Neurobehavioural disorders in the infant reeler mouse model: Interaction of genetic vulnerability and consequences of maternal separation

Behavioural Brain Research

Volumn 177, Issue 1, 2007, Pages 142-149

  Ognibene, Elisa ^a   Adriani, Walter ^a   Macrì, Simone ^a   Laviola, Giovanni ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Autism; Gene environment interaction; Handling; Maternal separation; Mice; Ontogeny of behaviour; Schizophrenia; Ultrasound vocalisations

Indexed keywords

REELIN; SCLEROPROTEIN;

ANIMAL BEHAVIOR; ANIMAL COMMUNICATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; EMOTION; FEMALE; GENETIC SUSCEPTIBILITY; GENOTYPE; GENOTYPE PHENOTYPE CORRELATION; HETEROZYGOSITY; HOMOZYGOSITY; HORMONAL REGULATION; LOCOMOTION; MALE; MATERNAL DEPRIVATION; MOTIVATION; NERVE CELL NETWORK; NEUROCHEMISTRY; NEUROENDOCRINE SYSTEM; NEUROLOGIC DISEASE; NEUROPSYCHIATRY; NEWBORN; NONHUMAN; ONTOGENY; PATHOPHYSIOLOGY; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PSYCHOPHYSIOLOGY; PUP (RODENT); SEX DIFFERENCE; SOCIAL BEHAVIOR; STRESS; ULTRASOUND; VOCALIZATION; WILD TYPE;

ANIMALS; ANIMALS, NEWBORN; CELL ADHESION MOLECULES, NEURONAL; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX PROTEINS; HOMING BEHAVIOR; MATERNAL DEPRIVATION; MENTAL DISORDERS; MICE; MICE, NEUROLOGIC MUTANTS; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; REACTION TIME; SERINE ENDOPEPTIDASES; VOCALIZATION, ANIMAL;

EID: 33846001701     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2006.10.027     Document Type: Article

References (55)

