Testing the cumulative stress and mismatch hypotheses of psychopathology in a rat model of early-life adversity

Physiology and Behavior

Volumn 106, Issue 5, 2012, Pages 707-721

  Daskalakis, Nikolaos P ^a   Oitzl, Melly S ^a   Schächinger, Hartmut ^b   Champagne, Danielle L ^c,d   Ronald de Kloet, E ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF TRIER   (Germany)

^c LEIDEN UNIVERSITY   (Netherlands)

^d RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Cumulative stress hypothesis; Gnawing; Isolation rearing; Maternal care; Maternal separation; Mismatch hypothesis; Prepulse inhibition; Psychosis; Schizophrenia; Stress

Indexed keywords

APOMORPHINE; CORTICOSTERONE;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; EARLY LIFE STRESS; FEMALE; GNAWING; GROOMING; LATER LIFE STRESS; LICKING; LIFE STRESS; MALE; MATERNAL CARE; MATERNAL DEPRIVATION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; PSYCHOSIS; PUP (RODENT); RAT; SOCIAL ISOLATION; STARTLE REFLEX; STIMULUS RESPONSE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; APOMORPHINE; BEHAVIOR, ANIMAL; BODY WEIGHT; CORTICOSTERONE; DISEASE MODELS, ANIMAL; DOPAMINE AGONISTS; EXPLORATORY BEHAVIOR; EYE; INHIBITION (PSYCHOLOGY); PSYCHOPATHOLOGY; RATS; RATS, WISTAR; SENSORY GATING; SOCIAL ISOLATION; STARTLE REACTION; STRESS, PSYCHOLOGICAL; WEANING;

EID: 84862503178     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2012.01.015     Document Type: Article

References (63)

