Hippocampal-Dependent Inhibitory Learning and Memory Processes in the Control of Eating and Drug Taking

Author(s): Matthew M. Clasen*, Anthony L. Riley, Terry L. Davidson

Journal Name: Current Pharmaceutical Design

Volume 26 , Issue 20 , 2020

Become EABM
Become Reviewer
Call for Editor


As manifestations of excessive and uncontrolled intake, obesity and drug addiction have generated much research aimed at identifying common neuroadaptations that could underlie both disorders. Much work has focused on changes in brain reward and motivational circuitry that can overexcite eating and drug-taking behaviors. We suggest that the regulation of both behaviors depends on balancing excitation produced by stimuli associated with food and drug rewards with the behavioral inhibition produced by physiological “satiety” and other stimuli that signal when those rewards are unavailable. Our main hypothesis is that dysregulated eating and drug use are consequences of diet- and drug-induced degradations in this inhibitory power. We first outline a learning and memory mechanism that could underlie the inhibition of both food and drug-intake, and we describe data that identifies the hippocampus as a brain substrate for this mechanism. We then present evidence that obesitypromoting western diets (WD) impair the operation of this process and generate pathophysiologies that disrupt hippocampal functioning. Next, we present parallel evidence that drugs of abuse also impair this same learning and memory process and generate similar hippocampal pathophysiologies. We also describe recent findings that prior WD intake elevates drug self-administration, and the implications of using drugs (i.e., glucagon-like peptide- 1 agonists) that enhance hippocampal functioning to treat both obesity and addiction are also considered. We conclude with a description of how both WD and drugs of abuse could initiate a “vicious-cycle” of hippocampal pathophysiology and impaired hippocampal-dependent behavioral inhibition.

Keywords: Obesity, drug abuse, learning, memory, hippocampus, Western diet, vicious-cycle model.

Ogden CL, Carroll MD, Lawman HG, et al. Trends in obesity prevalence among children and adolescents in the United States, 1988-1994 through 2013-2014. JAMA 2016; 315(21): 2292-9.
[http://dx.doi.org/10.1001/jama.2016.6361] [PMID: 27272581]
Ng M, Fleming T, Robinson M, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384(9945): 766-81.
[http://dx.doi.org/10.1016/S0140-6736(14)60460-8] [PMID: 24880830]
Bose J, Hedden SL, Lipari RN. Key substance use and mental health indicators in the United States: results from the 2017 national survey on drug use and health. Rockville, MD: Substance Abuse and Mental Health Services Administration, US Department of Health and Human Services 2018.
Peacock A, Leung J, Larney S, et al. Global statistics on alcohol, tobacco and illicit drug use: 2017 status report. Addiction 2018; 113(10): 1905-26.
[http://dx.doi.org/10.1111/add.14234] [PMID: 29749059]
Blum K, Thanos PK, Gold MS. Dopamine and glucose, obesity, and reward deficiency syndrome. Front Psychol 2014; 5: 919-30.
[http://dx.doi.org/10.3389/fpsyg.2014.00919] [PMID: 25278909]
Volkow ND, Wise RA. How can drug addiction help us understand obesity? Nat Neurosci 2005; 8(5): 555-60.
[http://dx.doi.org/10.1038/nn1452] [PMID: 15856062]
Volkow ND, Baler RD. Now vs Later brain circuits: implications for obesity and addiction. Trends Neurosci 2015; 38(6): 345-52.
[http://dx.doi.org/10.1016/j.tins.2015.04.002] [PMID: 25959611]
Volkow ND, Wang GJ, Tomasi D, Baler RD. Obesity and addiction: neurobiological overlaps. Obes Rev 2013; 14(1): 2-18.
[http://dx.doi.org/10.1111/j.1467-789X.2012.01031.x] [PMID: 23016694]
Rogers PJ. Food and drug addictions: Similarities and differences. Pharmacol Biochem Behav 2017; 153: 182-90.
[http://dx.doi.org/10.1016/j.pbb.2017.01.001] [PMID: 28063947]
Johnson AW. Eating beyond metabolic need: how environmental cues influence feeding behavior. Trends Neurosci 2013; 36(2): 101-9.
[http://dx.doi.org/10.1016/j.tins.2013.01.002] [PMID: 23333343]
Perry CJ, Zbukvic I, Kim JH, Lawrence AJ. Role of cues and contexts on drug-seeking behaviour. Br J Pharmacol 2014; 171(20): 4636-72.
[http://dx.doi.org/10.1111/bph.12735] [PMID: 24749941]
Davidson TL, Sample CH, Swithers SE. An application of Pavlovian principles to the problems of obesity and cognitive decline. Neurobiol Learn Mem 2014; 108: 172-84. a..
[http://dx.doi.org/10.1016/j.nlm.2013.07.014] [PMID: 23887140]
Davidson TL, Tracy AL, Schier LA, Swithers SE. A view of obesity as a learning and memory disorder. J Exp Psychol Anim Learn Cogn 2014; 40(3): 261-79. b..
[http://dx.doi.org/10.1037/xan0000029] [PMID: 25453037]
Bouton ME. Context, ambiguity, and classical-conditioning. Curr Dir Psychol Sci 1994; 3: 49-53.
Schepers ST, Bouton ME. Hunger as a context: food seeking that is inhibited during hunger can renew in the context of satiety. Psychol Sci 2017; 28(11): 1640-8.
[http://dx.doi.org/10.1177/0956797617719084] [PMID: 28957015]
Thrailkill EA, Bouton ME. Extinction and the associative structure of heterogeneous instrumental chains. Neurobiol Learn Mem 2016; 133: 61-8.
[http://dx.doi.org/10.1016/j.nlm.2016.06.005] [PMID: 27296700]
Todd TP, Winterbauer NE, Bouton ME. Contextual control of appetite. Renewal of inhibited food-seeking behavior in sated rats after extinction. Appetite 2012; 58(2): 484-9.
[http://dx.doi.org/10.1016/j.appet.2011.12.006] [PMID: 22200411]
Rosas JM, Todd TP, Bouton ME. Context change and associative learning. Wiley Interdiscip Rev Cogn Sci 2013; 4(3): 237-44.
[http://dx.doi.org/10.1002/wcs.1225] [PMID: 23772263]
Swartzentruber D. Modulatory mechanisms in Pavlovian conditioning. Anim Learn Behav 1995; 23: 123-43.
Andersen P, Morris R, Amaral D, Bliss T, O’Keefe J. The Hippocampus Book. 1st ed. New York, NY: Oxford University Press 2006.
Schumacher A, Vlassov E, Ito R. The ventral hippocampus, but not the dorsal hippocampus is critical for learned approach-avoidance decision making. Hippocampus 2016; 26(4): 530-42.
[http://dx.doi.org/10.1002/hipo.22542] [PMID: 26493973]
Schumacher A, Villaruel FR, Ussling A, Riaz S, Lee ACH, Ito R. Ventral hippocampal CA1 and CA3 differentially mediate learned approach-avoidance conflict processing. Curr Biol 2018; 28(8): 1318-1324.e4.
[http://dx.doi.org/10.1016/j.cub.2018.03.012] [PMID: 29606418]
Sakimoto Y, Sakata S. Hippocampal theta activity during behavioral inhibition for conflicting stimuli. Behav Brain Res 2014; 275: 183-90.
[http://dx.doi.org/10.1016/j.bbr.2014.08.063] [PMID: 25218872]
Sakimoto Y, Sakata S. The role of the hippocampal theta rhythm in non-spatial discrimination and associative learning task. Neurosci Biobehav Rev 2018; S0149-7634(18): 30315-4. Epub ahead of print.
[http://dx.doi.org/10.1016/j.neubiorev.2018.09.016] [PMID: 30261198]
Holland PC, Lamoureux JA, Han JS, Gallagher M. Hippocampal lesions interfere with Pavlovian negative occasion setting. Hippocampus 1999; 9(2): 143-57.
[http://dx.doi.org/10.1002/(SICI)1098-1063(1999)9:2<143:AID-HIPO6>3.0.CO;2-Z] [PMID: 10226775]
Ito R, Lee ACH. The role of the hippocampus in approach-avoidance conflict decision-making: Evidence from rodent and human studies. Behav Brain Res 2016; 313: 345-57.
[http://dx.doi.org/10.1016/j.bbr.2016.07.039] [PMID: 27457133]
Anderson MC, Bunce JG, Barbas H. Prefrontal-hippocampal pathways underlying inhibitory control over memory. Neurobiol Learn Mem 2016; 134(Pt A): 145-61.
[http://dx.doi.org/10.1016/j.nlm.2015.11.008] [PMID: 26642918]
Chudasama Y, Doobay VM, Liu Y. Hippocampal-prefrontal cortical circuit mediates inhibitory response control in the rat. J Neurosci 2012; 32(32): 10915-24.
[http://dx.doi.org/10.1523/JNEUROSCI.1463-12.2012] [PMID: 22875926]
Hsu TM, Noble EE, Liu CM, et al. A hippocampus to prefrontal cortex neural pathway inhibits food motivation through glucagon-like peptide-1 signaling. Mol Psychiatry 2018; 23(7): 1555-65.