1. Ader R., and Grota L.J. Effects of early experience on adrenocortical reactivity. Physiol Behav 4 (1969) 303-305
2. Agid O., Shapira B., Zislin J., Ritsner M., Hanin B., Murad H., et al. Environment and vulnerability to major psychiatric illness-a case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Mol Psychiatry 4 (1999) 163-172
3. Alleva E., Laviola G., Tirelli E., and Bignami G. Short-, medium-, and long-term effects of prenatal oxazepam on neurobehavioural development of mice. Psychopharmacology (Berl) 87 4 (1985) 434-441
4. Andersen T.E., Finsen B., Goffinet A.M., Issinger O.G., and Boldyreff B. A reeler mutant mouse with a new, spontaneous mutation in the reelin gene. Brain Res Mol Brain Res 105 1/2 (2002) 153-156
5. Assenza G., Biamonte F., Cesa R., Strata P., and Keller F. Interaction between reelin and estrogens on Purkinje cells during development: a model of cerebellar pathology in autism and related disorders. Abstract national congress of the Italian society for neuroscience and joint Italian-Swedish neuroscience meeting Regina Isabella Congress Center Lacco Ameno (2006)
6. Bateson P., Barker D., Clutton-Brock T., Deb D., D'Udine B., Foley R.A., et al. Developmental plasticity and human health. Nature 430 6998 (2004) 419-421
7. Bartlett C.W., Gharani N., Millonig J.H., and Brzustowicz L.M. Three autism candidate genes: a synthesis of human genetic analysis with other disciplines. Int J Dev Neurosci 23 (2005) 221-234
8. Biagini G., Merlo Pich E., Carani C., Marrama P., and Agnati F.L. Postnatal maternal separation during the SHRP enhances the adrenocortical response to novelty in adult rats by affecting feedback regulation in the CA1 hippocampal field. Int J Dev Neurosci 16 (1997) 187-197
9. Branchi I., Santucci D., and Alleva E. Ultrasonic vocalisation emitted by infant rodents: a tool for assessment of neurobehavioural development. Behav Brain Res 125 (2001) 49-56
10. Branchi I., and Ricceri L. Transgenic and knock-out mouse pups: the growing need for behavioural analysis. Gen Brain Behav 3 (2002) 135-141
11. Caspi A., Reichenberg A., Weiser M., Rabinowitz J., Kaplan Z., Knobler H., et al. Cognitive performance in schizophrenia patients assessed before and following the first psychotic episodi. Schizophr Res 65 2/3 (2003) 87-94
12. Cirulli F., Adriani W., and Laviola G. Sexual segregation in infant mice: behavioural and neuroendocrine responses to d-amphetamine administration. Psychopharmacology 134 (1997) 140-152
13. Cirulli F., Santucci D., Laviola G., Alleva E., and Levine S. Behavioural and hormonal responses to stress in the newborn mouse: effects of maternal deprivation and chlordiazepoxide. Dev Psychobiol 27 (1994) 301-316
14. Costa E., Davis J., Grayson D.R., Guidotti A., Pappas G.D., and Pesold C. Dendritic spine hypoplasia and downregulation of reelin and GABAergic tone in schizophrenia vulnerability. Neurobiol Dis 8 (2001) 723-742
15. Costa E., Davis J., Pesold C., Tueting P., and Guidotti A. The heterozygote reeler mouse as a model for the development of a new generation of antipsychotics. Curr Opin Pharmacol 2 (2002) 56-62
16. Elwood R.W., and Keeling F. Temporal organization of ultrasonic vocalizations in infant mice. Dev Psychobiol 15 (1982) 221-227
17. Fatemi S.H., Earle J.A., and McMenomy T. Reduction in reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorders and major depression. Mol Psychiatry 5 (2000) 653-654
18. Francis D.D., and Meaney M.J. Maternal care and the development of stress responses. Curr Opin Neurobiol 9 (1999) 128-134
19. Gluckman P.D., Hanson M.A., Spencer H.G., and Bateson P. Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc Biol Sci (2005)
20. Gottesman I.I., and Hanson D.R. Human development: biological and genetic processes. Annu Rev Psychol 2 (2005) 263-286
21. Heim C., and Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders-preclinical and clinical studies. Biol Psychiatry 49 (2001) 1023-1039
22. Heim C., Newport D.J., Bonsall R., Miller A.H., and Nemeroff C.B. Altered pituitary-adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. Am J Psychiatry 158 (2001) 575-581
23. Heim C., Newport D.J., Heit S., Graham Y.P., Wilcox M., Bonsall R., et al. Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 284 (2000) 592-597
24. Hofer M.A. Early relationships as regulators of infant physiology and behaviour. Acta Paediatr 397 (1994) 9-18
25. Jobe T.H., and Harrow M. Long-term outcome of patients with schizophrenia: a review. Can J Psychiatry 50 (2005) 892-900
26. Laviola G., and Andersen S.L. Brain development, sex differences and stress: implications for psychopathology. Neurosci Biobehav Rev 27 (2003) 2003
27. Laviola G., Sedowofia K., Innes J., Clayton R., and Manning A. Genetic differences in maternal behaviour patterns in mice administered phenobarbital during pregnancy. Psychopharmacology (Berl) 102 3 (1990) 383-390
