Impact of early-life stress on the medial prefrontal cortex functions-a search for the pathomechanisms of anxiety and mood disorders

Pharmacological Reports

Volumn 65, Issue 6, 2013, Pages 1462-1470

  Chocyk, Agnieszka ^a   Majcher Maoelanka, Iwona ^a   Dudys, Dorota ^a   Przyborowska, Aleksandra ^a   Wêdzony, Krzysztof ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

Anxiety; Early life stress; Epigenetics; Maternal separation; Medial prefrontal cortex; Mood disorders; Prenatal stress; Synaptic plasticity

Indexed keywords

MICRORNA;

ANIMAL BEHAVIOR; ANXIETY DISORDER; DISEASE ACTIVITY; DNA METHYLATION; DNA SEQUENCE; EARLY LIFE STRESS; EPIGENETICS; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; HISTONE ACETYLATION; HUMAN; LONG TERM POTENTIATION; MEDIAL PREFRONTAL CORTEX; MOOD DISORDER; NERVE CELL PLASTICITY; NEUROPATHOLOGY; NONHUMAN; PREFRONTAL CORTEX; REINFORCEMENT; REVIEW;

ANIMALS; ANXIETY; EPIGENESIS, GENETIC; HUMANS; MOOD DISORDERS; PREFRONTAL CORTEX; STRESS, PSYCHOLOGICAL;

EID: 84894158533     PISSN: 22995684     EISSN: 22995684     Source Type: Journal    
DOI: 10.1016/s1734-1140(13)71506-8     Document Type: Article

References (72)

