Environmental enrichment models a naturalistic form of maternal separation and shapes the anxiety response patterns of offspring

Psychoneuroendocrinology

Volumn 52, Issue 1, 2015, Pages 153-167

  Connors, E J ^a   Migliore, M M ^a   Pillsbury, S L ^a   Shaik, A N ^a   Kentner, A C ^a  

^a MASSACHUSETTS COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

Author keywords

Anxiety; Enrichment; GABA; GLUR1; Glutamate; Maternal care; Prefrontal cortex; Social housing

Indexed keywords

4 AMINOBUTYRIC ACID; CORTICOSTERONE; GLUTAMATE RECEPTOR 1; GLUTAMIC ACID; SEROTONIN; AMPA RECEPTOR; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; EMOTIONAL STABILITY; ENVIRONMENTAL ENRICHMENT; EXPLORATORY BEHAVIOR TEST; FEMALE; GROWTH CURVE; HIPPOCAMPUS; LIGHT DARK TEST; MALE; MATERNAL BEHAVIOR; MATERNAL DEPRIVATION; MOTHER CHILD RELATION; NONHUMAN; OPEN ARMS TEST; PREFRONTAL CORTEX; PROGENY; RAT; SOCIAL INTERACTION; ANIMAL; ENVIRONMENT; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SEX DIFFERENCE; SOCIAL BEHAVIOR; SPRAGUE DAWLEY RAT;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; ENVIRONMENT; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MALE; MATERNAL BEHAVIOR; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SEX FACTORS; SOCIAL BEHAVIOR;

EID: 84922610866     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.10.021     Document Type: Article

References (72)