[http://dx.doi.org/10.1038/mp.2017.91] [PMID: 28461695]
Hebben N, Corkin S, Eichenbaum H, Shedlack K. Diminished ability to interpret and report internal states after bilateral medial temporal resection: case H.M. Behav Neurosci 1985; 99(6): 1031-9.
[http://dx.doi.org/10.1037/0735-7044.99.6.1031] [PMID: 3843537]
Rozin PDS, Moscovitch M, Rajaram S. What causes humans to begin and end a meal? A role for memory for what has been eaten, as evidenced by a study of multiple meal eating in amnesic patients. Psychol Sci 1998; 9: 392-6.
Davidson TL, Jarrard LE. A role for hippocampus in the utilization of hunger signals. Behav Neural Biol 1993; 59(2): 167-71.
[http://dx.doi.org/10.1016/0163-1047(93)90925-8] [PMID: 8476385]
Davidson TL, Kanoski SE, Chan K, Clegg DJ, Benoit SC, Jarrard LE. Hippocampal lesions impair retention of discriminative responding based on energy state cues. Behav Neurosci 2010; 124(1): 97-105.
[http://dx.doi.org/10.1037/a0018402] [PMID: 20141284]
Kennedy PJ, Shapiro ML. Retrieving memories via internal context requires the hippocampus. J Neurosci 2004; 24(31): 6979-85.
[http://dx.doi.org/10.1523/JNEUROSCI.1388-04.2004] [PMID: 15295033]
Davidson TL, Chan K, Jarrard LE, Kanoski SE, Clegg DJ, Benoit SC. Contributions of the hippocampus and medial prefrontal cortex to energy and body weight regulation. Hippocampus 2009; 19(3): 235-52.
[http://dx.doi.org/10.1002/hipo.20499] [PMID: 18831000]
Hannapel RC, Henderson YH, Nalloor R, Vazdarjanova A, Parent MB. Ventral hippocampal neurons inhibit postprandial energy intake. Hippocampus 2017; 27(3): 274-84.
[http://dx.doi.org/10.1002/hipo.22692] [PMID: 28121049]
Henderson YO, Smith GP, Parent MB. Hippocampal neurons inhibit meal onset. Hippocampus 2013; 23(1): 100-7.
[http://dx.doi.org/10.1002/hipo.22062] [PMID: 22927320]
Hannapel R, Ramesh J, Ross A, LaLumiere RT, Roseberry AG, Parent MB. Postmeal optogenetic inhibition of dorsal or ventral hippocampal pyramidal neurons increases future intake. eNeuro 2019; 6(1): 457-518.
[http://dx.doi.org/10.1523/ENEURO.0457-18.2018] [PMID: 30693314]
Medina-Remón A, Kirwan R, Lamuela-Raventós RM, Estruch R. Dietary patterns and the risk of obesity, type 2 diabetes mellitus, cardiovascular diseases, asthma, and neurodegenerative diseases. Crit Rev Food Sci Nutr 2018; 58(2): 262-96.
[http://dx.doi.org/10.1080/10408398.2016.1158690] [PMID: 27127938]
Leigh SJ, Morris MJ. The role of reward circuitry and food addiction in the obesity epidemic: An update. Biol Psychol 2018; 131: 31-42.
[http://dx.doi.org/10.1016/j.biopsycho.2016.12.013] [PMID: 28011401]
Pérez-Ortiz JM, Galiana-Simal A, Salas E, González-Martín C, García-Rojo M, Alguacil LF. A high-fat diet combined with food deprivation increases food seeking and the expression of candidate biomarkers of addiction. Addict Biol 2017; 22(4): 1002-9.
[http://dx.doi.org/10.1111/adb.12389] [PMID: 27001197]
Stevenson RJ, Francis HM. The hippocampus and the regulation of human food intake. Psychol Bull 2017; 143(10): 1011-32.
[http://dx.doi.org/10.1037/bul0000109] [PMID: 28616995]
Yeomans MR. Adverse effects of consuming high fat-sugar diets on cognition: implications for understanding obesity. Proc Nutr Soc 2017; 76(4): 455-65.
[http://dx.doi.org/10.1017/S0029665117000805] [PMID: 28514983]
Kanoski SE, Zhang Y, Zheng W, Davidson TL. The effects of a high-energy diet on hippocampal function and blood-brain barrier integrity in the rat. J Alzheimers Dis 2010; 21(1): 207-19.
[http://dx.doi.org/10.3233/JAD-2010-091414] [PMID: 20413889]
Davidson TL, Monnot A, Neal AU, Martin AA, Horton JJ, Zheng W. The effects of a high-energy diet on hippocampal-dependent discrimination performance and blood-brain barrier integrity differ for diet-induced obese and diet-resistant rats. Physiol Behav 2012; 107(1): 26-33.
[http://dx.doi.org/10.1016/j.physbeh.2012.05.015] [PMID: 22634281]
Davidson TL, Hargrave SL, Swithers SE, et al. Inter-relationships among diet, obesity and hippocampal-dependent cognitive function. Neuroscience 2013; 253: 110-22.
[http://dx.doi.org/10.1016/j.neuroscience.2013.08.044] [PMID: 23999121]
Jones S, Sample CH, Hargrave SL, Davidson TL. Associative mechanisms underlying the function of satiety cues in the control of energy intake and appetitive behavior. Physiol Behav 2018; 192: 37-49.
[http://dx.doi.org/10.1016/j.physbeh.2018.03.017] [PMID: 29555194]
Hargrave SL, Davidson TL, Zheng W, Kinzig KP. Western diets induce blood-brain barrier leakage and alter spatial strategies in rats. Behav Neurosci 2016; 130(1): 123-35. a.
[http://dx.doi.org/10.1037/bne0000110] [PMID: 26595878]
Molteni R, Barnard RJ, Ying Z, Roberts CK, Gómez-Pinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 2002; 112(4): 803-14.
[http://dx.doi.org/10.1016/S0306-4522(02)00123-9] [PMID: 12088740]
Wang J, Freire D, Knable L, et al. Childhood and adolescent obesity and long-term cognitive consequences during aging. J Comp Neurol 2015; 523(5): 757-68.
[http://dx.doi.org/10.1002/cne.23708] [PMID: 25380530]
Beilharz JE, Maniam J, Morris MJ. Short-term exposure to a diet high in fat and sugar, or liquid sugar, selectively impairs hippocampal-dependent memory, with differential impacts on inflammation. Behav Brain Res 2016; 306: 1-7.
[http://dx.doi.org/10.1016/j.bbr.2016.03.018] [PMID: 26970578]
Tran DMD, Westbrook RF. A high-fat high-sugar diet-induced impairment in place-recognition memory is reversible and training-dependent. Appetite 2017; 110: 61-71.
[http://dx.doi.org/10.1016/j.appet.2016.12.010] [PMID: 27940315]
Hsu TM, Kanoski SE. Blood-brain barrier disruption: mechanistic links between Western diet consumption and dementia. Front Aging Neurosci 2014; 6: 88-93.
[http://dx.doi.org/10.3389/fnagi.2014.00088] [PMID: 24847262]
Daneman R, Prat A. The blood-brain barrier. Cold Spring Harb Perspect Biol 2015; 7(1): a020412
[http://dx.doi.org/10.1101/cshperspect.a020412] [PMID: 25561720]
Bogush M, Heldt NA, Persidsky Y. Blood brain barrier injury in diabetes: unrecognized effects on brain and cognition. J Neuroimmune Pharmacol 2017; 12(4): 593-601.
[http://dx.doi.org/10.1007/s11481-017-9752-7] [PMID: 28555373]
Haley MJ, Lawrence CB. The blood-brain barrier after stroke: Structural studies and the role of transcytotic vesicles. J Cereb Blood Flow Metab 2017; 37(2): 456-70.
[http://dx.doi.org/10.1177/0271678X16629976] [PMID: 26823471]
Montagne A, Zhao Z, Zlokovic BV. Alzheimer’s disease: A matter of blood-brain barrier dysfunction? J Exp Med 2017; 214(11): 3151-69.
[http://dx.doi.org/10.1084/jem.20171406] [PMID: 29061693]
van Vliet EA, Aronica E, Gorter JA. Blood-brain barrier dysfunction, seizures and epilepsy. Semin Cell Dev Biol 2015; 38: 26-34.
[http://dx.doi.org/10.1016/j.semcdb.2014.10.003] [PMID: 25444846]
Varatharaj A, Galea I. The blood-brain barrier in systemic inflammation. Brain Behav Immun 2017; 60: 1-12.
[http://dx.doi.org/10.1016/j.bbi.2016.03.010] [PMID: 26995317]
Barrientos RM, Kitt MM, Watkins LR, Maier SF. Neuroinflammation in the normal aging hippocampus. Neuroscience 2015; 309: 84-99.
