Fragmentation and high entropy of neonatal experience predict adolescent emotional outcome

Translational Psychiatry

Volumn 6, Issue , 2016, Pages

  Molet, J ^a   Heins, K ^b   Zhuo, X ^a   Mei, Y T ^a   Regev, L ^a   Baram, T Z ^a   Stern, H ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; SUCROSE;

ADOLESCENT; ADOLESCENT BEHAVIOR; ANHEDONIA; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BIOLOGICAL RHYTHM; BRAIN DEVELOPMENT; BRAIN MATURATION; CLINICAL ASSESSMENT; CONTROLLED STUDY; DEPRESSION; DOPAMINERGIC ACTIVITY; EARLY LIFE STRESS; EMOTIONAL DISORDER; ENTROPY; ENVIRONMENTAL FACTOR; HELPLESSNESS; HUMAN; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; MATHEMATICAL ANALYSIS; NEWBORN; NEWBORN PERIOD; NONHUMAN; NURTURING BEHAVIOR; OUTCOME ASSESSMENT; PEER GROUP; PERSONAL EXPERIENCE; PLEASURE; PROGENY; RAT; REARING; SENSORY CORTEX; SENSORY STIMULATION; SOCIAL INTERACTION; ANIMAL; ANIMAL BEHAVIOR; EMOTION; FEMALE; MENTAL STRESS; PSYCHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; EMOTIONS; FEMALE; MALE; MATERNAL BEHAVIOR; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL;

EID: 84953790459     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.200     Document Type: Article

References (68)

1. Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry 2010; 68: 314-319
2. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003; 301: 386-389
3. Heim C, Binder EB. Current research trends in early life stress and depression: review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Exp Neurol 2012; 233: 102-111
4. NIMH Workgroup. Transformative Neurodevelopmental Research in Mental Illness-Report of the National Advisory Mental Health Council,s Workgroup. Available at http: //www.nimh.nih.gov/about/advisory-boards-and-groups/namhc/neurodevelopment-workgroup-report-33553.pdf
5. Espinosa JS, Stryker MP. Development and plasticity of the primary visual cortex. Neuron 2012; 75: 230-249
6. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsaki G. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 2004; 432: 758-761
7. Dulac C, O'Connell LA, Wu Z. Neural control of maternal and paternal behaviors. Science 2014; 345: 765-770
8. Aggleton JP, Blindt HS, Rawlins JN. Effects of amygdaloid and amygdaloidhippocampal lesions on object recognition and spatial working memory in rats. Behav Neurosci 1989; 103: 962-974
9. Bowlby J. Research into the origins of delinquent behaviour. Br Med J 1950; 1: 570-573
10. Gunnar MR. Reversing the effects of early deprivation after infancy: giving children families may not be enough. Front Neurosci 2010; 4: 170
11. Nelson CA 3rd, Zeanah CH, Fox NA, Marshall PJ, Smyke AT, Guthrie D. Cognitive recovery in socially deprived young children: the Bucharest Early Intervention Project. Science 2007; 318: 1937-1940
12. Maestripieri D, Higley JD, Lindell SG, Newman TK, McCormack KM, Sanchez MM. Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques (Macaca mulatta). Behav Neurosci 2006; 120: 1017-1024
13. Parker KJ, Buckmaster CL, Sundlass K, Schatzberg AF, Lyons DM. Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc Natl Acad Sci USA 2006; 103: 3000-3005
14. Sabatini MJ, Ebert P, Lewis DA, Levitt P, Cameron JL, Mirnics K. Amygdala gene expression correlates of social behavior in monkeys experiencing maternal separation. J Neurosci 2007; 27: 3295-3304
15. Seay B, Hansen E, Harlow HF. Mother-infant separation in monkeys. J Child Psychol Psychiatry 1962; 3: 123-132
16. Champagne FA, Francis DD, Mar A, Meaney MJ. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003; 79: 359-371
17. Dalle Molle R, Portella AK, Goldani MZ, Kapczinski FP, Leistner-Segal S, Salum GA et al. Associations between parenting behavior and anxiety in a rodent model and a clinical sample: relationship to peripheral BDNF levels. Transl Psychiatry 2012; 2: e195
18. Malter Cohen M, Jing D, Yang RR, Tottenham N, Lee FS, Casey BJ. Early-life stress has persistent effects on amygdala function and development in mice and humans. Proc Natl Acad Sci USA 2013; 110: 18274-18278
19. Raineki C, Cortes MR, Belnoue L, Sullivan RM. Effects of early-life abuse differ across development: infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala. J Neurosci 2012; 32: 7758-7765
20. Baram TZ, Davis EP, Obenaus A, Sandman CA, Small SL, Solodkin A et al. Fragmentation and unpredictability of early-life experience in mental disorders. Am J Psychiatry 2012; 169: 907-915
21. Rilling JK, Young LJ. The biology of mammalian parenting and its effect on offspring social development. Science 2014; 345: 771-776
22. Ivy AS, Rex CS, Chen Y, Dube C, Maras PM, Grigoriadis De et al. Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J Neurosci 2010; 30: 13005-13015
23. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7: 847-854
24. Ryan ND, Puig-Antich J, Ambrosini P, Rabinovich H, Robinson D, Nelson B et al. The clinical picture of major depression in children and adolescents. Arch Gen Psychiatry 1987; 44: 854-861
25. Dym CT, Pinhas A, Robak M, Sclafani A, Bodnar RJ. Genetic variance contributes to dopamine receptor antagonist-induced inhibition of sucrose intake in inbred and outbred mouse strains. Brain Res 2009; 1257: 40-52
26. Kraft TT, Huang D, Natanova E, Lolier M, Yakubov Y, La Magna S et al. Dopamine D1 and opioid receptor antagonist-induced reductions of fructose and saccharin intake in BALB/c and SWR inbred mice. Pharmacol Biochem Behav 2015; 131: 13-18
27. Muscat R, Willner P. Effects of dopamine receptor antagonists on sucrose consumption and preference. Psychopharmacology (Berl) 1989; 99: 98-102
28. Siviy SM, Crawford CA, Akopian G, Walsh JP. Dysfunctional play and dopamine physiology in the Fischer 344 rat. Behav Brain Res 2011; 220: 294-304
29. Siviy SM, Panksepp J. In search of the neurobiological substrates for social playfulness in mammalian brains. Neurosci Biobehav Rev 2011; 35: 1821-1830
30. Trezza V, Baarendse PJ, Vanderschuren LJ. The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci 2010; 31: 463-469
31. Vanderschuren LJ, Niesink RJ, Van Ree JM. The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 1997; 21: 309-326
32. Berns GS, McClure SM, Pagnoni G, Montague PR. Predictability modulates human brain response to reward. J Neurosci 2001; 21: 2793-2798
33. Rutledge RB, Skandali N, Dayan P, Dolan RJ. A computational and neural model of momentary subjective well-being. Proc Natl Acad Sci USA 2014; 111: 12252-12257
34. Pena CJ, Neugut YD, Calarco CA, Champagne FA. Effects of maternal care on the development of midbrain dopamine pathways and reward-directed behavior in female offspring. Eur J Neurosci 2014; 39: 946-956
35. Voorn P, Kalsbeek A, Jorritsma-Byham B, Groenewegen HJ. The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience 1988; 25: 857-887