1. Abraham WC, Bear MF: Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci, 1996, 19, 126-130. (Pubitemid 26086492)
2. Banasr M, Duman RS: Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol Psychiatry, 2008, 64, 863-870.
3. Baudin A, Blot K, Verney C, Estevez L, Santa-Maria J, Gressens P, Giros B et al.: Maternal deprivation induces deficits in temporal memory and cognitive flexibility and exaggerates synaptic plasticity in the rat medial prefrontal cortex. Neurobiol Learn Mem, 2012, 98, 207-214.
4. Bock J, Braun K: The impact of perinatal stress on the functional maturation of prefronto-cortical synaptic circuits: implications for the pathophysiology of ADHD? Prog Brain Res, 2011, 189, 155-169.
5. Bock J, Gruss M, Becker S, Braun K: Experienceinduced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb Cortex, 2005, 15, 802-808. (Pubitemid 40696119)
6. Bock J, Riedel A, Braun K: Differential changes of metabolic brain activity and interregional functional coupling in prefronto-limbic pathways during different stress conditions: functional imaging in freely behaving rodent pups. Front Cell Neurosci, 2012, 6, 19.
7. Bordner KA, George ED, Carlyle BC, Duque A, Kitchen RR, Lam TT, Colangelo CM et al.: Functional genomic and proteomic analysis reveals disruption of myelinrelated genes and translation in a mouse model of early life neglect. Front Psychiatry, 2011, 2, 18.
8. Braun K, Antemano R, Helmeke C, Buchner M, Poeggel G: Juvenile separation stress induces rapid region-and layer-specific changes in S100ss-and glial fibrillary acidic protein-immunoreactivity in astrocytes of the rodent medial prefrontal cortex. Neuroscience, 2009, 160, 629-638.
9. Brenhouse HC: Early life adversity alters the developmental profiles of addiction-related prefrontal cortex circuitry. Brain Sci, 2013, 3, 143-158.
10. Brenhouse HC, Andersen SL: Developmental trajectories during adolescence in males and females: a crossspecies understanding of underlying brain changes. Neurosci Biobehav Rev, 2011, 35, 1687-1703.
11. Callaghan BL, Richardson R: Early-life stress affects extinction during critical periods of development: an analysis of the effects of maternal separation on extinction in adolescent rats. Stress, 2012, 15, 671-679.
12. Castaneda AE, Tuulio-Henriksson A, Marttunen M, Suvisaari J, Lonnqvist J: A review on cognitive impairments in depressive and anxiety disorders with a focus on young adults. J Affect Disord, 2008, 106, 1-27. (Pubitemid 350309672)
13. Chan T, Kyere K, Davis BR, Shemyakin A, Kabitzke PA, Shair HN, Barr GA, Wiedenmayer CP: The role of the medial prefrontal cortex in innate fear regulation in infants, juveniles, and adolescents. J Neurosci, 2011, 31, 4991-4999.
14. Chatterjee D, Chatterjee-Chakraborty M, Rees S, Cauchi J, de Medeiros CB, Fleming AS: Maternal isolation alters the expression of neural proteins during development: 'Stroking' stimulation reverses these effects. Brain Res, 2007, 1158, 11-27. (Pubitemid 47068403)
15. Chocyk A, Bobula B, Dudys D, Przyborowska A, Majcher-Maslanka I, Hess G, Wedzony K: Early-life stress affects the structural and functional plasticity of the medial prefrontal cortex in adolescent rats. Eur J Neurosci, 2013, 38, 2089-2107.
16. Chocyk A, Dudys D, Przyborowska A, Maækowiak M, Wêdzony K: Impact of maternal separation on neural cell adhesion molecules expression in dopaminergic brain regions of juvenile, adolescent and adult rats. Pharmacol Rep, 2010, 62, 1218-1224.
17. Chuang JC, Jones PA: Epigenetics and microRNAs. Pediatr Res, 2007, 61, 24R-29R. (Pubitemid 46653064)
18. Daskalakis NP, Bagot RC, Parker KJ, Vinkers CH, de Kloet ER: The three-hit concept of vulnerability and resilience: Toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology, 2013, 38, 1858-1873.
19. de Kloet ER, Sibug RM, Helmerhorst FM, Schmidt MV: Stress, genes and the mechanism of programming the brain for later life. Neurosci Biobehav Rev, 2005, 29, 271-281. (Pubitemid 40461744)
20. Drevets WC, Price JL, Furey ML: Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct, 2008, 213, 93-118.
21. Gould E, Woolley CS, McEwen BS: Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. J Comp Neurol, 1991, 313, 479-485.
22. Gunnar MR: Integrating neuroscience and psychological approaches in the study of early experiences. Ann NY Acad Sci, 2003, 1008, 238-247. (Pubitemid 38265166)