[http://dx.doi.org/10.1016/j.neuroscience.2015.03.007] [PMID: 25772789]
Lyman M, Lloyd DG, Ji X, Vizcaychipi MP, Ma D. Neuroinflammation: the role and consequences. Neurosci Res 2014; 79: 1-12.
[http://dx.doi.org/10.1016/j.neures.2013.10.004] [PMID: 24144733]
Kern L, Mittenbühler MJ, Vesting AJ, Ostermann AL, Wunderlich CM, Wunderlich FT. Obesity-induced TNFα and IL-6 signaling: the missing link between obesity and inflammation-driven liver and colorectal cancers. Cancers (Basel) 2018; 11(1): 11-32.
[http://dx.doi.org/10.3390/cancers11010024] [PMID: 30591653]
Laflamme N, Rivest S. Effects of systemic immunogenic insults and circulating proinflammatory cytokines on the transcription of the inhibitory factor kappaB alpha within specific cellular populations of the rat brain. J Neurochem 1999; 73(1): 309-21.
[http://dx.doi.org/10.1046/j.1471-4159.1999.0730309.x] [PMID: 10386984]
Terrando N, Eriksson LI, Ryu JK, et al. Resolving postoperative neuroinflammation and cognitive decline. Ann Neurol 2011; 70(6): 986-95.
[http://dx.doi.org/10.1002/ana.22664] [PMID: 22190370]
Guillemot-Legris O, Muccioli GG. Obesity-induced neuroinflammation: beyond the hypothalamus. Trends Neurosci 2017; 40(4): 237-53.
[http://dx.doi.org/10.1016/j.tins.2017.02.005] [PMID: 28318543]
Hao S, Dey A, Yu X, Stranahan AM. Dietary obesity reversibly induces synaptic stripping by microglia and impairs hippocampal plasticity. Brain Behav Immun 2016; 51: 230-9.
[http://dx.doi.org/10.1016/j.bbi.2015.08.023] [PMID: 26336035]
Sobesky JL, Barrientos RM, De May HS, et al. High-fat diet consumption disrupts memory and primes elevations in hippocampal IL-1β, an effect that can be prevented with dietary reversal or IL-1 receptor antagonism. Brain Behav Immun 2014; 42: 22-32.
[http://dx.doi.org/10.1016/j.bbi.2014.06.017] [PMID: 24998196]
Beilharz JE, Maniam J, Morris MJ. Diet-induced cognitive deficits: The role of fat and sugar, potential mechanisms and nutritional interventions. Nutrients 2015; 7(8): 6719-38.
[http://dx.doi.org/10.3390/nu7085307] [PMID: 26274972]
Beilharz JE, Kaakoush NO, Maniam J, Morris MJ. The effect of short-term exposure to energy-matched diets enriched in fat or sugar on memory, gut microbiota and markers of brain inflammation and plasticity. Brain Behav Immun 2016; 57: 304-13.
[http://dx.doi.org/10.1016/j.bbi.2016.07.151] [PMID: 27448745]
Boitard C, Cavaroc A, Sauvant J, et al. Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain Behav Immun 2014; 40: 9-17.
[http://dx.doi.org/10.1016/j.bbi.2014.03.005] [PMID: 24662056]
Pardridge WM, Boado RJ, Farrell CR. Brain-type glucose transporter (GLUT-1) is selectively localized to the blood-brain barrier. Studies with quantitative western blotting and in situ hybridization. J Biol Chem 1990; 265(29): 18035-40.
[PMID: 2211679]
Thorens B, Mueckler M. Glucose transporters in the 21st Century. Am J Physiol Endocrinol Metab 2010; 298(2): E141-5.
[http://dx.doi.org/10.1152/ajpendo.00712.2009] [PMID: 20009031]
Jais A, Solas M, Backes H, et al. Myeloid-cell-derived VEGF maintains brain glucose uptake and limits cognitive impairment in obesity. Cell 2016; 166(5): 1338-40.
[http://dx.doi.org/10.1016/j.cell.2016.08.010] [PMID: 27565353]
Schüler R, Seebeck N, Osterhoff MA, et al. VEGF and GLUT1 are highly heritable, inversely correlated and affected by dietary fat intake: Consequences for cognitive function in humans. Mol Metab 2018; 11: 129-36.
[http://dx.doi.org/10.1016/j.molmet.2018.02.004] [PMID: 29506909]
Hargrave SL, Davidson TL, Lee TJ, Kinzig KP. Brain and behavioral perturbations in rats following Western diet access. Appetite 2015; 93: 35-43.
[http://dx.doi.org/10.1016/j.appet.2015.03.037] [PMID: 25862980]
Glick SD, Cox RD. Changes in morphine self-administration after tel-diencephalic lesions in rats. Psychopharmacology (Berl) 1978; 57(3): 283-8.
[http://dx.doi.org/10.1007/BF00426752] [PMID: 97710]
Chambers RA, Self DW. Motivational responses to natural and drug rewards in rats with neonatal ventral hippocampal lesions: an animal model of dual diagnosis schizophrenia. Neuropsychopharmacology 2002; 27(6): 889-905.
[http://dx.doi.org/10.1016/S0893-133X(02)00365-2] [PMID: 12464446]
Chambers RA, Taylor JR. Animal modeling dual diagnosis schizophrenia: sensitization to cocaine in rats with neonatal ventral hippocampal lesions. Biol Psychiatry 2004; 56(5): 308-16.
[http://dx.doi.org/10.1016/j.biopsych.2004.05.019] [PMID: 15336512]
Brady AM, Saul RD, Wiest MK. Selective deficits in spatial working memory in the neonatal ventral hippocampal lesion rat model of schizophrenia. Neuropharmacology 2010; 59(7-8): 605-11.
[http://dx.doi.org/10.1016/j.neuropharm.2010.08.012] [PMID: 20732335]
Karlsson RM, Kircher DM, Shaham Y, O’Donnell P. Exaggerated cue-induced reinstatement of cocaine seeking but not incubation of cocaine craving in a developmental rat model of schizophrenia. Psychopharmacology (Berl) 2013; 226(1): 45-51.
[http://dx.doi.org/10.1007/s00213-012-2882-y] [PMID: 23010798]
Berg SA, Sentir AM, Cooley BS, Engleman EA, Chambers RA. Nicotine is more addictive, not more cognitively therapeutic in a neurodevelopmental model of schizophrenia produced by neonatal ventral hippocampal lesions. Addict Biol 2014; 19(6): 1020-31.
[http://dx.doi.org/10.1111/adb.12082] [PMID: 23919443]
Berg SA, Czachowski CL, Chambers RA. Alcohol seeking and consumption in the NVHL neurodevelopmental rat model of schizophrenia. Behav Brain Res 2011; 218(2): 346-9.
[http://dx.doi.org/10.1016/j.bbr.2010.12.017] [PMID: 21184782]
Conroy SK, Rodd Z, Chambers RA. Ethanol sensitization in a neurodevelopmental lesion model of schizophrenia in rats. Pharmacol Biochem Behav 2007; 86(2): 386-94.
[http://dx.doi.org/10.1016/j.pbb.2006.07.017] [PMID: 16934862]
Sell LA, Morris JS, Bearn J, Frackowiak RS, Friston KJ, Dolan RJ. Neural responses associated with cue evoked emotional states and heroin in opiate addicts. Drug Alcohol Depend 2000; 60(2): 207-16.
[http://dx.doi.org/10.1016/S0376-8716(99)00158-1] [PMID: 10940548]
Wexler BE, Gottschalk CH, Fulbright RK, et al. Functional magnetic resonance imaging of cocaine craving. Am J Psychiatry 2001; 158(1): 86-95.
[http://dx.doi.org/10.1176/appi.ajp.158.1.86] [PMID: 11136638]
Kilts CD, Schweitzer JB, Quinn CK, et al. Neural activity related to drug craving in cocaine addiction. Arch Gen Psychiatry 2001; 58(4): 334-41.
[http://dx.doi.org/10.1001/archpsyc.58.4.334] [PMID: 11296093]
Schneider F, Habel U, Wagner M, et al. Subcortical correlates of craving in recently abstinent alcoholic patients. Am J Psychiatry 2001; 158(7): 1075-83.
[http://dx.doi.org/10.1176/appi.ajp.158.7.1075] [PMID: 11431229]
Franklin TR, Wang Z, Wang J, et al. Limbic activation to cigarette smoking cues independent of nicotine withdrawal: a perfusion fMRI study. Neuropsychopharmacology 2007; 32(11): 2301-9.
[http://dx.doi.org/10.1038/sj.npp.1301371] [PMID: 17375140]
Fuchs RA, Evans KA, Ledford CC, et al. The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology 2005; 30(2): 296-309.
[http://dx.doi.org/10.1038/sj.npp.1300579] [PMID: 15483559]
Fuchs RA, Eaddy JL, Su ZI, Bell GH. Interactions of the basolateral amygdala with the dorsal hippocampus and dorsomedial prefrontal cortex regulate drug context-induced reinstatement of cocaine-seeking in rats. Eur J Neurosci 2007; 26(2): 487-98.
