Transgenerational sex-specific impact of preconception stress on the development of dendritic spines and dendritic length in the medial prefrontal cortex

Brain Structure and Function

Volumn 221, Issue 2, 2016, Pages 855-863

  Bock, Joerg ^a,b   Poeschel, Julia ^c   Schindler, Julia ^c   Börner, Florian ^c   Shachar Dadon, Alice ^d   Ferdman, Neta ^d   Gaisler Salomon, Inna ^d,e   Leshem, Micah ^d   Braun, Katharina ^a,b   Poeggel, Gerd ^c  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b Center for Brain and Behavioral Sciences (CBBS)   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d UNIVERSITY OF HAIFA   (Israel)

^e Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Prefrontal; Pregestational stress; Prereproductive stress; Synaptic development; Transgenerational

Indexed keywords

ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; CHRONIC UNPREDICTABLE STRESS; CONCEPTION; CONTROLLED STUDY; DAM (ANIMAL); DENDRITE; DENDRITIC SPINE; FEMALE; INFRALIMBIC CORTEX; LEFT HEMISPHERE; MALE; MEDIAL PREFRONTAL CORTEX; MOTHER; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEAR REPROGRAMMING; ORBITAL CORTEX; PREGNANCY; PRELIMBIC CORTEX; PRENATAL STRESS; PRIORITY JOURNAL; PROGENY; PYRAMIDAL NERVE CELL; RAT; REPRODUCTION; SEX DIFFERENCE; ANIMAL; BRAIN; CINGULATE GYRUS; EMOTION; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; SPRAGUE DAWLEY RAT; SYNAPSE;

ANIMALS; BRAIN; DENDRITES; DENDRITIC SPINES; EMOTIONS; FEMALE; GYRUS CINGULI; MALE; PREFRONTAL CORTEX; PREGNANCY; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; STRESS, PSYCHOLOGICAL; SYNAPSES;

EID: 84959354692     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0940-4     Document Type: Article

References (54)

