Nicotine is more addictive, not more cognitively therapeutic in a neurodevelopmental model of schizophrenia produced by neonatal ventral hippocampal lesions

Addiction Biology

Volumn 19, Issue 6, 2014, Pages 1020-1031

  Berg, Sarah A ^a   Sentir, Alena M ^a   Cooley, Benjamin S ^a   Engleman, Eric A ^a   Chambers, R Andrew ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Addiction; dual diagnosis; hippocampus; nicotine dependence; schizophrenia; self administration

Indexed keywords

NICOTINE; NICOTINIC AGENT;

ADOLESCENT; ADOLESCENT BEHAVIOR; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG SELF ADMINISTRATION; HIPPOCAMPUS; LOCOMOTION; MALE; NEONATAL VENTRAL HIPPOCAMPAL LESION; NERVE CELL DIFFERENTIATION; NONHUMAN; RADIAL ARM MAZE TEST; RAT; REINFORCEMENT; SCHIZOPHRENIA; SELF MEDICATION; SPATIAL LEARNING; TOBACCO DEPENDENCE; WORKING MEMORY; ANALYSIS OF VARIANCE; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; DRUG SEEKING BEHAVIOR; INSTRUMENTAL CONDITIONING; MAZE TEST; MEMORY DISORDER; NEWBORN; PATHOLOGY; PSYCHIATRIC DIAGNOSIS; PSYCHOLOGY; SHORT TERM MEMORY; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CONDITIONING, OPERANT; DIAGNOSIS, DUAL (PSYCHIATRY); DISEASE MODELS, ANIMAL; DRUG-SEEKING BEHAVIOR; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY DISORDERS; MEMORY, SHORT-TERM; NICOTINE; NICOTINIC AGONISTS; RATS, SPRAGUE-DAWLEY; REINFORCEMENT SCHEDULE; SCHIZOPHRENIC PSYCHOLOGY; SELF ADMINISTRATION; TOBACCO USE DISORDER;

EID: 84916215154     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12082     Document Type: Article

References (50)