[http://dx.doi.org/10.1111/j.1460-9568.2007.05674.x] [PMID: 17650119]
Wells AM, Lasseter HC, Xie X, Cowhey KE, Reittinger AM, Fuchs RA. Interaction between the basolateral amygdala and dorsal hippocampus is critical for cocaine memory reconsolidation and subsequent drug context-induced cocaine-seeking behavior in rats. Learn Mem 2011; 18(11): 693-702.
[http://dx.doi.org/10.1101/lm.2273111] [PMID: 22005750]
Xie X, Ramirez DR, Lasseter HC, Fuchs RA. Effects of mGluR1 antagonism in the dorsal hippocampus on drug context-induced reinstatement of cocaine-seeking behavior in rats. Psychopharmacology (Berl) 2010; 208(1): 1-11.
[http://dx.doi.org/10.1007/s00213-009-1700-7] [PMID: 19847405]
McGlinchey EM, Aston-Jones G. Dorsal hippocampus drives context-induced cocaine seeking via inputs to lateral septum. Neuropsychopharmacology 2018; 43(5): 987-1000.
[http://dx.doi.org/10.1038/npp.2017.144] [PMID: 28695893]
Rogers JL, See RE. Selective inactivation of the ventral hippocampus attenuates cue-induced and cocaine-primed reinstatement of drug-seeking in rats. Neurobiol Learn Mem 2007; 87(4): 688-92.
[http://dx.doi.org/10.1016/j.nlm.2007.01.003] [PMID: 17337218]
Kutlu MG, Gould TJ. Effects of drugs of abuse on hippocampal plasticity and hippocampus-dependent learning and memory: contributions to development and maintenance of addiction. Learn Mem 2016; 23(10): 515-33.
[http://dx.doi.org/10.1101/lm.042192.116] [PMID: 27634143]
Cadet JL, Bisagno V. Neuropsychological consequences of chronic drug use: relevance to treatment approaches. Front Psychiatry 2016; 6: 189-98.
[http://dx.doi.org/10.3389/fpsyt.2015.00189] [PMID: 26834649]
Meltzer JA, Constable RT. Activation of human hippocampal formation reflects success in both encoding and cued recall of paired associates. Neuroimage 2005; 24(2): 384-97.
[http://dx.doi.org/10.1016/j.neuroimage.2004.09.001] [PMID: 15627581]
Squire LR, Ojemann JG, Miezin FM, Petersen SE, Videen TO, Raichle ME. Activation of the hippocampus in normal humans: a functional anatomical study of memory. Proc Natl Acad Sci USA 1992; 89(5): 1837-41.
[http://dx.doi.org/10.1073/pnas.89.5.1837] [PMID: 1542680]
Tulving E, Markowitsch HJ. Episodic and declarative memory: role of the hippocampus. Hippocampus 1998; 8(3): 198-204.
[http://dx.doi.org/10.1002/(SICI)1098-1063(1998)8:3<198:AID-HIPO2>3.0.CO;2-G] [PMID: 9662134]
Hartley T, Bird CM, Chan D, et al. The hippocampus is required for short-term topographical memory in humans. Hippocampus 2007; 17(1): 34-48.
[http://dx.doi.org/10.1002/hipo.20240] [PMID: 17143905]
Saling MM. Verbal memory in mesial temporal lobe epilepsy: beyond material specificity. Brain 2009; 132(Pt 3): 570-82.
[http://dx.doi.org/10.1093/brain/awp012] [PMID: 19251757]
Aharonovich E, Liu X, Samet S, Nunes E, Waxman R, Hasin D. Postdischarge cannabis use and its relationship to cocaine, alcohol, and heroin use: a prospective study. Am J Psychiatry 2005; 162(8): 1507-14.
[http://dx.doi.org/10.1176/appi.ajp.162.8.1507] [PMID: 16055773]
Aharonovich E, Hasin DS, Brooks AC, Liu X, Bisaga A, Nunes EV. Cognitive deficits predict low treatment retention in cocaine dependent patients. Drug Alcohol Depend 2006; 81(3): 313-22.
[http://dx.doi.org/10.1016/j.drugalcdep.2005.08.003] [PMID: 16171953]
Ardila A, Rosselli M, Strumwasser S. Neuropsychological deficits in chronic cocaine abusers. Int J Neurosci 1991; 57(1-2): 73-9.
[http://dx.doi.org/10.3109/00207459109150348] [PMID: 1938157]
Kalapatapu RK, Vadhan NP, Rubin E, et al. A pilot study of neurocognitive function in older and younger cocaine abusers and controls. Am J Addict 2011; 20(3): 228-39.
[http://dx.doi.org/10.1111/j.1521-0391.2011.00128.x] [PMID: 21477051]
O’Malley S, Adamse M, Heaton RK, Gawin FH. Neuropsychological impairment in chronic cocaine abusers. Am J Drug Alcohol Abuse 1992; 18(2): 131-44.
[http://dx.doi.org/10.3109/00952999208992826] [PMID: 1562011]
Vonmoos M, Hulka LM, Preller KH, et al. Cognitive dysfunctions in recreational and dependent cocaine users: role of attention-deficit hyperactivity disorder, craving and early age at onset. Br J Psychiatry 2013; 203(1): 35-43.
[http://dx.doi.org/10.1192/bjp.bp.112.118091] [PMID: 23703315]
Woicik PA, Moeller SJ, Alia-Klein N, et al. The neuropsychology of cocaine addiction: recent cocaine use masks impairment. Neuropsychopharmacology 2009; 34(5): 1112-22.
[http://dx.doi.org/10.1038/npp.2008.60] [PMID: 18496524]
Ornstein TJ, Iddon JL, Baldacchino AM, et al. Profiles of cognitive dysfunction in chronic amphetamine and heroin abusers. Neuropsychopharmacology 2000; 23(2): 113-26.
[http://dx.doi.org/10.1016/S0893-133X(00)00097-X] [PMID: 10882838]
Simon SL, Domier C, Carnell J, Brethen P, Rawson R, Ling W. Cognitive impairment in individuals currently using methamphetamine. Am J Addict 2000; 9(3): 222-31.
[http://dx.doi.org/10.1080/10550490050148053] [PMID: 11000918]
Simon SL, Domier CP, Sim T, Richardson K, Rawson RA, Ling W. Cognitive performance of current methamphetamine and cocaine abusers. J Addict Dis 2002; 21(1): 61-74.
[http://dx.doi.org/10.1300/J069v21n01_06] [PMID: 11831501]
Simon SL, Dacey J, Glynn S, Rawson R, Ling W. The effect of relapse on cognition in abstinent methamphetamine abusers. J Subst Abuse Treat 2004; 27(1): 59-66.
[http://dx.doi.org/10.1016/j.jsat.2004.03.011] [PMID: 15223095]
Jacobsen LK, Krystal JH, Mencl WE, Westerveld M, Frost SJ, Pugh KR. Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol Psychiatry 2005; 57(1): 56-66.
[http://dx.doi.org/10.1016/j.biopsych.2004.10.022] [PMID: 15607301]
Nixon SJ, Kujawski A, Parsons OA, Yohman JR. Semantic (verbal) and figural memory impairment in alcoholics. J Clin Exp Neuropsychol 1987; 9(4): 311-22.
[http://dx.doi.org/10.1080/01688638708405053] [PMID: 3597725]
Davis PE, Liddiard H, McMillan TM. Neuropsychological deficits and opiate abuse. Drug Alcohol Depend 2002; 67(1): 105-8.
[http://dx.doi.org/10.1016/S0376-8716(02)00012-1] [PMID: 12062785]
Curran HV, Kleckham J, Bearn J, Strang J, Wanigaratne S. Effects of methadone on cognition, mood and craving in detoxifying opiate addicts: a dose-response study. Psychopharmacology (Berl) 2001; 154(2): 153-60.
[http://dx.doi.org/10.1007/s002130000628] [PMID: 11314677]
Battisti RA, Roodenrys S, Johnstone SJ, Respondek C, Hermens DF, Solowij N. Chronic use of cannabis and poor neural efficiency in verbal memory ability. Psychopharmacology (Berl) 2010; 209(4): 319-30.
[http://dx.doi.org/10.1007/s00213-010-1800-4] [PMID: 20217055]
Messinis L, Kyprianidou A, Malefaki S, Papathanasopoulos P. Neuropsychological deficits in long-term frequent cannabis users. Neurology 2006; 66(5): 737-9.
[http://dx.doi.org/10.1212/01.wnl.0000201279.83203.c6] [PMID: 16534113]
Pope HG Jr, Yurgelun-Todd D. The residual cognitive effects of heavy marijuana use in college students. JAMA 1996; 275(7): 521-7.
[http://dx.doi.org/10.1001/jama.1996.03530310027028] [PMID: 8606472]
Pope HG Jr, Gruber AJ, Hudson JI, Huestis MA, Yurgelun-Todd D. Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 2001; 58(10): 909-15.
[http://dx.doi.org/10.1001/archpsyc.58.10.909] [PMID: 11576028]
Solowij N, Stephens RS, Roffman RA, et al. Marijuana Treatment Project Research Group. Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA 2002; 287(9): 1123-31.