28. Laviola G., Adriani W., Gaudino C., Marino R., and Keller F. Paradoxical effects of prenatal acetilcholinesterase blockade on neurobehavioural development and drug-induced stereotipies in reeler mice. Psychopharmacology 187 3 (2006) 331-344 [Epub 2006 June]
29. Lehmann J., and Feldon J. Long-term bio-behavioural effects of maternal separation in the rat: consistent or confusing?. Rev Neurosci 11 (2000) 383-408
30. Lehmann J., Pryce C.R., Jongen-Relo A.L., Stöhr T., Pothuizen H.J., and Feldon J. Comparison of maternal separation and early handling in terms of neurobehavioural effects in aged rats. Neurobiol Aging 23 (2002) 457-466
31. Levine S. Infantile experience and resistance to physiological stress. Science 126 (1957) 405-406
32. Levine S., Haltmeyer G.C., Karas G.G., and Denenberg V.H. Physiological and behavioural effects of infantile stimulation. Physiol Behav 2 (1967) 55-63
33. 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 277 (1997) 1659-1662
34. Liu W.S., Pesold C., Rodriguez M.A., Carboni G., Auta J., and Lacor P. Downregulation of dendritic spine and glutamic acid decarboxylase 67 expressions in reelin haploinsufficient reeler mouse. Proc Natl Acad Sci USA 98 (2001) 3477-3482
35. Macrì S., Mason G.J., and Würbel 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 20 (2004) 1017-1024
36. Macrì S., and Würbel H. Effects of variation in postnatal maternal environment on maternal behaviour and fear and stress responses in rats. Anim Behav 73 (2007) 171-184
37. Macrì S., and Würbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav 50 (2006) 667-680
38. Matthews K., Hall S.F., Wilkinson L.S., and Robbins T.W. Retarded acquisition and reduced expression of conditioned locomotor activity in adult rats following repeated maternal separation: effects of prefeeding, d-amphetamine, dopamine antagonists and clonidine. Psychopharmacology 126 (1996) 75-84
39. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann Rev Neurosci 24 (2001) 1161-1192
40. Naito H., and Tonoue T. Sex difference in ultrasound distress call by rat pups. Behav Brain Res 25 (1987) 13-21
41. Ognibene E, Adriani W, Granstrem O, Pieretti S, La viola G. Impulsivity-anxiety-related behaviour and profiles of morphine-induced analgesia in heterozygous reeler mice, Brain Res, in press, doi:10.1016/j.brainres.2006.11.007.
42. Persico A.M., and Keller F. The neurobiological context of autism. Mol Neurobiol 28 (2003) 1-22
43. Podhorna J., and Didriksen M. The heterozygous reeler mouse: behavioural phenotype. Behav Brain Res 153 (2003) 43-54
44. Qiu S., Korwek K.M., Pratt-Davis A.R., Peters M., Bergman M.Y., and Weeber E.J. Cognitive disruption and altered hippocampus synaptic function in Reelin haploinsufficient mice. Neurobiol Learn Memory 85 (2006) 228-242
45. Ricceri L., Markina N., Valanzano A., Fortuna S., Cometa M.F., Meneguz A., et al. Developmental exposure to chlorpyrifos alters reactivity to environmental and social cues in adolescent mice. Toxicol Appl Pharmacol (2003) 189-201
46. Romeo R., Mueller A., Sisti M., Ogawa S., McEwen B.S., and Brake W. Anxiety and fear behaviours in adult male and female C57BL/6 mice are modulated by maternal separation. Hormones Behav 43 5 (2003) 561-567
47. Salinger W.L., Ladrow P., and Wheeler C. Behavioural phenotype of the reeler mutant mouse: effects of Reln gene dosage and social isolation. Behav Neurosci 6 (2003) 1257-1275
48. Santucci D., Cagiano R., and Calamandrei G. IGF-I and IGF-I24-41 but not IGF-I57-70 affect somatic and neurobehavioural development of newborn male mice. Brain Res Bull (1994) 367-371
49. Schmidt M.V., Levine S., Alam S., Harbich D., Sterlemann V., Ganea K., et al. Metabolic signals modulate hypothalamic-pituitary-adrenal axis activation during maternal separation of the neonatal mouse. J Neuroendocrinol 18 (2006) 865-874
50. Selemon L.D., and Goldman-Rakic P.S. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 45 (1999) 17-25
51. Stern J.M. Somatosensation and maternal care in Norway rats. In: Rosenblett J.S., and Snowdon C.T. (Eds). Parental care: evolution, mechanism, and adaptive significance (1996), Academic Press, San Diego 243-294
52. Tissir F., and Goffinet A.M. Reelin and brain development. Nat Rev Neurosci 4 (2003) 496-505
53. Tremolizzo L., Carboni G., Ruzicka W.B., Mitchell C.P., Sugaya P., Tueting P., et al. An epigenetic mouse model for molecular and behavioural neuropathologies related to schizophrenia vulnerability. Proc Natl Acad Sci 99 (2002) 17095-17100
54. Winslow J.T., and Insel T.R. The infant rat separation paradigm: a novel test for novel anxiolytics. Trends Pharmacol Sci 12 (1991) 402-404
55. Zimmerberg B., and Kajunsky E.W. Sexually dimorphic effects of postnatal allopregnanolone on the development of anxiety behaviour after early deprivation. Pharmacol Biochem Behav 78 (2004) 465-471