1. Berg SA, Chambers RA, (2008) Accentuated behavioral sensitization to nicotine in the neonatal ventral hippocampal lesion model of schizophrenia. Neuropharmacology 54: 1201-1207.
2. Berg SA, Czachowski CL, Chambers RA, (2011) Alcohol seeking and consumption in the NVHL neurodevelopmental rat model of schizophrenia. Behav Brain Res 218: 346-349.
3. Bickel WK, Odum AL, Madden GJ, (1999) Impulsivity and cigarrette smoking: delay discounting in current, never, and ex-smokers. Psychopharmacology (Berl) 146: 447-454.
4. Bracken AL, Chambers RA, Berg SA, Rodd ZA, McBride WJ, (2011) Nicotine exposure during adolescence enhances behavioral sensitivity to nicotine during adulthood in Wistar rats. Pharmacol Biochem Behav 99: 87-93.
5. Brambilla P, Perlini C, Rajagopalan P, Saharan P, Rambaldelli G, Bellani M, Dusi N, Cerini R, Pozzi Mucelli R, Tansella M, Thompson PM, (2013) Schizophrenia severity, social functioning and hippocampal neuroanatomy: three-dimensional mapping study. Br J Psychiatry 202: 50-55.
6. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS, (2000) Hippocampal volume reduction in major depression. Am J Psychiatry 157: 115-118.
7. Chambers RA, (2013) Adult hippocampal neurogenesis in the pathogenesis of addiction and dual diagnosis disorders. Drug Alcohol Depend 130: 1-12.
8. Chambers RA, Jones RM, Brown S, Taylor JR, (2005) Natural reward related learning in rats with neonatal ventral hippocampal lesions and prior cocaine exposure. Psychopharmacology (Berl) 179: 470-478.
9. Chambers RA, Krystal JK, Self DW, (2001) A neurobiological basis for substance abuse comorbidity in schizophrenia. Biol Psychiatry 50: 71-83.
10. Chambers RA, Moore J, McEvoy JP, Levin ED, (1996) Cognitive effects of neonatal hippocampal lesions in a rat model of schizophrenia. Neuropsychopharmacology 15: 587-594.
11. Chambers RA, Self DW, (2002) Motivational responses to natural and drug rewards in rats with neonatal ventral hippocampal lesions: an animal model of dual diagnosis schizophrenia. Neuropsychopharmacology 27: 889-905.
12. Chambers RA, Sentir AM, Conroy SK, Truitt WA, Shekhar A, (2010a) Cortical-striatal integration of cocaine history and prefrontal dysfunction in animal modeling of dual diagnosis. Biol Psychiatry 67: 788-792.
13. Chambers RA, Sentir AM, Engleman EA, (2010b) Ventral and dorsal striatal dopamine efflux and behavior in rats with simple vs. co-morbid histories of cocaine sensitization and neonatal ventral hippocampal lesions. Psychopharmacology (Berl) 212: 73-83.
14. Chambers RA, Taylor JR, (2004) Animal modeling dual diagnosis schizophrenia: sensitization to cocaine in rats with neonatal ventral hippocampal lesions. Biol Psychiatry 56: 308-316.
15. Chambers RA, Taylor JR, Potenza MN, (2003) Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 160: 1041-1052.
16. Compton MT, Kelley ME, Ramsay CE, Pringle M, Goulding SM, Esterberg ML, Stewart T, Walker EF, (2009) Association of pre-onset cannabis, alcohol, and tobacco use with age at onset of prodrome and age at onset of psychosis in first-episode patients. Am J Psychiatry 166: 1251-1257.
17. Conroy SK, Rodd Z, Chambers RA, (2007) Ethanol sensitization in a neurodevelopmental lesion model of schizophrenia in rats. Pharmacol Biochem Behav 86: 386-394.
18. Counotte DS, Goriounova NA, Li KW, Loos M, van der Schors RC, Schetters D, Schoffelmeer AN, Smit AB, Mansvelder HD, Pattij T, Spijker S, (2011) Lasting synaptic changes underlie attention deficits caused by nicotine exposure during adolescence. Nat Neurosci 14: 417-419.
19. Counotte DS, Spijker S, Van de Burgwal LH, Hogenboom F, Schoffelmeer AN, De Vries TJ, Smit AB, Pattij T, (2009) Long-lasting cognitive deficits resulting from adolescent nicotine exposure in rats. Neuropsychopharmacology 34: 299-306.
20. Dani JA, Harris RA, (2005) Nicotine addiction and comorbidity with alcohol abuse and mental illness. Nat Neurosci 8: 1465-1470.
21. DeHay T, Morris C, May MG, Devine K, Waxmonsky J, (2012) Tobacco use in youth with mental illnesses. J Behav Med 35: 139-148.
22. Durazzo TC, Mon A, Gazdzinski S, Meyerhoff DJ, (2013) Chronic cigarette smoking in alcohol dependence: associations with cortical thickness and N-acetylaspartate levels in the extended brain reward system. Addict Biol 18: 379-391.
23. Fuller RL, Luck SJ, Braun EL, Robinson BM, McMahon RP, Gold JM, (2009) Impaired visual working memory consolidation in schizophrenia. Neuropsychology 23: 71-80.
24. Gold JM, Hahn B, Zhang WW, Robinson BM, Kappenman ES, Beck VM, Luck SJ, (2010) Reduced capacity but spared precision and maintenance of working memory representations in schizophrenia. Arch Gen Psychiatry 67: 570-577.
