An investigation into "two hit" effects of BDNF deficiency and young-adult cannabinoid receptor stimulation on prepulse inhibition regulation and memory in mice

Frontiers in Behavioral Neuroscience

Volumn , Issue OCT, 2013, Pages

  Klug, Maren ^a,b   van den Buuse, Maarten ^a,c  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Brain derived neurotrophic factor; Cannabis; Memory; Mice; Prepulse inhibition; Schizophrenia

Indexed keywords

4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR; CANNABIS;

ADULT ANIMAL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; FEMALE; LEARNING; MALE; MAZE TEST; MEMORY DISORDER; MENTAL TASK; MOUSE; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PATHOPHYSIOLOGY; PREPULSE INHIBITION; PROTEIN DEPLETION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; RECOGNITION; REGULATORY MECHANISM; RISK FACTOR; SCHIZOPHRENIA; SENSORIMOTOR FUNCTION; SEX DIFFERENCE; SHORT TERM MEMORY; SPATIAL MEMORY; STARTLE REFLEX;

EID: 84886243956     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00149     Document Type: Article

References (62)

1. Angelucci, F., Brene, S., and Mathe, A. A. (2005). BDNF in schizophrenia, depression and corresponding animal models. Mol. Psychiatry 10, 345-352. doi: 10.1038/sj.mp.4001637
2. Angelucci, F., Ricci, V., Spalletta, G., Pomponi, M., Tonioni, F., Caltagirone, C., et al. (2008). Reduced serum concentrations of nerve growth factor, but not brain-derived neurotrophic factor, in chronic cannabis abusers. Eur. Neuropsychopharmacol. 18, 882-887. doi: 10.1016/j.euroneuro. 2008.07.008
3. Autry, A. E., and Monteggia, L. M. (2012). Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol. Rev. 64, 238-258. doi: 10.1124/pr.111.005108
4. Bath, K. G., Schilit, A., and Lee, F. S. (2013). Stress effects on BDNF expression: effects of age, sex, and form of stress. Neuroscience 239, 149-156. doi: 10.1016/j.neuro science.2013.01.074
5. Bayer, T. A., Falkai, P., and Maier, W. (1999). Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the "two hit hypothesis". J. Psychiatr. Res. 33, 543-548. doi: 10.1016/S0022-3956 (99)00039-4
6. Boucher, A. A., Hunt, G. E., Micheau, J., Huang, X., McGregor, I. S., Karl, T., et al. (2011). The schizophrenia susceptibility gene neuregulin 1 modulates tolerance to the effects of cannabinoids. Int. J. Neuropsychopharmacol. 14, 631-643. doi: 10.1017/S1461145710 00091X
7. Brzozka, M. M., Fischer, A., Falkai, P., and Havemann-Reinecke, U. (2011). Acute treatment with cannabinoid receptor agonist WIN55212.2 improves prepulse inhibition in psychosocially stressed mice. Behav. Brain Res. 218, 280-287. doi: 10.1016/j.bbr.2010. 11.003
8. Butovsky, E., Juknat, A., Goncharov, I., Elbaz, J., Eilam, R., Zangen, A., et al. (2005). In vivo up-regulation of brain-derived neurotrophic factor in specific brain areas by chronic exposure to Delta-tetrahydrocannabinol. J. Neurochem. 93, 802-811. doi: 10.1111/j.1471-4159.2005.03074.x
9. Chaperon, F., and Thiebot, M. H. (1999). Behavioral effects of cannabinoid agents in animals. Crit. Rev. Neurobiol. 13, 243-281.
10. Chavez, C., Hollaus, M., Scarr, E., Pavey, G., Gogos, A., and Van Den Buuse, M. (2010). The effect of estrogen on dopamine and serotonin receptor and transporter levels in the brain: an autoradiography study. Brain Res. 1321, 51-59. doi: 10.1016/j.brainres.2009.12.093
11. Chen, Z. Y., Jing, D., Bath, K. G., Ieraci, A., Khan, T., Siao, C. J., et al. (2006). Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314, 140-143. doi: 10.1126/science.1129663
12. Chourbaji, S., Hellweg, R., Brandis, D., Zorner, B., Zacher, C., Lang, U. E., et al. (2004). Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior. Brain Res. Mol. Brain Res. 121, 28-36. doi: 10.1016/j.molbrainres. 2003.11.002
13. Conrad, C. D., Grote, K. A., Hobbs, R. J., and Ferayorni, A. (2003). Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol. Learn. Mem. 79, 32-40. doi: 10.1016/ S1074-7427(02)00018-7
14. Corbille, A. G., Valjent, E., Marsicano, G., Ledent, C., Lutz, B., Herve, D., et al. (2007). Role of cannabi-noid type 1 receptors in locomo-tor activity and striatal signaling in response to psychostimulants. J. Neurosci. 27, 6937-6947. doi: 10.1523/JNEUROSCI.3936-06.2007
15. De Bitencourt, R. M., Pamplona, F. A., and Takahashi, R. N. (2013). A current overview of cannabinoids and glucocorticoids in facilitating extinction of aversive memories: potential extinction enhancers. Neuropharmacology 64, 389-395.doi: 10.1016/j.neuropharm.2012. 05.039
16. Decoster, J., Van Os, J., Kenis, G., Henquet, C., Peuskens, J., De Hert, M., et al. (2011). Age at onset of psychotic disorder: cannabis, BDNF Val66Met, and sex-specific models of gene-environment interaction. Am. J. Med. Genet. B Neuropsychiatr. Genet. 156B, 363-369. doi: 10.1002/ajmg.b.31174
17. Dellu, F., Contarino, A., Simon, H., Koob, G. F., and Gold, L. H. (2000). Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice. Neurobiol. Learn. Mem. 73, 31-48.doi: 10.1006/nlme.1999.3919
18. Dellu, F., Mayo, W., Cherkaoui, J., Le Moal, M., and Simon, H. (1992). A two-trial memory task with automated recording: study in young and aged rats. Brain Res. 588, 132-139. doi: 10.1016/0006-8993 (92)91352-F
19. Derkinderen, P., Valjent, E., Toutant, M., Corvol, J. C., Enslen, H., Ledent, C., et al. (2003). Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J. Neurosci. 23, 2371-2382.
20. D'souza, D. C., Pittman, B., Perry, E., and Simen, A. (2009). Preliminary evidence of cannabinoid effects on brain-derived neurotrophic factor (BDNF) levels in humans. Psychopharmacology (Berl.) 202, 569-578.doi: 10.1007/s00213-008-1333-2
21. Durany, N., and Thome, J. (2004). Neurotrophic factors and the patho-physiology of schizophrenic psychoses. Eur. Psychiatry 19, 326-337. doi: 10.1016/j.eurpsy.2004.06.020
22. Gururajan, A., Manning, E. E., Klug, M., and Van Den Buuse, M. (2012). Drugs of abuse and increased risk of psychosis development. Aust. N.Z. J. Psychiatry 46, 1120-1135. doi: 10.1177/0004867412455232
23. Hashimoto, T., Volk, D. W., Eggan, S. M., Mirnics, K., Pierri, J. N., Sun, Z., et al. (2003). Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J. Neurosci. 23, 6315-6326.
24. Henquet, C., Di Forti, M., Morrison, P., Kuepper, R., and Murray, R. M. (2008). Gene-environment interplay between cannabis and psychosis. Schizophr. Bull. 34, 1111-1121. doi: 10.1093/schbul/ sbn108
25. Hill, R. A., and Van Den Buuse, M. (2011). Sex-dependent and region-specific changes in TrkB signaling in BDNF heterozygous mice. Brain Res. 1384, 51-60. doi: 10.1016/j.brainres.2011.01.060
26. Hill, R. A., Wu, Y. W., Kwek, P., and Van Den Buuse, M. (2012). Modulatory effects of sex steroid hormones on brain-derived neurotrophic factor-tyrosine kinase B expression during adolescent development in C57Bl/6 mice. J. Neuroendocrinol. 24, 774-788. doi: 10.1111/j.1365-2826.2012.02277.x
27. Ibarguen-Vargas, Y., Surget, A., VOURC'H, P., Leman, S., Andres, C. R., Gardier, A. M., et al. (2009). Deficit in BDNF does not increase vulnerability to stress but dampens antidepressant-like effects in the unpredictable chronic mild stress. Behav. Brain Res. 202, 245-251. doi: 10.1016/j.bbr. 2009.03.040
28. Jockers-Scherübl, M. C., Danker-Hopfe, H., Mahlberg, R., Selig, F., Rentzsch, J., Schurer, F., et al. (2004). Brain-derived neurotrophic factor serum concentrations are increased in drug-naive schizophrenic patients with chronic cannabis abuse and multiple substance abuse. Neurosci. Lett. 371, 79-83. doi: 10.1016/j.neulet.2004. 08.045
29. Klug, M., Hill, R. A., Choy, K. H., Kyrios, M., Hannan, A. J., and Van Den Buuse, M. (2012). Long-term behavioral and NMDA receptor effects of young-adult corticosterone treatment in BDNF heterozygous mice. Neurobiol. Dis. 46, 722-731. doi: 10.1016/j.nbd.2012.03.015
30. Klug, M., and Van Den Buuse, M. (2012). Chronic cannabinoid treatment during young adulthood induces sex-specific behavioural deficits in maternally separated rats. Behav. Brain Res. 233, 305-313. doi: 10.1016/j.bbr.2012.05.019
31. Llorente-Berzal, A., Fuentes, S., Gagliano, H., Lopez-Gallardo, M., Armario, A., Viveros, M. P., et al. (2011). Sex-dependent effects of maternal deprivation and adolescent cannabinoid treatment on adult rat behaviour. Addict. Biol. 16, 624-637. doi: 10.1111/j.1369-1600.2011.00318.x
32. Lu, Y., Christian, K., and Lu, B. (2008). BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol. Learn. Mem. 89, 312-323. doi: 10.1016/j.nlm.2007.08.018
33. Macqueen, G. M., Ramakrishnan, K., Croll, S. D., Siuciak, J. A., Yu, G., Young, L. T., et al. (2001). Performance of heterozygous brain-derived neurotrophic factor knockout mice on behavioral analogues of anxiety, nociception, and depression. Behav. Neurosci. 115, 1145-1153. doi: 10.1037/0735-7044.115.5.1145
34. Malone, D. T., and Taylor, D. A. (2006). The effect of Delta9- tetrahydrocannabinol on sensorimotor gating in socially isolated rats. Behav. Brain Res. 166, 101-109. doi: 10.1016/j.bbr.2005. 07.009
35. Martin, R. S., Secchi, R. L., Sung, E., Lemaire, M., Bonhaus, D. W., Hedley, L. R., et al. (2003). Effects of cannabinoid receptor ligands on psychosis-relevant behavior models in the rat. Psychopharmacology (Berl.) 165, 128-135.
36. Maynard, T. M., Sikich, L., Lieberman, J. A., and Lamantia, A. S. (2001). Neural development, cell-cell signaling, and the "two-hit" hypothesis of schizophrenia. Schizophr. Bull. 27, 457-476. doi:10.1093/oxfordjournals.schbul.a006887
37. McGrath, J. J., Feron, F. P., Burne, T. H., Mackay-Sim, A., and Eyles, D. W. (2003). The neurodevelop-mental hypothesis of schizophrenia: a review of recent developments. Ann. Med. 35, 86-93. doi: 10.1080/07853890310010005
38. McGregor, I. S., Issakidis, C. N., and Prior, G. (1996). Aversive effects of the synthetic cannabinoid CP 55,940 in rats. Pharmacol. Biochem. Behav. 53, 657-664. doi: 10.1016/0091-3057(95)02066-7
39. Monteggia, L. M., Barrot, M., Powell, C. M., Berton, O., Galanis, V., Gemelli, T., et al. (2004). Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc. Natl. Acad. Sci. U.S.A. 101, 10827-10832. doi: 10.1073/pnas.0402141101
40. Montkowski, A., and Holsboer, F. (1997). Intact spatial learning and memory in transgenic mice with reduced BDNF. Neuroreport 8, 779-782. doi: 10.1097/00001756-199702100-00040
41. Nagai, H., Egashira, N., Sano, K., Ogata, A., Mizuki, A., Mishima, K., et al. (2006). Antipsychotics improve Delta9-tetrahydrocannabinol-induced impairment of the prepulse inhibition of the startle reflex in mice. Pharmacol. Biochem. Behav. 84, 330-336. doi: 10.1016/j.pbb.2006.05.018
42. Naumenko, V. S., Bazovkina, D. V., Morozova, M. V., and Popova, N. K. (2013). Effects of brain-derived and glial cell line-derived neurotrophic factors on startle response and disrupted prepulse inhibition in mice of DBA/2J inbred strain. Neurosci. Lett. 550, 115-118. doi: 10.1016/j.neulet. 2013.06.056
43. Nieuwenhuis, S., Forstmann, B. U., and Wagenmakers, E. J. (2011). Erroneous analyses of interactions in neuroscience: a problem of significance. Nat. Neurosci. 14, 1105-1107. doi: 10.1038/nn.2886
44. Panlilio, L. V., Ferre, S., Yasar, S., Thorndike, E. B., Schindler, C. W., and Goldberg, S. R. (2012). Combined effects of THC and caf feine on working memory in rats. Br. J. Pharmacol. 165, 2529-2538. doi: 10.1111/j.1476-5381.2011.01554.x
45. Papaleo, F., Silverman, J. L., Aney, J., Tian, Q., Barkan, C. L., Chadman, K. K., et al. (2011). Working memory deficits, increased anxiety-like traits, and seizure susceptibility in BDNF overexpressing mice. Learn. Mem. 18, 534-544. doi: 10.1101/lm.2213711
46. Pavey, G. M., Copolov, D. L., and Dean, B. (2002). High-resolution phosphor imaging: validation for use with human brain tissue sections to determine the affinity and density of radioligand binding. J. Neurosci. Meth. 116, 157-163. doi: 10.1016/S0165-0270(02)00036-5
47. Phillips, P., and Johnson, S. (2001). How does drug and alcohol misuse develop among people with psychotic illness? A literature review. Soc. Psychiatry Psychiatr. Epidemiol. 36, 269-276. doi: 10.1007/s001270 170044
48. Piontkewitz, Y., Assaf, Y., and Weiner, I. (2009). Clozapine administration in adolescence prevents postpubertal emergence of brain structural pathology in an animal model of schizophrenia. Biol. Psychiatry 66, 1038-1046. doi: 10.1016/j.biopsych.2009.07.005
49. Roncada, P., Bortolato, M., Frau, R., Saba, P., Flore, G., Soggiu, A., et al. (2009). Gating deficits in isolation-reared rats are correlated with alterations in protein expression in nucleus accumbens. J. Neurochem. 108, 611-620. doi: 10.1111/j.1471-4159.2008.05806.x
50. Saylor, A. J., and McGinty, J. F. (2008). Amphetamine-induced locomotion and gene expression are altered in BDNF heterozygous mice. Genes Brain Behav. 7, 906-914. doi: 10.1111/j.1601-183X.2008.00430.x
51. Schneider, M. (2008). Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict. Biol. 13, 253-263. doi: 10.1111/j.1369-1600.2008.00110.x
52. Schofield, D., Tennant, C., Nash, L., Degenhardt, L., Cornish, A., Hobbs, C., et al. (2006). Reasons for cannabis use in psychosis. Aust. N.Z. J. Psychiatry 40, 570-574. doi: 10.1080/j.1440-1614.2006.01840.x
53. Seoane, A., Tinsley, C. J., and Brown, M. W. (2011). Interfering with perirhinal brain-derived neu-rotrophic factor expression impairs recognition memory in rats. Hippocampus 21, 121-126. doi: 10.1002/hipo.20763
54. Shilling, P. D., Saint Marie, R. L., Shoemaker, J. M., and Swerdlow, N. R. (2008). Strain differences in the gating-disruptive effects of apomor-phine: relationship to gene expression in nucleus accumbens signaling pathways. Biol. Psychiatry 63, 748-758. doi: 10.1016/j.biopsych. 2007.10.015
55. Spano, M. S., Fadda, P., Frau, R., Fattore, L., and Fratta, W. (2010). Cannabinoid self- administration attenuates PCP-induced schizophrenia like symptoms in adult rats. Eur. Neuropsychopharmacol. 20, 25-36. doi: 10.1016/j.euroneuro.2009. 09.004
56. Stanley-Cary, C. C., Harris, C., and Martin-Iverson, M. T. (2002). Differing effects of the cannabinoid agonist, CP 55,940, in an alcohol or Tween 80 solvent, on prepulse inhibition of the acoustic startle reflex in the rat. Behav. Pharmacol. 13, 15-28. doi: 10.1097/00008877-200202000-00002
57. Swerdlow, N. R., Braff, D. L., and Geyer, M. A. (2000). Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav. Pharmacol. 11, 185-204. doi: 10.1097/00008877-200006000-00002
58. Van Os, J., Bak, M., Hanssen, M., Bijl, R. V., De Graaf, R., and Verdoux, H. (2002). Cannabis use and psychosis: a longitudinal population-based study. Am. J. Epidemiol. 156, 319-327. doi: 10.1093/aje/ kwf043
59. Weickert, C. S., Hyde, T. M., Lipska, B. K., Herman, M. M., Weinberger, D. R., and Kleinman, J. E. (2003). Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 8, 592-610. doi: 10.1038/sj.mp.4001308
60. Winters, B. D., Kruger, J. M., Huang, X., Gallaher, Z. R., Ishikawa, M., Czaja, K., et al. (2012). Cannabinoid receptor 1-expressing neurons in the nucleus accumbens. Proc. Natl Acad. Sci. U.S.A. 109, E2717-E2725. doi: 10.1073/pnas.1206303109
61. Wright, M. J. Jr., Vandewater, S. A., Parsons, L. H., and Taffe, M. A. (2013). A9 Tetrahydrocannabinol impairs reversal learning but not extra-dimensional shifts in rhesus macaques. Neuroscience 235, 51-58. doi: 10.1016/j.neuroscience. 2013.01.018
62. Zamberletti, E., Prini, P., Speziali, S., Gabaglio, M., Solinas, M., Parolaro, D., et al. (2012). Gender-dependent behavioral and biochemical effects of adolescent delta-9-tetrahydrocannabinol in adult maternally deprived rats. Neuroscience 204, 245-257. doi: 10. 1016/j.neuroscience.2011.11.038