1. Ábrahám I.M., Kovács K.J. Postnatal handling alters the activation of stress-related neuronal circuitries. Eur. J. Neurosci. 2000, 12:3008-3014.
2. Anda R.F., Felittie V.J., Bremner J.D., Walker J.D., Whitefield C., Perry B.D., Dube S.R., Giles W.H. The enduring effects of abuse and related adverse experiences in childhood: a convergence of evidence from neurobiology and epidemiology. Eur. Archiv. Psychiatry Clin. Neurosci. 2008, 256:174-186.
3. Arbourelius L., Eklund M.B. Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle aged female rats. Neuroscience 2007, 145:738-750.
4. Baldini S., Restani L., Baroncelli L., Coltelli M., Franco R., Cenni M.C., Maffei L., Berardi N. Enriched early life experiences reduce adult anxiety-like behavior in rats: a role for insulin-like growth factor 1. J. Neurosci. 2013, 33:11715-11723.
5. Beauquis J., Roig P., De Nicola A.F., Saravia F. Short-term environmental enrichment enhances adult neuro-genesis, vascular network and dendritic complexity in the hippocampus of type 1 diabetic mice. PLoS ONE 2010, 5:e13993.
6. Bi L.-L., Wang J., Luo Z.Y., Chen S.-P., Geng F., Chen Y., Li S.-J., Yuan C., Lin S., Goa T.-M. Enhanced excitability in the infralimbic cortex produces anxiety-like behaviors. Neuropharmacology 2013, 72:148-156.
7. Boggiano M.M., Cavigelli S.A., Dorsey J.R., Kelley C.E., Ragan C.M., Chandler-Laney P.C. Effect of a cage divider permitting social stimuli on stress and food intake in rats. Physiol. Behav. 2008, 95:222-228.
8. Bulfin L.J., Clarke M.A., Buller K.M., Spencer S.J. Anxiety and hypothalamic-pituitary-adrenal axis responses to psychological stress are attenuated in male rats made lean by large litter rearing. Psychoneuroendocrinology 2011, 36:1080-1091.
9. Brambilla P., Perez J., Barale F., Schettini G., Soares J.C. GABAergic dysfunction in mood disorders. Mol. Psychiatry 2003, 8:721-737.
10. A and central benxodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 2000, 22:219-229.
11. Cameron N.M., Champagne F.A., Parent C., Fish E.W., Ozaki-Kuroda K., Meaney M.J. The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci. Biobehav. Rev. 2005, 29:843-865.
12. Cancedda L., Putignano E., Sale A., Berardi N., Maffei L. Acceleration of visual system development by environmental enrichment. J. Neurosci. 2004, 24:4840-4848.
13. Champagne F.A. Early adversity and developmental outcomes: interaction between genetics, epigenetics, and social experiences across the lifespan. Perspect. Psychol. Sci. 2010, 5:564-574.
14. Charney D.S., Deutch A. A functional neuroanatomy of anxiety and fear: implications for the pathophysiology and treatment of anxiety disorders. Crit. Rev. Neurol. 1996, 10:419-446.
15. Connors E.J., Shaik A.N., Migliore M.M., Kentner A.C. Environmental enrichment mitigates the sex-specific effects of gestational inflammation on social engagement and the hypothalamic pituitary adrenal axis-feedback system. Brain Behav. Immun. 2014, 42:178-190.
16. Connors E.J., Konkle A.T.M., Kentner A.C. Differential effects of environmental enrichment, social housing and isolation on maternal care and juvenile offspring behavior. Soc. Neurosci. 2013, Online.
17. Crawley J.N., Gerfen C.R., Rogawski M.A., Sibley D.R., Skolnick P., Wray S. Short Protocols in Neuroscience: Systems and Behavioral Methods 2007, John Wiley and Sons, Inc., Hoboken, NJ.
18. Croft A.P., O'Callaghan M.J., Shaw S.G., Connolly G., Jacquot C., Little H.J. Effects of minor laboratory procedures, adrenalectomy, social defear or acute alcohol on regional brain concentrations of corticosterone. Brain Res. 2008, 1238:12-22.
19. Cymerblit-Sabba A., Lasri T., Gruper M., Aga-Mizrachi S., Zubedat S., Avital A. Prenatal Enriched Environment improves emotional and attentional reactivity to adulthood stress. Behav. Brain Res. 2013, 241:185-190.
20. D'Andrea I., Gracci F., Alleva E., Branchi I. Early social enrichment provided by communal nest increases resilience to depression-like behavior more in female than in male mice. Behav. Brain Res. 2010, 215:71-76.
21. Dias G.P., Bevilagua M.C., da Luz A.C., Fleming R.L., de Carvalho L.A., Cocks G., Gardino P.F. Hippocampal biomarkers of fear memory in an animal model of generalized anxiety disorder. Behav. Brain Res. 2014, 263:34-45.
22. dos Santos L., de Andrade T.G.C.S., Graeff F.G. Social separation and diazepam withdrawal increase anxiety in the elevated plus-maze and serotonin turnover in the median raphe and hippocampus. J. Psychopharmacol. (Oxf.) 2010, 25:725-731.
23. Elliott B.M., Grunberg N.E. Effects of social and physical enrichment on open field activity differ in male and female Sprague-Dawley rats. Behav. Brain Res. 2005, 165:187-196.