[http://dx.doi.org/10.1001/jama.287.9.1123] [PMID: 11879109]
Schuster RM, Crane NA, Mermelstein R, Gonzalez R. The influence of inhibitory control and episodic memory on the risky sexual behavior of young adult cannabis users. J Int Neuropsychol Soc 2012; 18(5): 827-33.
[http://dx.doi.org/10.1017/S1355617712000586] [PMID: 22676889]
Davidson TL, Hargrave SL, Kearns DN, et al. Cocaine impairs serial-feature negative learning and blood-brain barrier integrity. Pharmacol Biochem Behav 2018; 170: 56-63.
[http://dx.doi.org/10.1016/j.pbb.2018.05.005] [PMID: 29753886]
Yao H, Duan M, Buch S. Cocaine-mediated induction of platelet-derived growth factor: implication for increased vascular permeability. Blood 2011; 117(8): 2538-47.
[http://dx.doi.org/10.1182/blood-2010-10-313593] [PMID: 21148086]
Rodríguez-Arias M, Montagud-Romero S, Rubio-Araiz A, et al. Effects of repeated social defeat on adolescent mice on cocaine-induced CPP and self-administration in adulthood: integrity of the blood-brain barrier. Addict Biol 2017; 22(1): 129-41.
[http://dx.doi.org/10.1111/adb.12301] [PMID: 26374627]
Gonçalves J, Leitão RA, Higuera-Matas A, et al. Extended-access methamphetamine self-administration elicits neuroinflammatory response along with blood-brain barrier breakdown. Brain Behav Immun 2017; 62: 306-17.
[http://dx.doi.org/10.1016/j.bbi.2017.02.017] [PMID: 28237710]
Bowyer JF, Ali S. High doses of methamphetamine that cause disruption of the blood-brain barrier in limbic regions produce extensive neuronal degeneration in mouse hippocampus. Synapse 2006; 60(7): 521-32.
[http://dx.doi.org/10.1002/syn.20324] [PMID: 16952162]
Bowyer JF, Thomas M, Schmued LC, Ali SF. Brain region-specific neurodegenerative profiles showing the relative importance of amphetamine dose, hyperthermia, seizures, and the blood-brain barrier. Ann N Y Acad Sci 2008; 1139: 127-39.
[http://dx.doi.org/10.1196/annals.1432.005] [PMID: 18991857]
Martins T, Baptista S, Gonçalves J, et al. Methamphetamine transiently increases the blood-brain barrier permeability in the hippocampus: role of tight junction proteins and matrix metalloproteinase-9. Brain Res 2011; 1411: 28-40.
[http://dx.doi.org/10.1016/j.brainres.2011.07.013] [PMID: 21803344]
Kousik SM, Graves SM, Napier TC, Zhao C, Carvey PM. Methamphetamine-induced vascular changes lead to striatal hypoxia and dopamine reduction. Neuroreport 2011; 22(17): 923-8.
[http://dx.doi.org/10.1097/WNR.0b013e32834d0bc8] [PMID: 21979424]
ElAli A, Urrutia A, Rubio-Araiz A, et al. Apolipoprotein-E controls adenosine triphosphate-binding cassette transporters ABCB1 and ABCC1 on cerebral microvessels after methamphetamine intoxication. Stroke 2012; 43(6): 1647-53.
[http://dx.doi.org/10.1161/STROKEAHA.111.648923] [PMID: 22426312]
Ramirez SH, Potula R, Fan S, et al. Methamphetamine disrupts blood-brain barrier function by induction of oxidative stress in brain endothelial cells. J Cereb Blood Flow Metab 2009; 29(12): 1933-45.
[http://dx.doi.org/10.1038/jcbfm.2009.112] [PMID: 19654589]
Mahajan SD, Aalinkeel R, Sykes DE, et al. Methamphetamine alters blood brain barrier permeability via the modulation of tight junction expression: Implication for HIV-1 neuropathogenesis in the context of drug abuse. Brain Res 2008; 1203: 133-48.
[http://dx.doi.org/10.1016/j.brainres.2008.01.093] [PMID: 18329007]
Banerjee A, Zhang X, Manda KR, Banks WA, Ercal N. HIV proteins (gp120 and Tat) and methamphetamine in oxidative stressinduced damage in the brain: potential role of the thiol antioxidant N-acetylcysteine amide. Free Radic Biol Med 2010; 48: 1388-98.
Toborek M, Seelbach MJ, Rashid CS, et al. Voluntary exercise protects against methamphetamine-induced oxidative stress in brain microvasculature and disruption of the blood-brain barrier. Mol Neurodegener 2013; 8: 22.
[http://dx.doi.org/10.1186/1750-1326-8-22] [PMID: 23799892]
Sajja RK, Rahman S, Cucullo L. Drugs of abuse and blood-brain barrier endothelial dysfunction: A focus on the role of oxidative stress. J Cereb Blood Flow Metab 2016; 36(3): 539-54.
[http://dx.doi.org/10.1177/0271678X15616978] [PMID: 26661236]
Mazzone P, Tierney W, Hossain M, Puvenna V, Janigro D, Cucullo L. Pathophysiological impact of cigarette smoke exposure on the cerebrovascular system with a focus on the blood-brain barrier: expanding the awareness of smoking toxicity in an underappreciated area. Int J Environ Res Public Health 2010; 7(12): 4111-26.
[http://dx.doi.org/10.3390/ijerph7124111] [PMID: 21317997]
Abbruscato TJ, Lopez SP, Mark KS, Hawkins BT, Davis TP. Nicotine and cotinine modulate cerebral microvascular permeability and protein expression of ZO-1 through nicotinic acetylcholine receptors expressed on brain endothelial cells. J Pharm Sci 2002; 91(12): 2525-38.
[http://dx.doi.org/10.1002/jps.10256] [PMID: 12434396]
Hawkins BT, Abbruscato TJ, Egleton RD, et al. Nicotine increases in vivo blood-brain barrier permeability and alters cerebral microvascular tight junction protein distribution. Brain Res 2004; 1027(1-2): 48-58.
[http://dx.doi.org/10.1016/j.brainres.2004.08.043] [PMID: 15494156]
Manda VK, Mittapalli RK, Bohn KA, Adkins CE, Lockman PR. Nicotine and cotinine increases the brain penetration of saquinavir in rat. J Neurochem 2010; 115(6): 1495-507.
[http://dx.doi.org/10.1111/j.1471-4159.2010.07054.x] [PMID: 20950334]
Sharma HS, Ali SF. Alterations in blood-brain barrier function by morphine and methamphetamine. Ann N Y Acad Sci 2006; 1074: 198-224.
[http://dx.doi.org/10.1196/annals.1369.020] [PMID: 17105918]
Little KY, Ramssen E, Welchko R, Volberg V, Roland CJ, Cassin B. Decreased brain dopamine cell numbers in human cocaine users. Psychiatry Res 2009; 168(3): 173-80.
[http://dx.doi.org/10.1016/j.psychres.2008.10.034] [PMID: 19233481]
Sekine Y, Ouchi Y, Sugihara G, et al. Methamphetamine causes microglial activation in the brains of human abusers. J Neurosci 2008; 28(22): 5756-61.
[http://dx.doi.org/10.1523/JNEUROSCI.1179-08.2008] [PMID: 18509037]
He J, Crews FT. Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol 2008; 210(2): 349-58.
[http://dx.doi.org/10.1016/j.expneurol.2007.11.017] [PMID: 18190912]
Ghavimi H, Charkhpour M, Ghasemi S, et al. Pioglitazone prevents morphine antinociceptive tolerance via ameliorating neuroinflammation in rat cerebral cortex. Pharmacol Rep 2015; 67(1): 78-84.
[http://dx.doi.org/10.1016/j.pharep.2014.08.003] [PMID: 25560579]
Bradford ST, Stamatovic SM, Dondeti RS, Keep RF, Andjelkovic AV. Nicotine aggravates the brain postischemic inflammatory response. Am J Physiol Heart Circ Physiol 2011; 300(4): H1518-29.
[http://dx.doi.org/10.1152/ajpheart.00928.2010] [PMID: 21239632]
Kousik SM, Napier TC, Carvey PM. The effects of psychostimulant drugs on blood brain barrier function and neuroinflammation. Front Pharmacol 2012; 3: 121-33.
[http://dx.doi.org/10.3389/fphar.2012.00121] [PMID: 22754527]
Erickson EK, Blednov YA, Harris RA, Mayfield RD. Glial gene networks associated with alcohol dependence. Sci Rep 2019; 9(1): 10949-62.
[http://dx.doi.org/10.1038/s41598-019-47454-4] [PMID: 31358844]
Kohno M, Link J, Dennis LE, et al. Neuroinflammation in addiction: A review of neuroimaging studies and potential immunotherapies. Pharmacol Biochem Behav 2019; 179: 34-42.
[http://dx.doi.org/10.1016/j.pbb.2019.01.007] [PMID: 30695700]
Woods SC. Gastrointestinal satiety signals I. An overview of gastrointestinal signals that influence food intake. Am J Physiol Gastrointest Liver Physiol 2004; 286(1): G7-G13.
