Hippocampal neurogenesis protects against cocaine-primed relapse

Addiction Biology

Volumn 19, Issue 4, 2014, Pages 562-574

  Deschaux, Olivier ^a,b   Vendruscolo, Leandro F ^b   Schlosburg, Joel E ^b   Diaz Aguilar, Luis ^b   Yuan, Clara J ^c   Sobieraj, Jeffery C ^b   George, Olivier ^b   Koob, George F ^b,c   Mandyam, Chitra D ^b,c  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Activated caspase3; BrdU; dentate gyrus; Ki 67; low frequency stimulation; self administration

Indexed keywords

BROXURIDINE; CASPASE 3; COCAINE; KI 67 ANTIGEN; DOPAMINE UPTAKE INHIBITOR;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; COCAINE SEEKING BEHAVIOR; CONTROLLED STUDY; DENTATE GYRUS; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; ELECTROSTIMULATION; EXTINCTION INDUCED INHIBITION OF COCAINE SEEKING; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HYPOTHESIS; LOW FREQUENCY STIMULATION; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; RELAPSE; ANALYSIS OF VARIANCE; ANIMAL; ASSOCIATION; COCAINE-RELATED DISORDERS; DISEASE MODEL; DRUG EFFECTS; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; RECURRENT DISEASE; REINFORCEMENT; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CASPASE 3; COCAINE; COCAINE-RELATED DISORDERS; CUES; DENTATE GYRUS; DISEASE MODELS, ANIMAL; DOPAMINE UPTAKE INHIBITORS; DRUG-SEEKING BEHAVIOR; ELECTRIC STIMULATION; EXTINCTION, PSYCHOLOGICAL; HIPPOCAMPUS; MALE; NEUROGENESIS; NEURONS; RATS; RATS, WISTAR; RECURRENCE; SELF ADMINISTRATION;

EID: 84904256383     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12019     Document Type: Article

References (79)