23. Hanson JL, Chung MK, Avants BB, Rudolph KD, Shirtcliff EA, Gee JC, Davidson RJ, Pollak SD: Structural variations in prefrontal cortex mediate the relationship between early childhood stress and spatial working memory. J Neurosci, 2012, 32, 7917-7925.
24. Hayes JP, Hayes SM, Mikedis AM: Quantitative metaanalysis of neural activity in posttraumatic stress disorder. Biol Mood Anxiety Disord, 2012, 2, 9.
25. Heidbreder CA, Groenewegen HJ: The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci Biobehav Rev, 2003, 27, 555-579. (Pubitemid 37346376)
26. Jensen PC, Monk C, Champagne FA: Epigenetic effects of prenatal stress on 11b-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS One, 2012, 7, e39791.
27. Jones PB: Adult mental health disorders and their age at onset. Br J Psychiatry Suppl, 2013, 54, s5-10.
28. Kanagawa T, Tomimatsu T, Hayashi S, Shioji M, Fukuda H, Shimoya K, Murata Y: The effects of repeated corticosteroid administration on the neurogenesis in the neonatal rat. Am J Obstet Gynecol, 2006, 194, 231-238. (Pubitemid 43017802)
29. Kao GS, Cheng LY, Chen LH, Tzeng WY, Cherng CG, Su CC, Wang CY, Yu L: Neonatal isolation decreases cued fear conditioning and frontal cortical histone 3 lysine 9 methylation in adult female rats. Eur J Pharmacol, 2012, 697, 65-72.
30. Kessler RC, McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, Aguilar-Gaxiola S et al.: Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br J Psychiatry, 2010, 197, 378-385.
31. Kolb B,Mychasiuk R,Muhammad A, Li Y, Frost DO, Gibb R: Experience and the developing prefrontal cortex. Proc Natl Acad Sci USA, 2012, 109, Suppl 2, 17186-17193.
32. Leussis MP, Freund N, Brenhouse HC, Thompson BS, Andersen SL: Depressive-like behavior in adolescents after maternal separation: sex differences, controllability, and GABA. Dev Neurosci, 2012, 34, 210-217.
33. Leventopoulos M, Ruedi-Bettschen D, Knuesel I, Feldon J, Pryce CR, Opacka-Juffry J: Long-term effects of early life deprivation on brain glia in Fischer rats. Brain Res, 2007, 1142, 119-126. (Pubitemid 46413198)
34. Levine A, Worrell TR, Zimnisky R, Schmauss C: Early life stress triggers sustained changes in histone deacetylase expression and histone H4 modifications that alter responsiveness to adolescent antidepressant treatment. Neurobiol Dis, 2012, 45, 488-498.
35. Lisboa SF, Stecchini MF, Correa FM, Guimaraes FS, Resstel LB: Different role of the ventral medial prefrontal cortex on modulation of innate and associative learned fear. Neuroscience, 2010, 171, 760-768.
36. Lisman J, Schulman H, Cline H: The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci, 2002, 3, 175-190. (Pubitemid 135706588)
37. Marek R, Strobel C, Bredy TW, Sah P: The amygdala and medial prefrontal cortex: partners in the fear circuit. J Physiol, 2013, 591, 2381-2391.
38. Markham JA, Koenig JI: Prenatal stress: role in psychotic and depressive diseases. Psychopharmacology (Berl), 2011, 214, 89-106.
39. Monroy E, Hernandez-Torres E, Flores G: Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. J Chem Neuroanat, 2010, 40, 93-101.
40. Muhammad A, Kolb B: Maternal separation altered behavior and neuronal spine density without influencing amphetamine sensitization. Behav Brain Res, 2011, 223, 7-16.
41. Musholt K, Cirillo G, Cavaliere C, Rosaria BM, Bock J, Helmeke C, Braun K, Papa M: Neonatal separation stress reduces glial fibrillary acidic protein-and S100b-immunoreactive astrocytes in the rat medial precentral cortex. Dev Neurobiol, 2009, 69, 203-211.
42. Mychasiuk R, Gibb R, Kolb B: Prenatal stress produces sexually dimorphic and regionally specific changes in gene expression in hippocampus and frontal cortex of developing rat offspring. Dev Neurosci, 2011, 33, 531-538.
43. Mychasiuk R, Ilnytskyy S, Kovalchuk O, Kolb B, Gibb R: Intensity matters: brain, behaviour and the epi-genome of prenatally stressed rats. Neuroscience, 2011, 180, 105-110.
44. Myers-Schulz B, Koenigs M: Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders. Mol Psychiatry, 2012, 17, 132-141.
45. Nederhof E, Schmidt MV: Mismatch or cumulative stress: toward an integrated hypothesis of programming effects. Physiol Behav, 2012, 106, 691-700.
46. O'Donnell KJ, Bugge JA, Freeman L, Khalife N, O'Connor TG, Glover V: Maternal prenatal anxiety and downregulation of placental 11b-HSD2. Psychoneuroendocrinology, 2012, 37, 818-826.
47. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF, Jr. et al.: Glial cells in (patho)-physiology. J Neurochem, 2012, 121, 4-27.