[http://dx.doi.org/10.1152/ajpgi.00448.2003] [PMID: 14665437]
Lynch WJ, Carroll ME. Regulation of drug intake. Exp Clin Psychopharmacol 2001; 9(2): 131-43.
[http://dx.doi.org/10.1037/1064-1297.9.2.131] [PMID: 11518086]
Norman AB, Tsibulsky VL. Satiety threshold regulates maintained self-administration: comment on Lynch and Carroll (2001). Exp Clin Psychopharmacol 2001; 9(2): 151-4.
[http://dx.doi.org/10.1037/1064-1297.9.2.151] [PMID: 11518089]
Panlilio LV, Katz JL, Pickens RW, Schindler CW. Variability of drug self-administration in rats. Psychopharmacology (Berl) 2003; 167(1): 9-19.
[http://dx.doi.org/10.1007/s00213-002-1366-x] [PMID: 12644888]
Tsibulsky VL, Norman AB. Satiety threshold during maintained cocaine self-administration in outbred mice. Neuroreport 2001; 12(2): 325-8.
[http://dx.doi.org/10.1097/00001756-200102120-00029] [PMID: 11209944]
Colpaert FC, Slangen JL. Risk and protective factors and estimates of substance use initiation: Results from the 2016 National Survey on Drug Use and Health InCBHSQ data review . Substance Abuse and Mental Health Services Administration (US). 2017.
Balster RL. Drugs as chemical stimuliTransduction mechanisms of drug stimuli. Berlin, Heidelberg: Springer 1988; pp. 3-11.
Colpaert FC. Drug discrimination in neurobiology. Pharmacol Biochem Behav 1999; 64(2): 337-45.
[http://dx.doi.org/10.1016/S0091-3057(99)00047-7] [PMID: 10515310]
Porter JH, Prus AJ. Discriminative stimulus properties of atypical and typical antipsychotic drugs: a review of preclinical studies. Psychopharmacology (Berl) 2009; 203(2): 279-94.
[http://dx.doi.org/10.1007/s00213-008-1308-3] [PMID: 18795269]
Glennon RA, Järbe TU, Frankenheim J. Drug discrimination: applications to drug abuse research. US Department of Health and Human Services, Public Health Service, Alcohol, Drug Abuse, and Mental Health Administration, National Institute on Drug Abuse 1991.
Riley AL. Use of drug discrimination learning in behavioral toxicology: classification and characterization of toxins Neurotoxicology: approaches and methods. San Diego, CA: Academic Press 1995; pp. 309-21.
Järbe TU. Drug discrimination learning Experimental psychopharmacology. Totowa, NJ: Humana Press 1987; pp. 433-79.
Mastropaolo JP, Moskowitz KH, Dacanay RJ, Riley AL. Conditioned taste aversions as a behavioral baseline for drug discrimination learning: an assessment with phencyclidine. Pharmacol Biochem Behav 1989; 32(1): 1-8.
[http://dx.doi.org/10.1016/0091-3057(89)90203-7] [PMID: 2734321]
Overton DA. Historical context of state dependent learning and discriminative drug effects. Behav Pharmacol 1991; 2(4 And 5): 253-64.
[http://dx.doi.org/10.1097/00008877-199109000-00002] [PMID: 11224069]
Riley AL, Clasen MM, Friar M. Conditioned taste aversion baseline of drug discrimination learning: Assessments and applicationsDrug discrimination: A behavioral approach for understanding subjective drug effects. Berlin: Springer 2009; pp. 1-21.
Davidson TL, Jones S, Roy M, Stevenson RJ. The cognitive control of eating and body weight: It’s more than what you “think”. Front Psychol 2019; 10: 62-84.
[http://dx.doi.org/10.3389/fpsyg.2019.00062] [PMID: 30814963]
Clifton PG, Vickers SP, Somerville EM. Little and often: ingestive behavior patterns following hippocampal lesions in rats. Behav Neurosci 1998; 112(3): 502-11.
[http://dx.doi.org/10.1037/0735-7044.112.3.502] [PMID: 9676968]
Hargrave SL, Jones S, Davidson TL. The Outward Spiral: A vicious cycle model of obesity and cognitive dysfunction. Curr Opin Behav Sci 2016; 9: 40-6. B..
[http://dx.doi.org/10.1016/j.cobeha.2015.12.001] [PMID: 26998507]
Wellman PJ, Nation JR, Davis KW. Impairment of acquisition of cocaine self-administration in rats maintained on a high-fat diet. Pharmacol Biochem Behav 2007; 88(1): 89-93.
[http://dx.doi.org/10.1016/j.pbb.2007.07.008] [PMID: 17764729]
Puhl MD, Cason AM, Wojnicki FH, Corwin RL, Grigson PS. A history of bingeing on fat enhances cocaine seeking and taking. Behav Neurosci 2011; 125(6): 930-42.
[http://dx.doi.org/10.1037/a0025759] [PMID: 21988520]
Corsica JA, Hood MM. Eating disorders in an obesogenic environment. J Am Diet Assoc 2011; 111(7): 996-1000.
[http://dx.doi.org/10.1016/j.jada.2011.04.011] [PMID: 21703376]
King BM. The modern obesity epidemic, ancestral hunter-gatherers, and the sensory/reward control of food intake. Am Psychol 2013; 68(2): 88-96.
[http://dx.doi.org/10.1037/a0030684] [PMID: 23244211]
Chaput JP, Klingenberg L, Astrup A, Sjödin AM. Modern sedentary activities promote overconsumption of food in our current obesogenic environment. Obes Rev 2011; 12(5): e12-20.
[http://dx.doi.org/10.1111/j.1467-789X.2010.00772.x] [PMID: 20576006]
Cordain L, Eaton SB, Sebastian A, et al. Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 2005; 81(2): 341-54.
[http://dx.doi.org/10.1093/ajcn.81.2.341] [PMID: 15699220]
Rhodes D, Clemens J, Goldman J, Lacomb R, Moshfegh A. 2011- 2012 What We Eat in America, NHANES Tables 1-40 Worldwide Web Site: Food Surveys Research Group 2014.
Kubant R, Poon AN, Sánchez-Hernández D, et al. A comparison of effects of lard and hydrogenated vegetable shortening on the development of high-fat diet-induced obesity in rats. Nutr Diabetes 2015., 5e188
[http://dx.doi.org/10.1038/nutd.2015.40] [PMID: 26657014]
Biessels GJ, Reagan LP. Hippocampal insulin resistance and cognitive dysfunction. Nat Rev Neurosci 2015; 16(11): 660-71.
[http://dx.doi.org/10.1038/nrn4019] [PMID: 26462756]
Khan NA, Baym CL, Monti JM, et al. Central adiposity is negatively associated with hippocampal-dependent relational memory among overweight and obese children. J Pediatr 2015; 166(2): 302-8.e1.
[http://dx.doi.org/10.1016/j.jpeds.2014.10.008] [PMID: 25454939]
Mamrot P, Hanć T. The association of the executive functions with overweight and obesity indicators in children and adolescents: A literature review. Neurosci Biobehav Rev 2019; 107: 59-68.
[http://dx.doi.org/10.1016/j.neubiorev.2019.08.021] [PMID: 31470031]
Birch LL, Anzman SL. Learning to eat in an obesogenic environment: a developmental systems perspective on childhood obesity. Child Dev Perspect 2010; 4: 138-43.
Jasik CB, Lustig RH. Adolescent obesity and puberty: the “perfect storm”. Ann N Y Acad Sci 2008; 1135: 265-79.
[http://dx.doi.org/10.1196/annals.1429.009] [PMID: 18574233]
Kranz S, Findeis JL, Shrestha SS. Use of the Revised Children’s Diet Quality Index to assess preschooler’s diet quality, its sociodemographic predictors, and its association with body weight status. J Pediatr (Rio J) 2008; 84(1): 26-34.
[http://dx.doi.org/10.2223/JPED.1745] [PMID: 18264615]
Chambers RA, Taylor JR, Potenza MN. Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 2003; 160(6): 1041-52.
[http://dx.doi.org/10.1176/appi.ajp.160.6.1041] [PMID: 12777258]
Sinha R. Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 2008; 1141: 105-30.
[http://dx.doi.org/10.1196/annals.1441.030] [PMID: 18991954]
Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000; 24(24): 417-63. A..
[http://dx.doi.org/10.1016/S0149-7634(00)00014-2] [PMID: 10817843]
Spear LP. Neurobehavioral changes in adolescence. Curr Dir Psychol Sci 2000; 9(): 111-4. B..
Spear LP. Adolescent neurodevelopment. J Adolesc Health 2013; 52(2)(Suppl. 2): S7-S13.
[http://dx.doi.org/10.1016/j.jadohealth.2012.05.006] [PMID: 23332574]
Spear LP. A developmental biological perspective of adolescent substance abuse: animal models The Oxford Handbook of Adolescence Substance Abuse. New York, NY: Oxford University Press 2016; pp. 354-63.