36. Ventura R, Coccurello R, Andolina D, Latagliata EC, Zanettini C, Lampis V et al. Postnatal aversive experience impairs sensitivity to natural rewards and increases susceptibility to negative events in adult life. Cereb Cortex 2013; 23: 1606-1617
37. Brunson KL, Kramar E, Lin B, Chen Y, Colgin LL, Yanagihara TK et al. Mechanisms of late-onset cognitive decline after early-life stress. J Neurosci 2005; 25: 9328-9338
38. Molet J, Maras PM, Avishai-Eliner S, Baram TZ. Naturalistic rodent models of chronic early-life stress. Dev Psychobiol 2014; 56: 1675-1688
39. Ivy AS, Brunson KL, Sandman C, Baram TZ. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for earlylife stress. Neuroscience 2008; 154: 1132-1142
40. Papp M, Willner P, Muscat R. An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology (Berl) 1991; 104: 255-259
41. Panksepp J, Siviy S, Normansell L. The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev 1984; 8: 465-492
42. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th edn., American Psychiatric Publishing: Washington, DC, USA, 2013
43. Romer Thomsen K, Whybrow PC, Kringelbach ML. Reconceptualizing anhedonia: novel perspectives on balancing the pleasure networks in the human brain. Front Behav Neurosci 2015; 9: 49
44. Mikulecka A, Subrt M, Parizkova M, Mares P, Kubova H. Consequences of early postnatal benzodiazepines exposure in rats. II. Social behavior. Front Behav Neurosci 2014; 8: 169
45. Vanderschuren LJ, Niesink RJ, Spruijt BM, Van Ree JM. Influence of environmental factors on social play behavior of juvenile rats. Physiol Behav 1995; 58: 119-123
46. Varlinskaya EI, Spear LP. Social interactions in adolescent and adult Sprague- Dawley rats: impact of social deprivation and test context familiarity. Behav Brain Res 2008; 188: 398-405
47. Porsolt RD, Le Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977; 266: 730-732
48. Rees SL, Panesar S, Steiner M, Fleming AS. The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm Behav 2004; 46: 411-419
49. Eghbal-Ahmadi M, Avishai-Eliner S, Hatalski CG, Baram TZ. Differential regulation of the expression of corticotropin-releasing factor receptor type 2 (CRF2) in hypothalamus and amygdala of the immature rat by sensory input and food intake. J Neurosci 1999; 19: 3982-3991
50. Suchecki D, Rosenfeld P, Levine S. Maternal regulation of the hypothalamicpituitary- adrenal axis in the infant rat: the roles of feeding and stroking. Brain Res Dev Brain Res 1993; 75: 185-192
51. Stanton ME, Levine S. Inhibition of infant glucocorticoid stress response: specific role of maternal cues. Dev Psychobiol 1990; 23: 411-426
52. Aisa B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 2007; 32: 256-266
53. Colorado RA, Shumake J, Conejo NM, Gonzalez-Pardo H, Gonzalez-Lima F. Effects of maternal separation, early handling, and standard facility rearing on orienting and impulsive behavior of adolescent rats. Behav Processes 2006; 71: 51-58
54. Hill RA, Klug M, Kiss Von Soly S, Binder MD, Hannan AJ, Van den Buuse M. Sexspecific disruptions in spatial memory and anhedonia in a 'two hit' rat model correspond with alterations in hippocampal brain-derived neurotrophic factor expression and signaling. Hippocampus 2014; 24: 1197-1211
55. Kundakovic M, Lim S, Gudsnuk K, Champagne FA. Sex-specific and straindependent effects of early life adversity on behavioral and epigenetic outcomes. Front Psychiatry 2013; 4: 78
56. Matthews K, Wilkinson LS, Robbins TW. Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiol Behav 1996; 59: 99-107
57. Michaels CC, Holtzman SG. Neonatal stress and litter composition alter sucrose intake in both rat dam and offspring. Physiol Behav 2006; 89: 735-741
58. Michaels CC, Holtzman SG. Enhanced sensitivity to naltrexone-induced drinking suppression of fluid intake and sucrose consumption in maternally separated rats. Pharmacol Biochem Behav 2007; 86: 784-796
59. Shalev U, Kafkafi N. Repeated maternal separation does not alter sucrose-reinforced and open-field behaviors. Pharmacol Biochem Behav 2002; 73: 115-122
60. Dimatelis JJ, Stein DJ, Russell VA. Behavioral changes after maternal separation are reversed by chronic constant light treatment. Brain Res 2012; 1480: 61-71
61. Lee JH, Kim HJ, Kim JG, Ryu V, Kim BT, Kang DW et al. Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 2007; 58: 32-39
62. Benekareddy M, Vadodaria KC, Nair AR, Vaidya VA. Postnatal serotonin type 2 receptor blockade prevents the emergence of anxiety behavior, dysregulated stress-induced immediate early gene responses, and specific transcriptional changes that arise following early life stress. Biol Psychiatry 2011; 70: 1024-1032
63. Tang AC, Reeb-Sutherland BC, Romeo RD, McEwen BS. On the causes of early life experience effects: evaluating the role of mom. Front Neuroendocrinol 2014; 35: 245-251
64. Nishi M, Horii-Hayashi N, Sasagawa T. Effects of early life adverse experiences on the brain: implications from maternal separation models in rodents. Front Neurosci 2014; 8: 166
65. Evans GW, Gonnella C, Marcynyszyn LA, Gentile L, Salpekar N. The role of chaos in poverty and children's socioemotional adjustment. Psychol Sci 2005; 16: 560-565
66. Marder E, Goaillard JM. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 2006; 7: 563-574
67. Woo CC, Hingco EE, Taylor GE, Leon M. Exposure to a broad range of odorants decreases cell mortality in the olfactory bulb. Neuroreport 2006; 17: 817-821
68. Crone EA, Dahl RE. Understanding adolescence as a period of social-affective engagement and goal flexibility. Nat Rev Neurosci 2012; 13: 636-650