25. Grant BF, Hasin DS, Chou SP, Stinson FS, Dawson DA, (2004) Nicotine dependence and psychiatric disorders in the United States: results from the National Epidemiologic Survey on alcohol and related conditions. Arch Gen Psychiatry 61: 1107-1115.
26. Hahn B, (2013) A test of the cognitive self-medication hypothesis of tobacco smoking in schizophrenia. Biol Psychiatry. doi: 10.1016/j.biopsych.2013.03.017.
27. Heerey EA, Bell-Warren KR, Gold JM, (2008) Decision-making impairments in the context of intact reward sensitivity in schizophrenia. Biol Psychiatry 64: 62-69.
28. Lasser K, Boyd JW, Woolhandler S, Heimmerlstein D, McCormick D, Bor D, (2000) Smoking in mental illness: a population-based prevalence study. JAMA 284: 2606-2610.
29. Leonard S, Adler L, Benhammou K, Berger R, Breese CR, Drebring C, Gault J, Lee M, Logel J, Olincy A, Ross RG, Stevens K, Sullivan B, Vianzon R, Virnich DE, Waldo M, Walton K, Freedman R, (2001) Smoking and mental illness. Pharmacol Biochem Behav 70: 561-570.
30. Levin ED, (1988) Psychopharmacological effects in the radial-arm maze. Neurosci Biobehav Rev 12: 169-175.
31. Lipska BK, Jaskiw GE, Weinberger DR, (1993) Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia. Neuropsychopharmacology 9: 67-75.
32. Liu X, Matochik JA, Cadet JL, London ED, (1998) Smaller volume of prefrontal lobe in polysubstance abusers: a magnetic resonance imaging study. Neuropsychopharmacology 18: 243-252.
33. Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR, Craig CR, Collins AC, Damaj MI, Donny EC, Gardiner PS, Grady SR, Heberlein U, Leonard SS, Levin ED, Lukas RJ, Markou A, Marks MJ, McCallum SE, Parameswaran N, Perkins KA, Picciotto MR, Quik M, Rose JE, Rothenfluh A, Schafer WR, Stolerman IP, Tyndale RF, Wehner JM, Zirger JM, (2007) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190: 269-319.
34. McDermott MS, Marteau TM, Hollands GJ, Hankins M, Aveyard P, (2013) Change in anxiety following successful and unsuccessful attempts at smoking cessation: cohort study. Br J Psychiatry 202: 62-67.
35. Mokdad AH, Marks JS, Stroup JS, Gerberding JL, (2004) Actual causes of death in the United States, 2000. JAMA 291: 1238-1245.
36. Olton D, Samuelson RJ, (1976) Rememberances of places passed: spatial memory in rats. J Exp Psychol Anim Behav Process 2: 97-116.
37. Parks J, Svendsen D, Singer P, Foti ME, (2006) Morbidity and mortaloty in people with serious mental illness. National Associatry of State Mental Health Program Directors: Alexandria, VA.
38. Prochaska JJ, Hall SM, Bero LA, (2008) Tobacco use among individuals with schizophrenia: what role has the tobacco industry played. Schizophr Bull 34: 555-567.
39. Pulay AJ, Stinson FS, Ruan WJ, Smith SM, Pickering RP, Dawson DA, Grant BF, (2010) The relationship of DSM-IV personality disorders to nicotine dependence-results from a national survey. Drug Alcohol Depend 108: 141-145.
40. Reitz C, den Heijer T, van Duijn C, Hofman A, Breteler MMB, (2007) Relation between smoking and risk of dementia and Alzheimer disease: the Rotterdam study. Neurology 69: 998-1005.
41. Slotkin TA, (2008) If nicotiine is a developmental neurotoxicant in animal studies, dare we recommend nicotine replacement therapy in pregnant women and adolescence? Neurotoxicol Teratol 30: 1-19.
42. Steinberg ML, Williams JM, Ziedonis DM, (2004) Financial implications of cigarette smoking among individuals with schizophrenia. Tob Control 13: 206.
43. Sudai E, Croitoru O, Shaldubina A, Abraham L, Gispan I, Flaumenhaft Y, Roth-Deri I, Kinor N, Aharoni S, Ben-Tzion M, Yadid G, (2011) High cocaine dosage decreases neurogenesis in the hippocampus and impairs working memory. Addict Biol 16: 251-260.
44. Teicher MH, Anderson CM, Polcari A, (2012) Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc Natl Acad Sci U S A 109: E563-E572.
45. Tseng KY, Chambers RA, Lipska BK, (2009) The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behav Brain Res 204: 295-305.
46. Tseng KY, Lewis BL, Lipska BK, O'Donnell P, (2007) Post-pubertal disruption of medial prefrontal cortical dopamine-glutamate interactions in a developmental animal model of schizophrenia. Biol Psychiatry 62: 730-738.
47. Volkow ND, (2009) Substance use disorders in schizophrenia-clinical implications of comorbidity. Schizophr Bull 35: 469-472.
48. Weinberger DR, (1999) Cell biology of the hippocampal formation in schizophrenia. Biol Psychiatry 45: 395-402.
49. Williams JM, Ziedonis DM, Abanyie F, Steinberg ML, Foulds J, Benowitz NL, (2005) Increased nicotine and cotinine levels in smokers with schizophrenia and schizoaffective disorder is not a metabolic effect. Schizophr Res 79: 323-335.
50. Zhang X, Stein EA, Hong LE, (2010) Smoking and schizophrenia independently and additively reduce white matter integrity between striatum and frontal cortex. Biol Psychiatry 68: 674-677.