Ebbeling CB, Leidig MM, Sinclair KB, Hangen JP, Ludwig DS. A reduced-glycemic load diet in the treatment of adolescent obesity. Arch Pediatr Adolesc Med 2003; 157(8): 773-9.
[http://dx.doi.org/10.1001/archpedi.157.8.773] [PMID: 12912783]
Lobstein T, Baur L, Uauy R. IASO International Obesity TaskForce. Obesity in children and young people: a crisis in public health. Obes Rev 2004; 5(Suppl. 1): 4-104.
[http://dx.doi.org/10.1111/j.1467-789X.2004.00133.x] [PMID: 15096099]
Whitaker RC, Wright JA, Pepe MS, Seidel KD, Dietz WH. Predicting obesity in young adulthood from childhood and parental obesity. N Engl J Med 1997; 337(13): 869-73.
[http://dx.doi.org/10.1056/NEJM199709253371301] [PMID: 9302300]
Boitard C, Etchamendy N, Sauvant J, et al. Juvenile, but not adult exposure to high-fat diet impairs relational memory and hippocampal neurogenesis in mice. Hippocampus 2012; 22(11): 2095-100.
[http://dx.doi.org/10.1002/hipo.22032] [PMID: 22593080]
Frazier CR, Mason P, Zhuang X, Beeler JA. Sucrose exposure in early life alters adult motivation and weight gain. PLoS One 2008; 3(9): e3221
[http://dx.doi.org/10.1371/journal.pone.0003221] [PMID: 18797507]
Blanco-Gandía MC, Cantacorps L, Aracil-Fernández A, et al. Effects of bingeing on fat during adolescence on the reinforcing effects of cocaine in adult male mice. Neuropharmacology 2017; 113(Pt A): 31-44. a.
[http://dx.doi.org/10.1016/j.neuropharm.2016.09.020] [PMID: 27666001]
Blanco-Gandía MC, Ledesma JC, Aracil-Fernández A, et al. The rewarding effects of ethanol are modulated by binge eating of a high-fat diet during adolescence. Neuropharmacology 2017; 121: 219-30.
[http://dx.doi.org/10.1016/j.neuropharm.2017.04.040] [PMID: 28457972]
Bocarsly ME, Barson JR, Hauca JM, Hoebel BG, Leibowitz SF, Avena NM. Effects of perinatal exposure to palatable diets on body weight and sensitivity to drugs of abuse in rats. Physiol Behav 2012; 107(4): 568-75.
[http://dx.doi.org/10.1016/j.physbeh.2012.04.024] [PMID: 22564493]
Clasen MM, Sanon TV, Hempel BJ, et al. Ad-libitum high fat diet consumption during adolescence and adulthood impacts the intravenous self-administration of cocaine in male Sprague-Dawley rats. Exp Clin Psychopharmacol 2019. a Epub ahead of print
Becker JB, Koob GF. Sex differences in animal models: focus on addiction. Pharmacol Rev 2016; 68(2): 242-63.
[http://dx.doi.org/10.1124/pr.115.011163] [PMID: 26772794]
Becker JB, McClellan ML, Reed BG. Sex differences, gender and addiction. J Neurosci Res 2017; 95(1-2): 136-47.
[http://dx.doi.org/10.1002/jnr.23963] [PMID: 27870394]
Riley AL, Hempel BJ, Clasen MM. Sex as a biological variable: Drug use and abuse. Physiol Behav 2018; 187: 79-96.
[http://dx.doi.org/10.1016/j.physbeh.2017.10.005] [PMID: 29030249]
Hallam J, Boswell RG, DeVito EE, Kober H. Focus: sex and gender health: gender-related differences in food craving and obesity. Yale J Biol Med 2016; 89(2): 161-73.
[PMID: 27354843]
Mauvais-Jarvis F. Sex differences in metabolic homeostasis, diabetes, and obesity. Biol Sex Differ 2015; 6: 14.
[http://dx.doi.org/10.1186/s13293-015-0033-y] [PMID: 26339468]
Palmer BF, Clegg DJ. The sexual dimorphism of obesity. Mol Cell Endocrinol 2015; 402: 113-9.
[http://dx.doi.org/10.1016/j.mce.2014.11.029] [PMID: 25578600]
Lipari RN, Ahrnsbrak RD, Pemberton MR, Porter JD. Risk and protective factors and estimates of substance use initiation: Results from the 2016 National Survey on Drug Use and Health InCBHSQ data review 2017 Sep Substance Abuse and Mental Health Services Administration (US). In:
Balster RL, Bigelow GE. Guidelines and methodological reviews concerning drug abuse liability assessment. Drug Alcohol Depend 2003; 70(3)(Suppl.): S13-40.
[http://dx.doi.org/10.1016/S0376-8716(03)00097-8] [PMID: 12759195]
McColl S, Sellers EM. Research design strategies to evaluate the impact of formulations on abuse liability. Drug Alcohol Depend 2006; 83(Suppl. 1): S52-62.
[http://dx.doi.org/10.1016/j.drugalcdep.2006.01.015] [PMID: 16554125]
O’Connor EC, Chapman K, Butler P, Mead AN. The predictive validity of the rat self-administration model for abuse liability. Neurosci Biobehav Rev 2011; 35(3): 912-38.
[http://dx.doi.org/10.1016/j.neubiorev.2010.10.012] [PMID: 21036191]
van Ree JM, Slangen JL, de Wied D. Intravenous self-administration of drugs in rats. J Pharmacol Exp Ther 1978; 204(3): 547-57.
[PMID: 633066]
Brockwell NT, Eikelboom R, Beninger RJ. Caffeine-induced place and taste conditioning: production of dose-dependent preference and aversion. Pharmacol Biochem Behav 1991; 38(3): 513-7.
[http://dx.doi.org/10.1016/0091-3057(91)90006-N] [PMID: 2068188]
Riley AL. The paradox of drug taking: the role of the aversive effects of drugs. Physiol Behav 2011; 103(1): 69-78.
[http://dx.doi.org/10.1016/j.physbeh.2010.11.021] [PMID: 21118698]
Wise RA, Yokel RA, DeWit H. Both positive reinforcement and conditioned aversion from amphetamine and from apomorphine in rats. Science 1976; 191(4233): 1273-5.
[http://dx.doi.org/10.1126/science.1257748] [PMID: 1257748]
Davis CM, Riley AL. Conditioned taste aversion learning: implications for animal models of drug abuse. Ann N Y Acad Sci 2010; 1187: 247-75.
[http://dx.doi.org/10.1111/j.1749-6632.2009.05147.x] [PMID: 20201857]
Verendeev A, Riley AL. Conditioned taste aversion and drugs of abuse: history and interpretation. Neurosci Biobehav Rev 2012; 36(10): 2193-205.
[http://dx.doi.org/10.1016/j.neubiorev.2012.08.004] [PMID: 22921283]
Tzschentke TM. Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 2007; 12(3-4): 227-462.
[http://dx.doi.org/10.1111/j.1369-1600.2007.00070.x] [PMID: 17678505]
Chester JA, Lumeng L, Li TK, Grahame NJ. High- and low-alcohol-preferring mice show differences in conditioned taste aversion to alcohol. Alcohol Clin Exp Res 2003; 27(1): 12-8.
[PMID: 12543999]
Ettenberg A, Fomenko V, Kaganovsky K, Shelton K, Wenzel JM. On the positive and negative affective responses to cocaine and their relation to drug self-administration in rats. Psychopharmacology (Berl) 2015; 232(13): 2363-75.
[http://dx.doi.org/10.1007/s00213-015-3873-6] [PMID: 25662610]
Hill KG, Alva H, Blednov YA, Cunningham CL. Reduced ethanol-induced conditioned taste aversion and conditioned place preference in GIRK2 null mutant mice. Psychopharmacology (Berl) 2003; 169(1): 108-14.
[http://dx.doi.org/10.1007/s00213-003-1472-4] [PMID: 12721779]
Shuster L. Genetics of responses to drugs of abuse. Int J Addict 1990-1991; 25(1A): 57-79.
[http://dx.doi.org/10.3109/10826089009067005] [PMID: 2246084]
Morales L, Del Olmo N, Valladolid-Acebes I, et al. Shift of circadian feeding pattern by high-fat diets is coincident with reward deficits in obese mice. PLoS One 2012; 7(5)e36139
[http://dx.doi.org/10.1371/journal.pone.0036139] [PMID: 22570696]
Blanco-Gandía MC, Aracil-Fernández A, Montagud-Romero S, et al. Changes in gene expression and sensitivity of cocaine reward produced by a continuous fat diet. Psychopharmacology (Berl) 2017; 234(15): 2337-52.c..
[http://dx.doi.org/10.1007/s00213-017-4630-9] [PMID: 28456841]
Blanco-Gandía MC, Montagud-Romero S, Aguilar MA, Miñarro J, Rodríguez-Arias M. Housing conditions modulate the reinforcing properties of cocaine in adolescent mice that binge on fat. Physiol Behav 2018; 183: 18-26.
[http://dx.doi.org/10.1016/j.physbeh.2017.10.014] [PMID: 29050902]
King HE, Riley AL. A history of morphine-induced taste aversion learning fails to affect morphine-induced place preference conditioning in rats. Learn Behav 2013; 41(4): 433-42.
[http://dx.doi.org/10.3758/s13420-013-0118-6] [PMID: 23943541]
Hunt T, Amit Z. Conditioned taste aversion induced by self-administered drugs: paradox revisited. Neurosci Biobehav Rev 1987; 11(1): 107-30.
[http://dx.doi.org/10.1016/S0149-7634(87)80005-2] [PMID: 3554039]
Dannenhoffer CA, Spear LP. Age differences in conditioned place preferences and taste aversions to nicotine. Dev Psychobiol 2016; 58(5): 660-6.
[http://dx.doi.org/10.1002/dev.21400] [PMID: 27027859]
Nelson KH, Hempel BJ, Clasen MM, Rice KC, Riley AL. Conditioned taste avoidance, conditioned place preference and hyperthermia induced by the second generation ‘bath salt’ α-pyrrolidinopentiophenone (α-PVP). Pharmacol Biochem Behav 2017; 156: 48-55.
[http://dx.doi.org/10.1016/j.pbb.2017.04.003] [PMID: 28427995]
Roma PG, Flint WW, Higley JD, Riley AL. Assessment of the aversive and rewarding effects of alcohol in Fischer and Lewis rats. Psychopharmacology (Berl) 2006; 189(2): 187-99.
[http://dx.doi.org/10.1007/s00213-006-0553-6] [PMID: 17013639]
Simpson GR, Riley AL. Morphine preexposure facilitates morphine place preference and attenuates morphine taste aversion. Pharmacol Biochem Behav 2005; 80(3): 471-9.
[http://dx.doi.org/10.1016/j.pbb.2005.01.003] [PMID: 15740790]
Turenne SD, Miles C, Parker LA, Siegel S. Individual differences in reactivity to the rewarding/aversive properties of drugs: assessment by taste and place conditioning. Pharmacol Biochem Behav 1996; 53(3): 511-6.
[http://dx.doi.org/10.1016/0091-3057(95)02042-X] [PMID: 8866948]
Clasen MM, Sanon TV, Kearns DN, Davidson TL, Riley AL. Ad libitum high fat diet consumption during adolescence and adulthood fails to impact the affective properties of cocaine in male Sprague-Dawley rats. Exp Clin Psychopharmacol In Press
[http://dx.doi.org/10.1037/pha0000328] [PMID: 31621346]
Astrup A, Carraro R, Finer N, et al. NN8022-1807 Investigators. Safety, tolerability and sustained weight loss over 2 years with the once-daily human GLP-1 analog, liraglutide. Int J Obes 2012; 36(6): 843-54.
[http://dx.doi.org/10.1038/ijo.2011.158] [PMID: 21844879]
Hayes MR, Kanoski SE, Alhadeff AL, Grill HJ. Comparative effects of the long-acting GLP-1 receptor ligands, liraglutide and exendin-4, on food intake and body weight suppression in rats. Obesity (Silver Spring) 2011; 19(7): 1342-9.
[http://dx.doi.org/10.1038/oby.2011.50] [PMID: 21415845]
Kanoski SE, Rupprecht LE, Fortin SM, De Jonghe BC, Hayes MR. The role of nausea in food intake and body weight suppression by peripheral GLP-1 receptor agonists, exendin-4 and liraglutide. Neuropharmacology 2012; 62(5-6): 1916-27.
[http://dx.doi.org/10.1016/j.neuropharm.2011.12.022] [PMID: 22227019]
Liberini CG, Lhamo R, Ghidewon M, et al. Liraglutide pharmacotherapy reduces body weight and improves glycaemic control in juvenile obese/hyperglycaemic male and female rats. Diabetes Obes Metab 2018; 21: 866-75.
[http://dx.doi.org/10.1111/dom.13591] [PMID: 30456866]
Ladenheim EE. Liraglutide and obesity: a review of the data so far. Drug Des Devel Ther 2015; 9: 1867-75.
[http://dx.doi.org/10.2147/DDDT.S58459] [PMID: 25848222]
Kanoski SE, Hayes MR, Skibicka KP. GLP-1 and weight loss: unraveling the diverse neural circuitry. Am J Physiol Regul Integr Comp Physiol 2016; 310(10): R885-95.
[http://dx.doi.org/10.1152/ajpregu.00520.2015] [PMID: 27030669]
Jones S, Sample CH, Davidson TL. The effects of a GLP-1 analog liraglutide on reward value and the learned inhibition of appetitive behavior in male and female rats. Int J Obes 2019; 43(9): 1875-9.
[http://dx.doi.org/10.1038/s41366-018-0240-9] [PMID: 30367111]
Palleria C, Leo A, Andreozzi F, et al. Liraglutide prevents cognitive decline in a rat model of streptozotocin-induced diabetes independently from its peripheral metabolic effects. Behav Brain Res 2017; 321: 157-69.
[http://dx.doi.org/10.1016/j.bbr.2017.01.004] [PMID: 28062257]
Yang Y, Fang H, Xu G, et al. Liraglutide improves cognitive impairment via the AMPK and PI3K/Akt signaling pathways in type 2 diabetic rats. Mol Med Rep 2018; 18(2): 2449-57.
[http://dx.doi.org/10.3892/mmr.2018.9180] [PMID: 29916537]
Porter DW, Kerr BD, Flatt PR, Holscher C, Gault VA. Four weeks administration of Liraglutide improves memory and learning as well as glycaemic control in mice with high fat dietary-induced obesity and insulin resistance. Diabetes Obes Metab 2010; 12(10): 891-9.
[http://dx.doi.org/10.1111/j.1463-1326.2010.01259.x] [PMID: 20920042]
McClean PL, Parthsarathy V, Faivre E, Hölscher C. The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer’s disease. J Neurosci 2011; 31(17): 6587-94.
[http://dx.doi.org/10.1523/JNEUROSCI.0529-11.2011] [PMID: 21525299]
Zhang Y, Xie JZ, Xu XY, et al. Liraglutide ameliorates hyperhomocysteinemia-induced alzheimer-like pathology and memory deficits in rats via multi-molecular targeting. Neurosci Bull 2019; 35(4): 724-34.
[http://dx.doi.org/10.1007/s12264-018-00336-7] [PMID: 30632006]
Skibicka KP. The central GLP-1: implications for food and drug reward. Front Neurosci 2013; 7: 181-90.
[http://dx.doi.org/10.3389/fnins.2013.00181] [PMID: 24133407]
Roberto M, Spierling SR, Kirson D, Zorrilla EP. Corticotropin-releasing factor (CRF) and addictive behaviorsInternational review of neurobiology. Cambridge, MA: Academic Press 2017; pp. 5-51.
Karkhanis A, Holleran KM, Jones SR. Dynorphin/kappa opioid receptor signaling in preclinical models of alcohol, drug, and food addictionInternational review of neurobiology. Cambridge, MA: Academic Press 2017; pp. 53-88.
Zallar LJ, Farokhnia M, Tunstall BJ, Vendruscolo LF, Leggio L. The role of the ghrelin system in drug addictionInternational review of neurobiology. Cambridge, MA: Academic Press 2017; pp. 89-119.
Barson JR, Leibowitz SF. Orexin/hypocretin system: role in food and drug overconsumption International review of neurobiology. Cambridge, MA: Academic Press 2017; pp. 199-237.
Thomsen M, Holst JJ, Molander A, Linnet K, Ptito M, Fink-Jensen A. Effects of glucagon-like peptide 1 analogs on alcohol intake in alcohol-preferring vervet monkeys. Psychopharmacology (Berl) 2019; 236(2): 603-11.
[http://dx.doi.org/10.1007/s00213-018-5089-z] [PMID: 30382353]
Vallöf D, Maccioni P, Colombo G, et al. The glucagon-like peptide 1 receptor agonist liraglutide attenuates the reinforcing properties of alcohol in rodents. Addict Biol 2016; 21(2): 422-37.
[http://dx.doi.org/10.1111/adb.12295] [PMID: 26303264]
Hernandez NS, Ige KY, Mietlicki-Baase EG, et al. Glucagon-like peptide-1 receptor activation in the ventral tegmental area attenuates cocaine seeking in rats. Neuropsychopharmacology 2018; 43(10): 2000-8.
[http://dx.doi.org/10.1038/s41386-018-0010-3] [PMID: 29497166]
Sørensen G, Reddy IA, Weikop P, et al. The glucagon-like peptide 1 (GLP-1) receptor agonist exendin-4 reduces cocaine self-administration in mice. Physiol Behav 2015; 149: 262-8.
[http://dx.doi.org/10.1016/j.physbeh.2015.06.013] [PMID: 26072178]

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2020
Published on: 21 June, 2020
Page: [2334 - 2352]
Pages: 19
DOI: 10.2174/1381612826666200206091447
Price: $65

Article Metrics

PDF: 15