Subscribe to RSS
DOI: 10.1055/s-0034-1395344
Purkinje Cell Dendritic Atrophy Induced by Prenatal Stress Is Mitigated by Early Environmental Enrichment
Publication History
13 February 2014
11 September 2014
Publication Date:
23 December 2014 (online)
![](https://www.thieme-connect.de/media/neuropediatrics/201501/lookinside/thumbnails/10.1055-s-0034-1395344-1.jpg)
Abstract
Background Prenatal stress (PS) in experimental animals causes long-lasting changes in Purkinje cell dendritic morphology. Furthermore, these structural changes are associated with an increase in anxiogenic behaviors in the elevated plus maze (EPM) and open-field (OF) test.
Objectives As environmental enrichment (EE) has significant restorative effects on brain neurons and behavior, the aim of this study was to evaluate if postweaning EE mitigates the decrease in Purkinje cell dendritic expansion and exploratory behavior induced by PS in mice.
Materials and Methods Restraint stress was induced from gestational day 14 (G14) to G21. Approximately 50% of the PS animals were submitted to the EE paradigm between postnatal days 22 (P22) and P52. At P52 and P82, male animals were behaviorally evaluated, and then the morphology of the cerebellar vermal Purkinje cells was analyzed.
Results We found that EE significantly ameliorates the Purkinje cell dendritic atrophy and anxiety-like behavior in the EPM.
Conclusion Our data show that long-lasting Purkinje cell dendritic impairments and anxiety-like behavior can be mitigated by postweaning EE.
-
References
- 1 O'Connor TG, Heron J, Glover V ; Alspac Study Team. Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. J Am Acad Child Adolesc Psychiatry 2002; 41 (12) 1470-1477
- 2 Van den Bergh BR, Marcoen A. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev 2004; 75 (4) 1085-1097
- 3 Davis EP, Snidman N, Wadhwa PD, Glynn LM, Schetter CD, Sandman CA. Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy 2004; 6: 319-331
- 4 Howes OD, McDonald C, Cannon M, Arseneault L, Boydell J, Murray RM. Pathways to schizophrenia: the impact of environmental factors. Int J Neuropsychopharmacol 2004; 7 (Suppl. 01) S7-S13
- 5 Ronald A, Pennell CE, Whitehouse AJ. Prenatal maternal stress associated with ADHD and autistic traits in early childhood. Front Psychol 2011; 1: 223
- 6 Talge NM, Neal C, Glover V. Early Stress, Translational Research and Prevention Science Network: Fetal and Neonatal Experience on Child and Adolescent Mental Health. Antenatal maternal stress and long-term effects on child neurodevelopment: how and why?. J Child Psychol Psychiatry 2007; 48 (3-4) 245-261
- 7 Martin P, Albers M. Cerebellum and schizophrenia: a selective review. Schizophr Bull 1995; 21 (2) 241-250
- 8 Rasser PE, Schall U, Peck G , et al. Cerebellar grey matter deficits in first-episode schizophrenia mapped using cortical pattern matching. Neuroimage 2010; 53 (4) 1175-1180
- 9 Buss C, Davis EP, Muftuler LT, Head K, Sandman CA. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 2010; 35 (1) 141-153
- 10 Pascual R, Ebner D, Araneda R, Urqueta MJ, Bustamante C. Maternal stress induces long-lasting Purkinje cell developmental impairments in mouse offspring. Eur J Pediatr 2010; 169 (12) 1517-1522
- 11 Diamond MC, Rosenzweig MR, Bennett EL, Lindner B, Lyon L. Effects of environmental enrichment and impoverishment on rat cerebral cortex. J Neurobiol 1972; 3 (1) 47-64
- 12 Li M, Wang M, Ding S, Li C, Luo X. Environmental enrichment during gestation improve behavior consequences and synaptic plasticity in hippocampus on prenatal-stressed offspring rats. Acta Histochem Cytochem 2012; 45 (3) 157-166
- 13 Nithianantharajah J, Hannan AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 2006; 7 (9) 697-709
- 14 Fujioka T, Sakata Y, Yamaguchi K, Shibasaki T, Kato H, Nakamura S. The effects of prenatal stress on the development of hypothalamic paraventricular neurons in fetal rats. Neuroscience 1999; 92 (3) 1079-1088
- 15 Simpson J, Kelly JP. The impact of environmental enrichment in laboratory rats—behavioural and neurochemical aspects. Behav Brain Res 2011; 222 (1) 246-264
- 16 Beauquis J, Roig P, De Nicola AF, Saravia F. Short-term environmental enrichment enhances adult neurogenesis, vascular network and dendritic complexity in the hippocampus of type 1 diabetic mice. PLoS ONE 2010; 5 (11) e13993
- 17 Larsell O. The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J Comp Neurol 1952; 97 (2) 281-356
- 18 Van Essen DC. Surface-based atlases of cerebellar cortex in the human, macaque, and mouse. Ann N Y Acad Sci 2002; 978: 468-479
- 19 Zecevic N, Rakic P. Differentiation of Purkinje cells and their relationship to other components of developing cerebellar cortex in man. J Comp Neurol 1976; 167 (1) 27-47
- 20 Ulupinar E, Yucel F. Prenatal stress reduces interneuronal connectivity in the rat cerebellar granular layer. Neurotoxicol Teratol 2005; 27 (3) 475-484
- 21 Ulupinar E, Yucel F, Ortug G. The effects of prenatal stress on the Purkinje cell neurogenesis. Neurotoxicol Teratol 2006; 28 (1) 86-94
- 22 Rinaudo P, Wang E. Fetal programming and metabolic syndrome. Annu Rev Physiol 2012; 74: 107-130
- 23 Loeber RT, Cintron CM, Yurgelun-Todd DA. Morphometry of individual cerebellar lobules in schizophrenia. Am J Psychiatry 2001; 158 (6) 952-954
- 24 Champagne FA. Early environments, glucocorticoid receptors, and behavioral epigenetics. Behav Neurosci 2013; 127 (5) 628-636
- 25 Weaver IC. Epigenetic effects of glucocorticoids. Semin Fetal Neonatal Med 2009; 14 (3) 143-150
- 26 Kinnunen AK, Koenig JI, Bilbe G. Repeated variable prenatal stress alters pre- and postsynaptic gene expression in the rat frontal pole. J Neurochem 2003; 86 (3) 736-748
- 27 Floeter MK, Greenough WT. Cerebellar plasticity: modification of Purkinje cell structure by differential rearing in monkeys. Science 1979; 206 (4415) 227-229
- 28 Leggio MG, Mandolesi L, Federico F , et al. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 2005; 163 (1) 78-90
- 29 Cernak K, Stevens V, Price R, Shumway-Cook A. Locomotor training using body-weight support on a treadmill in conjunction with ongoing physical therapy in a child with severe cerebellar ataxia. Phys Ther 2008; 88 (1) 88-97
- 30 Hoekzema E, Carmona S, Tremols V , et al. Enhanced neural activity in frontal and cerebellar circuits after cognitive training in children with attention-deficit/hyperactivity disorder. Hum Brain Mapp 2010; 31 (12) 1942-1950
- 31 Ilg W, Synofzik M, Brötz D, Burkard S, Giese MA, Schöls L. Intensive coordinative training improves motor performance in degenerative cerebellar disease. Neurology 2009; 73 (22) 1823-1830
- 32 Koeneke S, Lutz K, Wüstenberg T, Jäncke L. Long-term training affects cerebellar processing in skilled keyboard players. Neuroreport 2004; 15 (8) 1279-1282
- 33 Dickerson PA, Lally BE, Gunnel E, Birkle DL, Salm AK. Early emergence of increased fearful behavior in prenatally stressed rats. Physiol Behav 2005; 86 (4) 586-593
- 34 Estanislau C, Morato S. Behavior ontogeny in the elevated plus-maze: prenatal stress effects. Int J Dev Neurosci 2006; 24 (4) 255-262
- 35 Rimondini R, Agren G, Börjesson S, Sommer W, Heilig M. Persistent behavioral and autonomic supersensitivity to stress following prenatal stress exposure in rats. Behav Brain Res 2003; 140 (1-2) 75-80
- 36 Schmahmann JD. The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol Rev 2010; 20 (3) 236-260
- 37 Schutter DJLG. The cerebello-hypothalamic-pituitary-adrenal axis dysregulation hypothesis in depressive disorder. Med Hypotheses 2012; 79 (6) 779-783
- 38 Andreatini R, Bacellar LF. Animal models: trait or state measure? The test-retest reliability of the elevated plus-maze and behavioral despair. Prog Neuropsychopharmacol Biol Psychiatry 2000; 24 (4) 549-560
- 39 Hall FS, Huang S, Fong GW, Sundstrom JM, Pert A. Differential basis of strain and rearing effects on open-field behavior in Fawn Hooded and Wistar rats. Physiol Behav 2000; 71 (5) 525-532
- 40 Pascual R, Bustamante C. Early postweaning social isolation but not environmental enrichment modifies vermal Purkinje cell dendritic outgrowth in rats. Acta Neurobiol Exp (Warsz) 2013; 73 (3) 387-393