1. van Os J., Kenis G., Rutten B.P. The environment and schizophrenia. Nature 2010, 468:203-212.
2. Brown A.S. The environment and susceptibility to schizophrenia. Prog Neurobiol 2011, 93:23-58.
3. Heins M., Simons C., Lataster T., Pfeifer S., Versmissen D., Lardinois M., et al. Childhood trauma and psychosis: A case-control and case-sibling comparison across different levels of genetic liability, psychopathology, and type of trauma. Am J Psychiatry 2011, 168:1286-1294.
4. Champagne D.L., Ronald de Kloet E., Joels M. Fundamental aspects of the impact of glucocorticoids on the (immature) brain. Semin Fetal Neonatal Med 2009, 14:136-142.
5. Pryce C.R., Ruedi-Bettschen D., Dettling A.C., Weston A., Russig H., Ferger B., et al. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci Biobehav Rev 2005, 29:649-674.
6. Lehmann J., Feldon J. Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?. Rev Neurosci 2000, 11:383-408.
7. Schmidt M.V. Molecular mechanisms of early life stress-lessons from mouse models. Neurosci Biobehav Rev 2010, 34:845-852.
8. Schmidt M.V., Wang X.D., Meijer O.C. Early life stress paradigms in rodents: potential animal models of depression?. Psychopharmacology 2011, 214:131-140.
9. McEwen B.S. Protective and damaging effects of stress mediators. N Engl J Med 1998, 338:171-179.
10. Taylor S.E. Mechanisms linking early life stress to adult health outcomes. Proc Natl Acad Sci USA 2010, 107:8507-8512.
11. Champagne D.L., Bagot R.C., van Hasselt F., Ramakers G., Meaney M.J., de Kloet E.R., et al. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci 2008, 28:6037-6045.
12. Schmidt M.V. Animal models for depression and the mismatch hypothesis of disease. Psychoneuroendocrinology 2011, 36:330-338.
13. Ellenbroek B.A., Cools A.R. Early maternal deprivation and prepulse inhibition: the role of the postdeprivation environment. Pharmacol Biochem Behav 2002, 73:177-184.
14. Choy K.H., de Visser Y., Nichols N.R., van den Buuse M. Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus 2008, 18:655-667.
15. Choy K.H., de Visser Y.P., van den Buuse M. The effect of 'two hit' neonatal and young-adult stress on dopaminergic modulation of prepulse inhibition and dopamine receptor density. Br J Pharmacol 2009, 156:388-396.
16. Choy K.H., van den Buuse M. Attenuated disruption of prepulse inhibition by dopaminergic stimulation after maternal deprivation and adolescent corticosterone treatment in rats. Eur Neuropsychopharmacol 2008, 18:1-13.
17. Gluckman P.D., Hanson M.A., Buklijas T., Low F.M., Beedle A.S. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol 2009, 5:401-408.
18. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662. [New York, N.Y.].
19. Liu D., Diorio J., Day J.C., Francis D.D., Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 2000, 3:799-806.
20. Zhang T.Y., Chretien P., Meaney M.J., Gratton A. Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. J Neurosci 2005, 25:1493-1502.
21. Richter S., Schulz A., Zech C.M., Oitzl M.S., Daskalakis N.P., Blumenthal T.D., et al. Cortisol rapidly disrupts prepulse inhibition in healthy men. Psychoneuroendocrinology 2011, 36:109-114.
22. Walker E., Mittal V., Tessner K. Stress and the hypothalamic pituitary adrenal axis in the developmental course of schizophrenia. Annu Rev Clin Psychol 2008, 4:189-216.
23. Varty G.B., Geyer M.A. Effects of isolation rearing on startle reactivity, habituation, and prepulse inhibition in male Lewis, Sprague-Dawley, and Fischer F344 rats. Behav Neurosci 1998, 112:1450-1457.
24. Varty G.B., Marsden C.A., Higgins G.A. Reduced synaptophysin immunoreactivity in the dentate gyrus of prepulse inhibition-impaired isolation-reared rats. Brain Res 1999, 824:197-203.
25. Varty G.B., Braff D.L., Geyer M.A. Is there a critical developmental 'window' for isolation rearing-induced changes in prepulse inhibition of the acoustic startle response?. Behav Brain Res 1999, 100:177-183.
26. Varty G.B., Paulus M.P., Braff D.L., Geyer M.A. Environmental enrichment and isolation rearing in the rat: effects on locomotor behavior and startle response plasticity. Biol Psychiatry 2000, 47:864-873.
27. Daskalakis N.P., Claessens S.E., Laboyrie J.J., Enthoven L., Oitzl M.S., Champagne D.L., et al. The newborn rat's stress system readily habituates to repeated and prolonged maternal separation, while continuing to respond to stressors in context dependent fashion. Horm Behav 2011, 60:165-176.
28. Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003, 79:359-371.
29. Myers M.M., Brunelli S.A., Squire J.M., Shindeldecker R.D., Hofer M.A. Maternal behavior of SHR rats and its relationship to offspring blood pressures. Dev Psychobiol 1989, 22:29-53.
30. Garner J.P. Stereotypies and other abnormal repetitive behaviors: potential impact on validity, reliability, and replicability of scientific outcomes. ILAR J 2005, 46:106-117.
31. Ljungberg T., Ungerstedt U. A method for simultaneous recording of eight behavioral parameters related to monoamine neurotransmission. Pharmacol Biochem Behav 1978, 8:483-489.
32. Lazar N.L., Neufeld R.W., Cain D.P. Contribution of nonprimate animal models in understanding the etiology of schizophrenia. J Psychiatry Neurosci 2011, 36:100054.