48. Pascual R, Zamora-Leon SP: Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat. Acta Neurobiol Exp (Wars), 2007, 67, 471-479.
49. Pattwell SS, Duhoux S, Hartley CA, Johnson DC, Jing D, Elliott MD, Ruberry EJ et al.: Altered fear learning across development in both mouse and human. Proc Natl Acad Sci USA, 2012, 109, 16318-16323.
50. Provencal N, SudermanMJ, Guillemin C,Massart R, Ruggiero A,Wang D, Bennett AJ et al.: The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. J Neurosci, 2012, 32, 15626-15642.
51. Pryce CR, Ruedi-Bettschen D, Dettling AC, Feldon J: Early life stress: long-term physiological impact in rodents and primates. News Physiol Sci, 2002, 17, 150-155.
52. Reynolds RM: Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis -2012 Curt Richter Award Winner. Psychoneuroendocrinology, 2013, 38, 1-11.
53. Rinne-Albers MA, van der Wee NJ, Lamers-Winkelman F, Vermeiren RR: Neuroimaging in children, adolescents and young adults with psychological trauma. Eur Child Adolesc Psychiatry, 2013, [Epub ahead of print].
54. Schmidt MV: Animal models for depression and the mismatch hypothesis of disease. Psychoneuroendocrinology, 2011, 36, 330-338.
55. Schmidt MV, Abraham WC, Maroun M, Stork O, Richter-Levin G: Stress-induced metaplasticity: from synapses to behavior. Neuroscience, 2013, 250, 112-120.
56. Schmidt MV, Wang XD, Meijer OC: Early life stress paradigms in rodents: potential animal models of depression? Psychopharmacology (Berl), 2011, 214, 131-140.
57. Schouten M, Aschrafi A, Bielefeld P, Doxakis E, Fitzsimons CP: MicroRNAs and the regulation of neuronal plasticity under stress conditions. Neuroscience, 2013, 241, 188-205.
58. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ: Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology, 2011, 36, 529-538.
59. Stanton ME, Gutierrez YR, Levine S: Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats. Behav Neurosci, 1988, 102, 692-700.
60. Stevenson CW, Halliday DM, Marsden CA, Mason R: Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex. Neuroscience, 2008, 155, 852-863.
61. Stevenson CW, Spicer CH, Mason R, Marsden CA: Early life programming of fear conditioning and extinction in adult male rats. Behav Brain Res, 2009, 205, 505-510.
62. Uchida S, Hara K, Kobayashi A, Funato H, Hobara T, Otsuki K, Yamagata H et al.: Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. J Neurosci, 2010, 30, 15007-15018.
63. van Harmelen AL, van Tol MJ, van der Wee NJ, Veltman DJ, Aleman A, Spinhoven P, van Buchem MA et al.: Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment. Biol Psychiatry, 2010, 68, 832-838.
64. Wang L, Jiao J, Dulawa SC: Infant maternal separation impairs adult cognitive performance in BALB/cJ mice. Psychopharmacology (Berl), 2011, 216, 207-218.
65. Wang L, Paul N, Stanton SJ, Greeson JM, Smoski MJ: Loss of sustained activity in the ventromedial prefrontal cortex in response to repeated stress in individuals with early-life emotional abuse: implications for depression vulnerability. Front Psychol, 2013, 4, 320.
66. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S et al.: Epigenetic programming by maternal behavior. Nat Neurosci, 2004, 7, 847-854. (Pubitemid 38989508)
67. Weber M, Killgore WD, Rosso IM, Britton JC, Schwab ZJ, Weiner MR, Simon NM et al.: Voxel-based morphometric gray matter correlates of posttraumatic stress disorder. J Anxiety Disord, 2013, 27, 413-419.
68. WHO report: Cross-national comparisons of the prevalences and correlates of mental disorders. Bulletin of the World Health Organization, 2000, 78, 413-426.
69. Xie L, Korkmaz KS, Braun K, Bock J: Early life stressinduced histone acetylations correlate with activation of the synaptic plasticity genes Arc and Egr1 in the mouse hippocampus. J Neurochem, 2013, 125, 457-464.
70. Yu IT, Lee SH, Lee YS, Son H: Differential effects of corticosterone and dexamethasone on hippocampal neurogenesis in vitro. Biochem Biophys Res Commun, 2004, 317, 484-490. (Pubitemid 38452508)
71. Zhang J, Abdallah CG, Chen Y, Huang T, Huang Q, Xu C, Xiao Y et al.: Behavioral deficits, abnormal corticosterone, and reduced prefrontal metabolites of adolescent rats subject to early life stress. Neurosci Lett, 2013, 545, 132-137.
72. Zucchi FC, Yao Y, Ward ID, Ilnytskyy Y, Olson DM, Benzies K, Kovalchuk I et al.: Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring. PLoS One, 2013, 8, e56967.