1. Abraham WC, (1996) Induction of heterosynaptic and homosynaptic LTD in hippocampal sub-regions in vivo. J Physiol Paris 90: 305-306. (Pubitemid 27113365)
2. Abrous DN, Koehl M, Le Moal M, (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85: 523-569. (Pubitemid 40404636)
3. Aimone JB, Deng W, Gage FH, (2011) Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70: 589-596.
4. Aimone JB, Wiles J, Gage FH, (2006) Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9: 723-727.
5. Andersen ML, Perry JC, Bignotto M, Perez-Mendes P, Cinini SM, Mello LE, Tufik S, (2007) Influence of chronic cocaine treatment and sleep deprivation on sexual behavior and neurogenesis of the male rat. Prog Neuropsychopharmacol Biol Psychiatry 31: 1224-1229. (Pubitemid 47081307)
6. Atkins AL, Mashhoon Y, Kantak KM, (2008) Hippocampal regulation of contextual cue-induced reinstatement of cocaine-seeking behavior. Pharmacol Biochem Behav 90: 481-491.
7. Bashir ZI, Collingridge GL, (1994) An investigation of depotentiation of long-term potentiation in the CA1 region of the hippocampus. Exp Brain Res 100: 437-443. (Pubitemid 24281992)
8. Bast T, (2007) Toward an integrative perspective on hippocampal function: from the rapid encoding of experience to adaptive behavior. Rev Neurosci 18: 253-281.
9. 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.
10. Black YD, Green-Jordan K, Eichenbaum HB, Kantak KM, (2004) Hippocampal memory system function and the regulation of cocaine self-administration behavior in rats. Behav Brain Res 151: 225-238. (Pubitemid 38501446)
11. Bliss TV, Collingridge GL, (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39. (Pubitemid 23020772)
12. Brady AM, McCallum SE, Glick SD, O'Donnell P, (2008) Enhanced methamphetamine self-administration in a neurodevelopmental rat model of schizophrenia. Psychopharmacology (Berl) 200: 205-215.
13. Bruchey AK, Shumake J, Gonzalez-Lima F, (2007) Network model of fear extinction and renewal functional pathways. Neuroscience 145: 423-437. (Pubitemid 46350816)
14. Burke KA, Franz TM, Gugsa N, Schoenbaum G, (2006) Prior cocaine exposure disrupts extinction of fear conditioning. Learn Mem 13: 416-421. (Pubitemid 44157465)
15. Cameron HA, McKay RD, (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435: 406-417. (Pubitemid 32574293)
16. 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. (Pubitemid 35447626)
17. Chun SK, Sun W, Jung MW, (2009) LTD induction suppresses LTP-induced hippocampal adult neurogenesis. Neuroreport 20: 1279-1283.
18. Chun SK, Sun W, Park JJ, Jung MW, (2006) Enhanced proliferation of progenitor cells following long-term potentiation induction in the rat dentate gyrus. Neurobiol Learn Mem 86: 322-329. (Pubitemid 44436977)
19. Churchwell JC, Morris AM, Musso ND, Kesner RP, (2010) Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory. Neurobiol Learn Mem 93: 415-421.
20. Clark PJ, Bhattacharya TK, Miller DS, Kohman RA, Deyoung EK, Rhodes JS, (2012) New neurons generated from running are broadly recruited into neuronal activation associated with three different hippocampus-involved tasks. Hippocampus 22: 1860-1867.
21. Czeh B, Muller-Keuker JI, Rygula R, Abumaria N, Hiemke C, Domenici E, Fuchs E, (2007) Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment. Neuropsychopharmacology 32: 1490-1503. (Pubitemid 46920152)
22. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA, (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460: 563-572. (Pubitemid 36528662)
23. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC, (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42: 535-552. (Pubitemid 38639875)
24. del Olmo N, Miguens M, Higuera-Matas A, Torres I, Garcia-Lecumberri C, Solis JM, Ambrosio E, (2006) Enhancement of hippocampal long-term potentiation induced by cocaine self-administration is maintained during the extinction of this behavior. Brain Res 1116: 120-126. (Pubitemid 44485002)
25. Derrick BE, York AD, Martinez JL, Jr, (2000) Increased granule cell neurogenesis in the adult dentate gyrus following mossy fiber stimulation sufficient to induce long-term potentiation. Brain Res 857: 300-307. (Pubitemid 30107820)
26. Deschaux O, Motanis H, Spennato G, Moreau JL, Garcia R, (2011) Re-emergence of extinguished auditory-cued conditioned fear following a sub-conditioning procedure: effects of hippocampal and prefrontal tetanic stimulations. Neurobiol Learn Mem 95: 510-518.
27. Deschaux O, Thevenet A, Spennato G, Arnaud C, Moreau JL, Garcia R, (2010) Low-frequency stimulation of the hippocampus following fear extinction impairs both restoration of rapid eye movement sleep and retrieval of extinction memory. Neuroscience 170: 92-98.