24. Fernandes C., Gonzalez M.I., Wilson C.A., File S.E. Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol. Biochem. Behav. 1999, 64:731-738.
25. Feldman R., Gordon I., Influs M., Gutbir T., Ebstein R. Parental oxytocin and early caregiving jointly shape children's oxytocin response and social reciprocity. Neuropsychopharmacology 2013, 38:1154-1162.
26. Filaretova L., Morozova O., Laszlo F., Morschl E., Zelena D. Does chronic stress enhance the risk of diseases?. Endocr. Regul. 2013, 47:177-188.
27. Francis D.D., Champagne F.A., Liu D., Meaney M.J. Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann. N. Y. Acad. Sci. 1999, 896:66-84.
28. Fréchette M., Rennie K., Pappas B.A. Developmental fore-brain cholinergic lesion and environmental enrichment: behaviour, CA1 cytoarchitecture and neurogenesis. Brain Res. 2009, 1252:172-182.
29. Gabriel A.F., Paoletti G., Della Seta D., Panelli R., Marcus M.A.E., Farabollini F., Carli G., Joosten E.A.J. Enriched environment and the recovery from inflammatory pain: social versus physical aspects and their interaction. Behav. Brain Res. 2010, 208:90-95.
30. Garrido P., de Blas M., Del Arco A., Segovia G., Mora F. Aging increases basal but not stress-induced levels of corticosterone in the brain of the awake rat. Neurobiol. Aging 2012, 33:375-382.
31. Girbovan C., Plamondon H. Environmental enrichment in female rodents: considerations in the effects on behaviour and biochemical markers. Behav. Brain Res. 2013, 253:178-190.
32. Gracceva G., Venerosi A., Santucci D., Calamandrei G., Ricceri L. Early social enrichment affects responsiveness to different social cues in female mice. Behav. Brain Res. 2009, 196:304-309.
33. Haller J., Bakos N. Stress-induced social avoidance: a new model of stress-induced anxiety?. Physiol. Behav. 2002, 77:327-332.
34. Hasler G., van der Veen J.W., Grillon C., Drevets W., Shen J. Effect of acute psychological stress on prefrontal GABA concentration determined by proton magnetic resonance spectroscopy. Am. J. Psychiatry 2010, 167:1226-1231.
35. Hermes G., Nanxin L., Duman C., Duman R. Post-weaning chronic social isolation produces profound behavioral dysregulation with decreases in prefrontal cortex synaptic-associated protein expression in female rats. Physiol. Behav. 2011, 104:354-359.
36. Howell D.C. Statistical Methods for Psychology 2002, Belmont, Duxbury Press. 5th ed.
37. Huang F.L., Huang K.P., Wu J., Boucheron C. Environmental enrichment enhances neurogranin expression and hippocampal learning and memory but fails to rescue the impairments of neurogranin null mutant mice. J. Neurosci. 2006, 26:6230-6237.
38. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
39. Koh S., Magid R., Chung H., Stine C.D., Wilson D.N. Depressive behavior and selective down-regulation of serotonin receptor expression after early-life seizures: reversal by environmental enrichment. Epilepsy Behav. 2007, 10:26-31.
40. Konkle A.T.M., Kentner A.C., Baker S.L., Stewart A., Bielajew C. Environmental-enrichment-related variations in behavioral, biochemical, and physiologic responses of Sprague-Dawley and Long Evans rats. J. Am. Assoc. Lab. Anim. Sci.: JAALAS 2010, 49(4):427-436.
41. Korgan A.C., Green A.D., Perrot T.S., Esser M.J. Limbic system activation is affected by prenatal predator exposure and postnatal environmental enrichment and further moderated by dam and sex. Behav. Brain Res. 2014, 259:106-118.
42. Kumpfer K.L., Trait C.M. Family Skills Training for Parents and Children 2000, US Department of Justice, Office of Justice Programs, Office of Juvenile Justice and Delinquency Prevention, Washington, DC.
43. Latham N., Mason G. Frustration and preservation in stereotypic captive animals: is a taste of enrichment worse than none at all?. Behav. Brain Res. 2010, 211:96-104.
44. Leal-Galicia P., Castaneda-Bueno M., Quiroz-Baez R., Arias C. Long-term exposure to environmental enrichment since youth prevents recognition memory decline and increases synaptic plasticity markers in aging. Neurobiol. Learn. Mem. 2008, 90:511-518.
45. Leger M., Paizanis E., Dzahini K., Quiedeville A., Bouet V., Cassel J.C., Freret T., Schumann-Bard P., Boulouard M. Environmental enrichment duration differentially affects behavior and neuroplasticity in adult mice. Cereb. Cortex. 2014, (in press). 10.1093/cercor/bhu119.
46. Magariños A.M., McWewn B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 1995, 69:89-98.
47. Martin J.R., Bättig K. Exploratory behavior of rats at oestrus. Anim. Behav. 1980, 3:900-905.
48. Ogawa T., Kuwagata M., Hori Y., Shioda S. Valproate-induced developmental neurotoxicity is affected by maternal conditions including shipping stress and environmental change during early pregnancy. Toxicol. