol 7:324–337

    Article  PubMed  CAS  Google Scholar 

  • Marinelli M, Le Moal M, Piazza PV (1996) Acute pharmacological blockade of corticosterone secretion reverses food restriction-induced sensitization of the locomotor response to cocaine. Brain Res 724:251–255

    Article  PubMed  CAS  Google Scholar 

  • Marinković P, Pesić V, Loncarević N, Smiljanić K, Kanazir S, Ruzdijić S (2007) Behavioral and biochemical effects of various food-restriction regimens in the rats. Physiol Behav 92:492–499

    Article  PubMed  Google Scholar 

  • Phillips TJ, Dickinson S, Burkhart-Kasch S (1994) Behavioral sensitization to drug stimulant effects in C57BL/6J and DBA/2J inbred mice. Behav Neurosci 108:789–803

    Article  PubMed  CAS  Google Scholar 

  • Piazza PV, Le Moal M (1997) Glucocorticoids as a biological substrate of reward: physiological and pathophysiological implications. Brain Res Brain Res Rev 25:359–372

    Article  PubMed  CAS  Google Scholar 

  • Pierce RC, Born B, Adams M, Kalivas PW (1996) Repeated intra-ventral tegmental area administration of SKF-38393 induces behavioral and neurochemical sensitization to a subsequent cocaine challenge. J Pharmacol Exp Ther 278:384–392

    PubMed  CAS  Google Scholar 

  • Pierce RC, Quick EA, Reeder DC, Morgan ZR, Kalivas PW (1998) Calcium-mediated second messengers modulate the expression of behavioral sensitization to cocaine. J Pharmacol Exp Ther 286:1171–1176

    PubMed  CAS  Google Scholar 

  • Post RM (1980) Intermittent versus continuous stimulation: effect of time interval on the development of sensitization or tolerance. Life Sci 26:1275–1282

    Article  PubMed  CAS  Google Scholar 

  • Robinson TE, Berridge KC (2001) Incentive-sensitization and addiction. Addiction 96:103–114

    Article  PubMed  CAS  Google Scholar 

  • Rougé-Pont F, Marinelli M, Le Moal M, Simon H, Piazza PV (1995) Stress-induced sensitization and glucocorticoids. II. Sensitization of the increase in extracellular dopamine induced by cocaine depends on stress-induced corticosterone secretion. J Neurosci 15:7189–7195

    PubMed  Google Scholar 

  • Saal D, Dong Y, Bonci A, Malenka RC (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37:577–582

    Article  PubMed  CAS  Google Scholar 

  • Sevak RJ, Koek W, Owens WA, Galli A, Daws LC, France CP (2008) Feeding conditions differentially affect the neurochemical and behavioral effects of dopaminergic drugs in male rats. Eur J Pharmacol 592:109–115

    Article  PubMed  CAS  Google Scholar 

  • Stuber GD, Evans SB, Higgins MS, Pu Y, Figlewicz DP (2002) Food restriction modulates amphetamine-conditioned place preference and nucleus accumbens dopamine release in the rat. Synapse 46:83–90

    Article  PubMed  CAS  Google Scholar 

  • Thanos PK, Ramalhete RC, Michaelides M, Piyis YK, Wang GJ, Volkow ND (2008) Leptin receptor deficiency is associated with upregulation of cannabinoid 1 receptors in limbic brain regions. Synapse 62:637–642

    Article  PubMed  CAS  Google Scholar 

  • Ungless MA, Whistler JL, Malenka RC, Bonci A (2001) Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411:583–587

    Article  PubMed  CAS  Google Scholar 

  • Vezina P (1996) D1 dopamine receptor activation is necessary for the induction of sensitization by amphetamine in the ventral tegmental area. J Neurosci 16:2411–2420

    PubMed  CAS  Google Scholar 

  • Zhen J, Reith ME, Carr KD (2006) Chronic food restriction and dopamine transporter function in rat striatum. Brain Res 1082:98–101

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We would like to thank Sarah Y. Branch, Calais S. Williams, and Dr. Carlos A. Paladini for their helpful contributions. All experiments performed comply with the state, local, and federal laws.

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Correspondence to Michael J. Beckstead.

Additional information

This work was funded by a Research Enhancement Fund through the San Antonio Life Sciences Institute, a K01 award through the National Institutes of Health (DA21699) to MJB, and an American Heart Association grant (SDG4350066) to ALS. The authors acknowledge that there are no conflicts of interest, either real or perceived.

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Sharpe, A.L., Klaus, J.D. & Beckstead, M.J. Meal schedule influences food restriction-induced locomotor sensitization to methamphetamine. Psychopharmacology 219, 795–803 (2012). https://doi.org/10.1007/s00213-011-2401-6

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  • DOI: https://doi.org/10.1007/s00213-011-2401-6

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