28. Dominguez-Escriba L, Hernandez-Rabaza V, Soriano-Navarro M, Barcia JA, Romero FJ, Garcia-Verdugo JM, Canales JJ, (2006) Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus. Eur J Neurosci 24: 586-594. (Pubitemid 44100350)
29. Dong Z, Cao J, Xu L, (2007) Opiate withdrawal modifies synaptic plasticity in subicular-nucleus accumbens pathway in vivo. Neuroscience 144: 845-854. (Pubitemid 46013986)
30. Dudek SM, Bear MF, (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 89: 4363-4367.
31. Eisch AJ, Barrot M, Schad CA, Self DW, Nestler EJ, (2000) Opiates inhibit neurogenesis in the adult rat hippocampus. Proc Natl Acad Sci U S A 97: 7579-7584. (Pubitemid 30431506)
32. Farinelli M, Deschaux O, Hugues S, Thevenet A, Garcia R, (2006) Hippocampal train stimulation modulates recallof fear extinction independently of prefrontalcortex synaptic plasticity and lesions. Learn Mem 13: 329-334. (Pubitemid 43830679)
33. Farmer J, Zhao X, van Praag H, Wodtke K, Gage FH, Christie BR, (2004) Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 124: 71-79. (Pubitemid 38186618)
34. Feng R, Rampon C, Tang YP, Shrom D, Jin J, Kyin M, Sopher B, Miller MW, Ware CB, Martin GM, Kim SH, Langdon RB, Sisodia SS, Tsien JZ, (2001) Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 32: 911-926. (Pubitemid 34024850)
35. Fuchs RA, Evans KA, Ledford CC, Parker MP, Case JM, Mehta RH, See RE, (2005) The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology 30: 296-309. (Pubitemid 40129481)
36. Garcia R, Spennato G, Nilsson-Todd L, Moreau JL, Deschaux O, (2008) Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats. Neurobiol Learn Mem 89: 560-566. (Pubitemid 351492569)
37. Garcia-Fuster MJ, Flagel SB, Mahmood ST, Mayo LM, Thompson RC, Watson SJ, Akil H, (2011) Decreased proliferation of adult hippocampal stem cells during cocaine withdrawal: possible role of the cell fate regulator FADD. Neuropsychopharmacology 36: 2303-2317.
38. Garcia-Fuster MJ, Perez JA, Clinton SM, Watson SJ, Akil H, (2010) Impact of cocaine on adult hippocampal neurogenesis in an animal model of differential propensity to drug abuse. Eur J Neurosci 31: 79-89.
39. Guo L, Zhou H, Wang R, Xu J, Zhou W, Zhang F, Tang S, Liu H, Jiang J, (2012) DBS of nucleus accumbens on heroin seeking behaviors in self-administering rats. Drug Alcohol Depend (in press)
40. Heynen AJ, Abraham WC, Bear MF, (1996) Bidirectional modification of CA1 synapses in the adult hippocampus in vivo. Nature 381: 163-166. (Pubitemid 26137965)
41. Huang CC, Hsu KS, (2001) Progress in understanding the factors regulating reversibility of long-term potentiation. Rev Neurosci 12: 51-68.
42. Hugues S, Chessel A, Lena I, Marsault R, Garcia R, (2006) Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation. Synapse 60: 280-287. (Pubitemid 44134348)
43. Hugues S, Deschaux O, Garcia R, (2004) Postextinction infusion of a mitogen-activated protein kinase inhibitor into the medial prefrontal cortex impairs memory of the extinction of conditioned fear. Learn Mem 11: 540-543. (Pubitemid 39299701)
44. Hugues S, Garcia R, (2007) Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory. Learn Mem 14: 520-524. (Pubitemid 47347431)
45. Kalivas PW, McFarland K, (2003) Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berl) 168: 44-56. (Pubitemid 36851162)
46. Kim WR, Christian K, Ming GL, Song H, (2011) Time-dependent involvement of adult-born dentate granule cells in behavior. Behav Brain Res 227: 470-479.
47. Lacefield CO, Itskov V, Reardon T, Hen R, Gordon JA, (2012) Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 22: 106-116.
48. Larson EB, Graham DL, Arzaga RR, Buzin N, Webb J, Green TA, Bass CE, Neve RL, Terwilliger EF, Nestler EJ, Self DW, (2011) Overexpression of CREB in the nucleus accumbens shell increases cocaine reinforcement in self-administering rats. J Neurosci 31: 16447-16457.
49. Lasseter HC, Xie X, Ramirez DR, Fuchs RA, (2010) Sub-region specific contribution of the ventral hippocampus to drug context-induced reinstatement of cocaine-seeking behavior in rats. Neuroscience 171: 830-839.
50. Lloyd SA, Balest ZR, Corotto FS, Smeyne RJ, (2010) Cocaine selectively increases proliferation in the adult murine hippocampus. Neurosci Lett 485: 112-116.
51. Mandyam CD, Koob GF, (2012) The addicted brain craves new neurons: putative role for adult-born progenitors in promoting recovery. Trends Neurosci 35: 250-260.
52. Maren S, (2011) Seeking a spotless mind: extinction, deconsolidation, and erasure of fear memory. Neuron 70: 830-845.
53. Maren S, Fanselow MS, (1995) Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J Neurosci 15: 7548-7564.
54. Mu Y, Zhao C, Gage FH, (2011) Dopaminergic modulation of cortical inputs during maturation of adult-born dentate granule cells. J Neurosci 31: 4113-4123.
55. Mustroph ML, Stobaugh DJ, Miller DS, DeYoung EK, Rhodes JS, (2011) Wheel running can accelerate or delay extinction of conditioned place preference for cocaine in male C57BL/6J mice, depending on timing of wheel access. Eur J Neurosci 34: 1161-1169.
56. Neisewander JL, Baker DA, Fuchs RA, Tran-Nguyen LT, Palmer A, Marshall JF, (2000) Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J Neurosci 20: 798-805. (Pubitemid 30225582)
57. Noonan MA, Bulin SE, Fuller DC, Eisch AJ, (2010) Reduction of adult hippocampal neurogenesis confers vulnerability in an animal model of cocaine addiction. J Neurosci 30: 304-315.
58. Noonan MA, Choi KH, Self DW, Eisch AJ, (2008) Withdrawal from cocaine self-administration normalizes deficits in proliferation and enhances maturity of adult-generated hippocampal neurons. J Neurosci 28: 2516-2526. (Pubitemid 351348201)
59. Paxinos G, Watson C, (1997) The Rat Brain in Stereotaxic Coordinates, 3rd edn. San Diego, CA: Academic Press.
60. Peters J, Kalivas PW, Quirk GJ, (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16: 279-288.
61. Quirk GJ, Mueller D, (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33: 56-72. (Pubitemid 350191313)
62. Recinto P, Samant AR, Chavez G, Kim A, Yuan CJ, Soleiman M, Grant Y, Edwards S, Wee S, Koob GF, George O, Mandyam CD, (2011) Levels of neural progenitors in the hippocampus predicts memory impairment and relapse to drug seeking as a function of excessive methamphetamine self-administration. Neuropsychopharmacology 37: 1275-1287.
63. Rogers JL, See RE, (2007) Selective inactivation of the ventral hippocampus attenuates cue-induced and cocaine-primed reinstatement of drug-seeking in rats. Neurobiol Learn Mem 87: 688-692. (Pubitemid 46483135)
64. Santini E, Muller RU, Quirk GJ, (2001) Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. J Neurosci 21: 9009-9017. (Pubitemid 33054862)
65. Schmidt-Hieber C, Jonas P, Bischofberger J, (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429: 184-187. (Pubitemid 38656194)
66. Smith DA, Browning M, Dunwiddie TV, (1993) Cocaine inhibits hippocampal long-term potentiation. Brain Res 608: 259-265. (Pubitemid 23111944)
67. Snyder JS, Kee N, Wojtowicz JM, (2001) Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85: 2423-2431. (Pubitemid 32525520)
68. Song J, Christian K, Ming GL, Song H, (2012) Modification of hippocampal circuitry by adult neurogenesis. Dev Neurobiol 72: 1032-1043.
69. Staubli U, Chun D, (1996) Factors regulating the reversibility of long-term potentiation. J Neurosci 16: 853-860. (Pubitemid 26028841)
70. 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.
71. Sun W, Rebec GV, (2003) Lidocaine inactivation of ventral subiculum attenuates cocaine-seeking behavior in rats. J Neurosci 23: 10258-10264. (Pubitemid 37444602)
72. Sutton MA, Schmidt EF, Choi KH, Schad CA, Whisler K, Simmons D, Karanian DA, Monteggia LM, Neve RL, Self DW, (2003) Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour. Nature 421: 70-75. (Pubitemid 36077086)
73. Thompson AM, Swant J, Gosnell BA, Wagner JJ, (2004) Modulation of long-term potentiation in the rat hippocampus following cocaine self-administration. Neuroscience 127: 177-185. (Pubitemid 38829163)
74. Urrea C, Castellanos DA, Sagen J, Tsoulfas P, Bramlett HM, Dietrich WD, (2007) Widespread cellular proliferation and focal neurogenesis after traumatic brain injury in the rat. Restor Neurol Neurosci 25: 65-76. (Pubitemid 46631014)
75. van Praag H, Christie BR, Sejnowski TJ, Gage FH, (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96: 13427-13431.
76. Vendruscolo LF, Schlosburg JE, Misra KK, Chen SA, Greenwell TN, Koob GF, (2011) Escalation patterns of varying periods of heroin access. Pharmacol Biochem Behav 98: 570-574.
77. Vorel SR, Liu X, Hayes RJ, Spector JA, Gardner EL, (2001) Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292: 1175-1178. (Pubitemid 32440941)
78. Wang HY, Crupi D, Liu J, Stucky A, Cruciata G, Di Rocco A, Friedman E, Quartarone A, Ghilardi MF, (2011) Repetitive transcranial magnetic stimulation enhances BDNF-TrkB signaling in both brain and lymphocyte. J Neurosci 31: 11044-11054.
79. Yamaguchi M, Suzuki T, Seki T, Namba T, Juan R, Arai H, Hori T, Asada T, (2004) Repetitive cocaine administration decreases neurogenesis in adult rat hippocampus. Ann N Y Acad Sci 1025: 351-362. (Pubitemid 39643881)