Co-segregation of hyperactivity, active coping styles, and cognitive dysfunction in mice selectively bred for low levels of anxiety

Frontiers in Behavioral Neuroscience

Volumn , Issue AUG, 2013, Pages

  Yen, Yi Chun ^a   Anderzhanova, Elmira ^a   Bunck, Mirjam ^a   Schuller, Julia ^a   Landgraf, Rainer ^a   Wotjak, Carsten T ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

ADHD; Amphetamine; Hyperactivity; LAB; Selective breeding

Indexed keywords

AMPHETAMINE; HALOPERIDOL; LITHIUM;

ALLELE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; ATTENTION DEFICIT DISORDER; BEHAVIORAL TEST; BREEDING; COGNITIVE DEFECT; CONTROLLED STUDY; COPING BEHAVIOR; CROSS BREEDING; DISCRIMINANT ANALYSIS; ELEVATED PLUS MAZE; ENDOPHENOTYPE; EXPERIMENTAL TEST; EXPLORATORY BEHAVIOR; FEMALE; GENETIC SELECTION; HABITUATION; HEDONIA; HOLEBOARD TEST; HYPERACTIVITY; MALE; MANIA; MATHEMATICAL ANALYSIS; MAZE TEST; MOUSE; MOUSE STRAIN; NONHUMAN; OBJECT INTERACTION; OPEN FIELD TEST; PREPULSE INHIBITION; PSYCHOLOGIC TEST; SCHIZOPHRENIA; SOCIAL INTERACTION; STRAIN DIFFERENCE; VENN DIAGRAM;

EID: 84883393750     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00103     Document Type: Article

References (57)

1. Advokat, C. (2010). What are the cognitive effects of stimulant medications. Emphasis on adults with attention-deficit/hyperactivity disorder (ADHD). Neurosci. Biobehav. Rev. 34, 1256-1266. doi: 10.1016/j.neubiorev.2010.03.006
2. Advokat, C., and Scheithauer, M. (2013). Attention-deficit hyperactivity disorder (ADHD) stimulant medications as cognitive enhancers. Front. Neurosci. 7:82. doi: 10.3389/fnins.2013.00082
3. Andersen, S. L. (2005). Stimulants and the developing brain. Trends Pharmacol. Sci. 26, 237-243. doi: 10.1016/j.tips.2005.03.009
4. Andersen, S. L., Arvanitogiannis, A., Pliakas, A. M., LeBlanc, C., and Carlezon, W. A. Jr. (2002). Altered responsiveness to cocaine in rats exposed to methylphenidate during development. Nat. Neurosci. 5, 13-14. doi: 10.1038/nn777
5. Benus, R. F., Bohus, B., Koolhaas, J. M., and van Oortmerssen, G. A. (1991). Heritable variation for aggression as a reflection of individual coping strategies. Experientia 47, 1008-1019. doi: 10.1007/BF01923336
6. Bolhuis, J. E., Schouten, W. G., de Leeuw, J. A., Schrama, J. W., and Wiegant, V. M. (2004). Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behav. Brain Res. 152, 351-360. doi: 10.1016/j.bbr.2003.10.024
7. Britton, G. B. (2011). Cognitive and emotional behavioural changes associated with methylphenidate treatment: a review of preclinical studies. Int. J. Neuropsychopharmacol. doi: 10.1017/S1461145711000472. [Epub ahead of print].
8. Bunck, M., Czibere, L., Horvath, C., Graf, C., Frank, E., Kessler, M. S., et al. (2009). A hypomorphic vasopressin allele prevents anxiety-related behavior. PLoS ONE4:e5129. doi: 10.1371/journal.pone.0005129
9. Chudasama, Y., Nathwani, F., and Robbins, T. W. (2005). D-Amphetamine remediates attentional performance in rats with dorsal prefrontal lesions. Behav. Brain Res. 158, 97-107. doi: 10.1016/j.bbr.2004.08.011
10. Crawley, J. N., Chen, T., Puri, A., Washburn, R., Sullivan, T. L., Hill, J. M., et al. (2007). Social approach behaviors in oxytocin knockout mice: comparison of two independent lines tested in different laboratory environments. Neuropeptides 41, 145-163. doi: 10.1016/j.npep.2007.02.002
11. Cubillo, A., Halari, R., Ecker, C., Giampietro, V., Taylor, E., and Rubia, K. (2010). Reduced activation and inter-regional functional connectivity of fronto-striatal networks in adults with childhood attention-deficit hyperactivity disorder (ADHD) and persisting symptoms during tasks of motor inhibition and cognitive switching. J. Psychiatr. Res. 44, 629-639. doi: 10.1016/j.jpsychires.2009.11.016
12. Davids, E., Zhang, K., Kula, N. S., Tarazi, F. I., and Baldessarini, R. J. (2002). Effects of norepinephrine and serotonin transporter inhibitors on hyperactivity induced by neonatal 6-hydroxydopamine lesioning in rats. J. Pharmacol. Exp. Ther. 301, 1097-1102. doi: 10.1124/jpet.301.3.1097
13. Davis, B. A., Clinton, S. M., Akil, H., and Becker, J. B. (2008). The effects of novelty-seeking phenotypes and sex differences on acquisition of cocaine self-administration in selectively bred high-responder and low-Responder rats. Pharmacol. Biochem. Behav. 90, 331-338. doi: 10.1016/j.pbb.2008.03.008
14. Engelmann, M., Wotjak, C. T., and Landgraf, R. (1995). Social discrimination procedure: an alternative method to investigate juvenile recognition abilities in rats. Physiol. Behav. 58, 315-321. doi: 10.1016/0031-938400053-L
15. Flagel, S. B., Robinson, T. E., Clark, J. J., Clinton, S. M., Watson, S. J., Seeman, P., et al. (2010). An animal model of genetic vulnerability to behavioral disinhibition and responsiveness to reward-related cues: implications for addiction. Neuropsychopharmacology 35, 388-400. doi: 10.1038/npp.2009.142
16. Frey, B. N., Valvassori, S. S., Reus, G. Z., Martins, M. R., Petronilho, F. C., Bardini, K., et al. (2006). Effects of lithium and valproate on amphetamine-induced oxidative stress generation in an animal model of mania. J. Psychiatry Neurosci. 31, 326-332.
17. Gamo, N. J., and Arnsten, A. F. (2011). Molecular modulation of prefrontal cortex: rational development of treatments for psychiatric disorders. Behav. Neurosci. 125, 282-296. doi: 10.1037/a0023165
18. Godsil, B. P., Stefanacci, L., and Fanselow, M. S. (2005). Bright light suppresses hyperactivity induced by excitotoxic dorsal hippocampus lesions in the rat. Behav. Neurosci. 119, 1339-1352. doi: 10.1037/0735-7044.119.5.1339
19. Golub, Y., Mauch, C. P., Dahlhoff, M., and Wotjak, C. T. (2009). Consequences of extinction training on associative and non-associative fear in a mouse model of Posttraumatic Stress Disorder (PTSD). Behav. Brain Res. 205, 544-549. doi: 10.1016/j.bbr.2009.08.019
20. Gould, T. J., Keith, R. A., and Bhat, R. V. (2001). Differential sensitivity to lithium's reversal of amphetamine-induced open-field activity in two inbred strains of mice. Behav. Brain Res. 118, 95-105. doi: 10.1016/S0166-432800318-1
21. Greenhill, L. L. (1992). Pharmacologic treatment of attention deficit hyperactivity disorder. Psychiatr. Clin. North Am. 15, 1-27.
22. Grillon, C., Ameli, R., Charney, D. S., Krystal, J., and Braff, D. (1992). Startle gating deficits occur across prepulse intensities in schizophrenic patients. Biol. Psychiatry32, 939-943. doi: 10.1016/0006-322390183-Z
23. Hegerl, U., Himmerich, H., Engmann, B., and Hensch, T. (2010). Mania and attention-deficit/hyperactivity disorder: common symptomatology, common pathophysiology and common treatment. Curr. Opin. Psychiatry 23, 1-7. doi: 10.1097/YCO.0b013e328331f694
24. Irwin, M. R., Marder, S. R., Fuentenebro, F., and Yuwiler, A. (1987). L-5-hydroxytryptophan attenuates positive psychotic symptoms induced by D-amphetamine. Psychiatry Res. 22, 283-289. doi: 10.1016/0165-178190107-7
25. Jacob, W., Yassouridis, A., Marsicano, G., Monory, K., Lutz, B., and Wotjak, C. T. (2009). Endocannabinoids render exploratory behaviour largely independent of the test aversiveness: role of glutamatergic transmission. Genes Brain Behav. 8, 685-698. doi: 10.1111/j.1601-183X.2009.00512.x
26. Kerman, I. A., Clinton, S. M., Bedrosian, T. A., Abraham, A. D., Rosenthal, D. T., Akil, H., et al. (2011). High novelty-seeking predicts aggression and gene expression differences within defined serotonergic cell groups. Brain Res. 1419, 34-45. doi: 10.1016/j.brainres.2011.08.038
27. Kessler, M. S., Bosch, O. J., Bunck, M., Landgraf, R., and Neumann, I. D. (2010). Maternal care differs in mice bred for high vs. low trait anxiety: impact of brain vasopressin and cross-fostering. Soc. Neurosci. 6, 156-168. doi: 10.1080/17470919.2010.495567
28. Kleinknecht, K. R., Bedenk, B. T., Kaltwasser, S. F., Grunecker, B., Yen, Y. C., Czisch, M., et al. (2012). Hippocampus-dependent place learning enables spatial flexibility in C57BL6/N mice. Front. Behav. Neurosci. 6:87. doi: 10.3389/fnbeh.2012.00087
29. Krömer, S. A., Kessler, M. S., Milfay, D., Birg, I. N., Bunck, M., Czibere, L., et al. (2005). Identification of glyoxalase-I as a protein marker in a mouse model of extremes in trait anxiety. J. Neurosci. 25, 4375-4384. doi: 10.1523/JNEUROSCI.0115-05.2005
30. Landgraf, R., Kessler, M. S., Bunck, M., Murgatroyd, C., Spengler, D., Zimbelmann, M., et al. (2007). Candidate genes of anxiety-related behavior in HAB/LAB rats and mice: focus on vasopressin and glyoxalase-I. Neurosci. Biobehav. Rev. 31, 89-102. doi: 10.1016/j.neubiorev.2006.07.003
31. Logan, R. W., Robledo, R. F., Recla, J. M., Philip, V. M., Bubier, J. A., Jay, J. J., et al. (2013). High-precision genetic mapping of behavioral traits in the diversity outbred mouse population. Genes Brain Behav. 12, 424-437. doi: 10.1111/gbb.12029
32. Miro, X., Meier, S., Dreisow, M. L., Frank, J., Strohmaier, J., Breuer, R., et al. (2012). Studies in humans and mice implicate neurocan in the etiology of mania. Am. J. Psychiatry 169, 982-990. doi: 10.1176/appi.ajp.2012.11101585
33. Moy, S. S., Nadler, J. J., Perez, A., Barbaro, R. P., Johns, J. M., Magnuson, T. R., et al. (2004). Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 3, 287-302. doi: 10.1111/j.1601-1848.2004.00076.x
34. Nadler, J. J., Moy, S. S., Dold, G., Trang, D., Simmons, N., Perez, A., et al. (2004). Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav. 3, 303-314. doi: 10.1111/j.1601-183X.2004.00071.x
35. Nestler, E. J., and Hyman, S. E. (2010). Animal models of neuropsychiatric disorders. Nat. Neurosci. 13, 1161-1169. doi: 10.1038/nn.2647
36. Nevels, R. M., Dehon, E. E., Alexander, K., and Gontkovsky, S. T. (2010). Psychopharmacology of aggression in children and adolescents with primary neuropsychiatric disorders: a review of current and potentially promising treatment options. Exp. Clin. Psychopharmacol. 18, 184-201. doi: 10.1037/a0018059
37. National Institute of Mental Health (2008). Attention Deficit Hyperactivity Disorder (ADHD). (NIH Publication No. 12-3572). Washington, DC: National Institutes of Health.
38. Nyberg, J. M., Vekovischeva, O., and Sandnabba, N. K. (2003). Anxiety profiles of mice selectively bred for intermale aggression. Behav. Genet. 33, 503-511. doi: 10.1023/A:1025718531997
39. Ohl, F., Roedel, A., Storch, C., Holsboer, F., and Landgraf, R. (2002). Cognitive performance in rats differing in their inborn anxiety. Behav. Neurosci. 116, 464-471. doi: 10.1037/0735-7044.116.3.464
40. Pawlak, C. R., Ho, Y. J., and Schwarting, R. K. (2008). Animal models of human psychopathology based on individual differences in novelty-seeking and anxiety. Neurosci. Biobehav. Rev. 32, 1544-1568. doi: 10.1016/j.neubiorev.2008.06.007
41. Pearlson, G. D. (2000). Neurobiology of schizophrenia. Ann. Neurol. 48, 556-566.
42. Perry, W., Minassian, A., Paulus, M. P., Young, J. W., Kincaid, M. J., Ferguson, E. J., et al. (2009). A reverse-translational study of dysfunctional exploration in psychiatric disorders: from mice to men. Arch. Gen. Psychiatry 66, 1072-1080. doi: 10.1001/archgenpsychiatry.2009.58
43. Price, T., and Langen, T. (1992). Evolution of correlated characters. Trends Ecol. Evol. 7, 307-310. doi: 10.1016/0169-534790229-5
44. Richter, K., Wolf, G., and Engelmann, M. (2005). Social recognition memory requires two stages of protein synthesis in mice. Learn. Mem. 12, 407-413. doi: 10.1101/lm.97505
45. Sarantis, K., Antoniou, K., Matsokis, N., and Angelatou, F. (2012). Exposure to novel environment is characterized by an interaction of D1/NMDA receptors underlined by phosphorylation of the NMDA and AMPA receptor subunits and activation of ERK1/2 signaling, leading to epigenetic changes and gene expression in rat hippocampus. Neurochem. Int. 60, 55-67. doi: 10.1016/j.neuint.2011.10.018
46. Shaywitz, B. A., Klopper, J. H., and Gordon, J. W. (1978). Methylphenidate in 6-hydroxydopamine-treated developing rat pups. Effects on activity and maze performance. Arch. Neurol. 35, 463-469. doi: 10.1001/archneur.1978.00500310065014
47. Smit-Rigter, L. A., Wadman, W. J., and van Hooft, J. A. (2010). Impaired social behavior in 5-HT(3A) receptor knockout mice. Front. Behav. Neurosci. 4:169. doi: 10.3389/fnbeh.2010.00169
48. Solanto, M. V. (2002). Dopamine dysfunction in AD/HD: integrating clinical and basic neuroscience research. Behav. Brain Res. 130, 65-71. doi: 10.1016/S0166-432800431-4
49. Strekalova, T., Spanagel, R., Dolgov, O., and Bartsch, D. (2005). Stress-induced hyperlocomotion as a confounding factor in anxiety and depression models in mice. Behav. Pharmacol. 16, 171-180. doi: 10.1097/00008877-200505000-00006
50. Terzian, A. L., Drago, F., Wotjak, C. T., and Micale, V. (2011). The dopamine and cannabinoid interaction in the modulation of emotions and cognition: assessing the role of cannabinoid CB1 receptor in neurons expressing dopamine D1 receptors. Front. Behav. Neurosci. 5:49. doi: 10.3389/fnbeh.2011.00049
51. Thanos, P. K., Michaelides, M., Benveniste, H., Wang, G. J., and Volkow, N. D. (2007). Effects of chronic oral methylphenidate on cocaine self-administration and striatal dopamine D2 receptors in rodents. Pharmacol. Biochem. Behav. 87, 426-433. doi: 10.1016/j.pbb.2007.05.020
52. Veenema, A. H., Torner, L., Blume, A., Beiderbeck, D. I., and Neumann, I. D. (2007). Low inborn anxiety correlates with high intermale aggression: link to ACTH response and neuronal activation of the hypothalamic paraventricular nucleus. Horm. Behav. 51, 11-19. doi: 10.1016/j.yhbeh.2006.07.004
53. Wigger, A., Loerscher, P., Weissenbacher, P., Holsboer, F., and Landgraf, R. (2001). Cross-fostering and cross-breeding of HAB and LAB rats: a genetic rat model of anxiety. Behav. Genet. 31, 371-382. doi: 10.1023/A:1012222402346
54. Yamashita, M., Sakakibara, Y., Hall, F. S., Numachi, Y., Yoshida, S., Kobayashi, H., et al. (2013). Impaired cliff avoidance reaction in dopamine transporter knockout mice. Psychopharmacology (Berl.) 227, 741-749. doi: 10.1007/s00213-013-3009-9
55. Yen, Y. C., Mauch, C. P., Dahlhoff, M., Micale, V., Bunck, M., Sartori, S. B., et al. (2012). Increased levels of conditioned fear and avoidance behavior coincide with changes in phosphorylation of the protein kinase B (AKT) within the amygdala in a mouse model of extremes in trait anxiety. Neurobiol. Learn. Mem. 98, 56-65. doi: 10.1016/j.nlm.2012.04.009
56. Yilmazer-Hanke, D. M., Wigger, A., Linke, R., Landgraf, R., and Schwegler, H. (2004). Two Wistar rat lines selectively bred for anxiety-related behavior show opposite reactions in elevated plus maze and fear-sensitized acoustic startle tests. Behav. Genet. 34, 309-318. doi: 10.1023/B:BEGE.0000017874.40934.64
57. Zito, J. M., Safer, D. J., dos Reis, S., Gardner, J. F., Boles, M., and Lynch, F. (2000). Trends in the prescribing of psychotropic medications to preschoolers. JAMA 283, 1025-1030. doi: 10.1001/jama.283.8.1025