1. Baider L, Peretz T, Hadani PE, Perry S, Avramov R, De-Nour AK (2000) Transmission of response to trauma? Second-generation Holocaust survivors’ reaction to cancer. Am J Psychiatry 157(6):904–910
2. Bock J, Gruss M, Becker S, Braun K (2005) Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb Cortex 15(6):802–808
3. Bock J, Murmu RP, Ferdman N, Leshem M, Braun K (2008) Refinement of dendritic and synaptic networks in the rodent anterior cingulate and orbitofrontal cortex: critical impact of early and late social experience. Dev Neurobiol 68(5):685–695
4. Bock J, Murmu MS, Biala Y, Weinstock M, Braun K (2011) Prenatal stress and neonatal handling induce sex-specific changes in dendritic complexity and dendritic spine density in hippocampal subregions of prepubertal rats. Neuroscience 193:34–43
5. Bock J, Rether K, Groger N, Xie L, Braun K (2014) Perinatal programming of emotional brain circuits: an integrative view from systems to molecules. Front Neurosci 8:11
6. Bohacek J, Farinelli M, Mirante O, Steiner G, Gapp K, Coiret G, Ebeling M, Duran-Pacheco G, Iniguez AL, Manuella F, Moreau JL, Mansuy IM (2014) Pathological brain plasticity and cognition in the offspring of males subjected to postnatal traumatic stress. Mol Psychiatry. doi:10.1038/mp.2014.80
7. Boudouresque F, Guillaume V, Grino M, Strbak V, Chautard T, Conte-Devolx B, Oliver C (1988) Maturation of the pituitary-adrenal function in rat fetuses. Neuroendocrinology 48(4):417–422
8. Cameron NM, Shahrokh D, Del C, Dhir SK, Szyf M, Champagne FA, Meaney MJ (2008) Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinol 20(6):795–801
9. Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29(3):386–397
10. Champagne FA, Curley JP (2009) Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neurosci Biobehav Rev 33(4):593–600
11. Champagne FA, Meaney MJ (2007) Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 121(6):1353–1363
12. Chocyk A, Bobula B, Dudys D, Przyborowska A, Majcher-Maslanka I, Hess G, Wedzony K (2013) Early-life stress affects the structural and functional plasticity of the medial prefrontal cortex in adolescent rats. Eur J Neurosci 38(1):2089–2107
13. Dietz DM, Laplant Q, Watts EL, Hodes GE, Russo SJ, Feng J, Oosting RS, Vialou V, Nestler EJ (2011) Paternal transmission of stress-induced pathologies. Biol Psychiatry 70(5):408–414
14. Dunn GA, Morgan CP, Bale TL (2011) Sex-specificity in transgenerational epigenetic programming. Horm Behav 59(3):290–295
15. Ferdman N, Murmu RP, Bock J, Braun K, Leshem M (2007) Weaning age, social isolation, and gender, interact to determine adult explorative and social behavior, and dendritic and spine morphology in prefrontal cortex of rats. Behav Brain Res 180(2):174–182
16. Franklin TB, Russig H, Weiss IC, Graff J, Linder N, Michalon A, Vizi S, Mansuy IM (2010) Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 68(5):408–415
17. Franklin TB, Linder N, Russig H, Thony B, Mansuy IM (2011) Influence of early stress on social abilities and serotonergic functions across generations in mice. PLoS One 6(7):e21842
18. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, Farinelli L, Miska E, Mansuy IM (2014) Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 17(5):667–669
19. Glaser EM, Van der Loos H (1981) Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J Neurosci Methods 4(2):117–125
20. Gos T, Bock J, Poeggel G, Braun K (2008) Stress-induced synaptic changes in the rat anterior cingulate cortex are dependent on endocrine developmental time windows. Synapse 62(3):229–232
21. Grigoryan G, Segal M (2013) Prenatal stress affects network properties of rat hippocampal neurons. Biol Psychiatry 73(11):1095–1102
22. Helmeke C, Ovtscharoff W Jr, Poeggel G, Braun K (2001a) Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. Cereb Cortex 11(8):717–727
23. Helmeke C, Poeggel G, Braun K (2001b) Differential emotional experience induces elevated spine densities on basal dendrites of pyramidal neurons in the anterior cingulate cortex of Octodon degus. Neuroscience 104(4):927–931
24. Hoffmann A, Spengler D (2012) The lasting legacy of social stress on the epigenome of the hypothalamic-pituitary-adrenal axis. Epigenomics 4(4):431–444
25. Izquierdo A, Wellman CL, Holmes A (2006) Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J Neurosci 26(21):5733–5738
26. Jirtle RL, Skinner MK (2007) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8(4):253–262
27. Van IJzendoorn MH, Bakermans-Kranenburg MJ, Sagi-Schwartz A (2003) Are children of Holocaust survivors less well-adapted? A meta-analytic investigation of secondary traumatization. J Trauma Stress 16(5):459–469
28. Koenig JI, Elmer GI, Shepard PD, Lee PR, Mayo C, Joy B, Hercher E, Brady DL (2005) Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behav Brain Res 156(2):251–261
29. Leshem M, Schulkin J (2012) Transgenerational effects of infantile adversity and enrichment in male and female rats. Dev Psychobiol 54(2):169–186
30. Li H, Zhang L, Fang Z, Lin L, Wu C, Huang Q (2010) Behavioral and neurobiological studies on the male progeny of maternal rats exposed to chronic unpredictable stress before pregnancy. Neurosci Lett 469(2):278–282
31. Lutz PE, Turecki G (2014) DNA methylation and childhood maltreatment: from animal models to human studies. Neuroscience 264C:142–156
32. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O (2003) Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27(1–2):119–127
33. Muhammad A, Kolb B (2011) Mild prenatal stress-modulated behavior and neuronal spine density without affecting amphetamine sensitization. Dev Neurosci 33(2):85–98
34. Muhammad A, Carroll C, Kolb B (2012) Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience 216:103–109
35. Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J (2006) Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 24(5):1477–1487
36. Mychasiuk R, Gibb R, Kolb B (2012) Prenatal stress alters dendritic morphology and synaptic connectivity in the prefrontal cortex and hippocampus of developing offspring. Synapse 66(4):308–314
37. Paxinos G, Watson C (2004) The rat brain in stereotaxic coordinates, vol 5. Elsevier/Academic Press, Amsterdam
38. Perez-Cruz C, Muller-Keuker JI, Heilbronner U, Fuchs E, Flugge G (2007) Morphology of pyramidal neurons in the rat prefrontal cortex: lateralized dendritic remodeling by chronic stress. Neural Plast 2007:46276
39. Poeggel G, Helmeke C, Abraham A, Schwabe T, Friedrich P, Braun K (2003) Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc Natl Acad Sci USA 100(26):16137–16142
40. Sagi-Schwartz A, van IMH, Bakermans-Kranenburg MJ (2008) Does intergenerational transmission of trauma skip a generation? No meta-analytic evidence for tertiary traumatization with third generation of Holocaust survivors. Attach Hum Dev 10(2):105–121
41. Shachar-Dadon A, Schulkin J, Leshem M (2009) Adversity before conception will affect adult progeny in rats. Dev Psychol 45(1):9–16
42. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87(4):387–406
43. Stevenson CW, Halliday DM, Marsden CA, Mason R (2008) Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex. Neuroscience 155(3):852–863
44. Sullivan RM (2004) Hemispheric asymmetry in stress processing in rat prefrontal cortex and the role of mesocortical dopamine. Stress 7(2):131–143
45. Szyf M (2013) How do environments talk to genes? Nat Neurosci 16(1):2–4
46. Weaver IC, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7(8):847–854
47. Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65(5):427–451
48. Weinstock M (2007) Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 10:1730–1740
49. Weinstock M (2008) The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32(6):1073–1086
50. Weiss IC, Franklin TB, Vizi S, Mansuy IM (2011) Inheritable effect of unpredictable maternal separation on behavioral responses in mice. Front Behav Neurosci 5:3
51. Yehuda R, Bierer LM (2008) Transgenerational transmission of cortisol and PTSD risk. Prog Brain Res 167:121–135
52. Yehuda R, Engel SM, Brand SR, Seckl J, Marcus SM, Berkowitz GS (2005) Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. J Clin Endocrinol Metab 90(7):4115–4118
53. Youngson NA, Whitelaw E (2008) Transgenerational epigenetic effects. Annu Rev Genomics Hum Genet 9:233–257
54. Zaidan H, Leshem M, Gaisler-Salomon I (2013) Prereproductive stress to female rats alters corticotropin releasing factor type 1 expression in ova and behavior and brain corticotropin releasing factor type 1 expression in offspring. Biol Psychiatry. doi:10.1016/j.biopsych.2013.04.014