33. Cools A.R., Brachten R., Heeren D., Willemen A., Ellenbroek B. Search after neurobiological profile of individual-specific features of Wistar rats. Brain Res Bull 1990, 24:49-69.
34. Ellenbroek B.A., Sluyter F., Cools A.R. The role of genetic and early environmental factors in determining apomorphine susceptibility. Psychopharmacology 2000, 148:124-131.
35. Daskalakis, N. P., Meelis, W., Fung, W. L. J., McNeilly, J., de Jong, I. E. M., McNeilly, A. S., et al., in preparation. Stress hyper-reactivity and schizophrenia-like endophenotype co-precipitate following early-life adversity and post-weaning social isolation experiences of genetically susceptible rats.
36. Ellenbroek B.A., Cools A.R. Apomorphine susceptibility and animal models for psychopathology: genes and environment. Behav Genet 2002, 32:349-361.
37. Ellenbroek B.A., Cools A.R. The long-term effects of maternal deprivation depend on the genetic background. Neuropsychopharmacology 2000, 23:99-106.
38. Geyer M.A., Swerdlow N.R. Measurement of startle response, prepulse inhibition, and habituation. Curr Protoc Neurosci 2001, [Chapter 8:Unit 8 7].
39. Ellenbroek B.A., Geyer M.A., Cools A.R. The behavior of APO-SUS rats in animal models with construct validity for schizophrenia. J Neurosci 1995, 15:7604-7611.
40. Plotsky P.M., Thrivikraman K.V., Nemeroff C.B., Caldji C., Sharma S., Meaney M.J. Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 2005, 30:2192-2204.
41. Parent C.I., Meaney M.J. The influence of natural variations in maternal care on play fighting in the rat. Dev Psychobiol 2008, 50:767-776.
42. Claessens S.E., Daskalakis N.P., van der Veen R., Oitzl M.S., de Kloet E.R., Champagne D.L. Development of individual differences in stress responsiveness: an overview of factors mediating the outcome of early life experiences. Psychopharmacology 2011, 214:141-154.
43. Daskalakis N.P., Fung W.L., Schnorr S., Meelis W., Oitzl M.S., De Kloet E.R. The three hit hypothesis of schizophrenia tested in genetically selected rats exposed to early life experience and adolescent psycho-social stressor. Int J Dev Neurosci 2010, 28:698.
44. Daskalakis N.P., Martens G.J., Cools A.R., de Kloet E.R. Schizophrenia endophenotypes and stress hyper-reactivity co-precipitate following adverse life events in genetically susceptible rats. Eur Neuropsychopharmacol 2011, 21:S85-S86.
45. Caspi A., Moffitt T.E. Gene-environment interactions in psychiatry: joining forces with neuroscience. Nature Rev 2006, 7:583-590.
46. Caspi A., Hariri A.R., Holmes A., Uher R., Moffitt T.E. Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am J Psychiatry 2010, 167:509-527.
47. Corcoran C., Walker E., Huot R., Mittal V., Tessner K., Kestler L., et al. The stress cascade and schizophrenia: etiology and onset. Schizophr Bull 2003, 29:671-692.
48. Marinelli M., Piazza P.V. Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur J Neurosci 2002, 16:387-394.
49. Ambroggi F., Turiault M., Milet A., Deroche-Gamonet V., Parnaudeau S., Balado E., et al. Stress and addiction: glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nat Neurosci 2009, 12:247-249.
50. Groenink L., Dirks A., Verdouw P.M., de Graaff M., Peeters B.W., Millan M.J., et al. CRF1 not glucocorticoid receptors mediate prepulse inhibition deficits in mice overexpressing CRF. Biol Psychiatry 2008, 63:360-368.
51. Karst H., Berger S., Turiault M., Tronche F., Schutz G., Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci USA 2005, 102:19204-19207.
52. Karst H., Berger S., Erdmann G., Schutz G., Joels M. Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc Natl Acad Sci USA 2010, 107:14449-14454.
53. Gluckman P.D., Hanson M.A., Beedle A.S. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol 2007, 19:1-19.
54. Ellenbroek B.A., van den Kroonenberg P.T., Cools A.R. The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr Res 1998, 30:251-260.
55. Ellenbroek B.A., Cools A.R. Maternal separation reduces latent inhibition in the conditioned taste aversion paradigm. Neurosci Res Commun 1995, 17:27-33.
56. Roceri M., Hendriks W., Racagni G., Ellenbroek B.A., Riva M.A. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 2002, 7:609-616.
57. Rots N.Y., de Jong J., Workel J.O., Levine S., Cools A.R., De Kloet E.R. Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J Neuroendocrinol 1996, 8:501-506.
58. Daskalakis, N. P., Champagne, D. L., Diamantopoulou, A., Remmers, E., Tjälve, M., Van der Veen, R., et al., submitted for publication. Beyond maternal absence: evidence for the role of peers and non-shared stressful experience in mediating the development of a fearful phenotype.
59. Macri S., Mason G.J., Wurbel H. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. Eur J Neurosci 2004, 20:1017-1024.
60. Tang A.C., Akers K.G., Reeb B.C., Romeo R.D., McEwen B.S. Programming social, cognitive, and neuroendocrine development by early exposure to novelty. Proc Natl Acad Sci USA 2006, 103:15716-15721.
61. Macri S., Wurbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav 2006, 50:667-680.
62. Moriceau S., Wilson D.A., Levine S., Sullivan R.M. Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. J Neurosci 2006, 26:6737-6748.
63. Sullivan R.M., Holman P.J. Transitions in sensitive period attachment learning in infancy: the role of corticosterone. Neurosci Biobehav Rev 2010, 34:835-844.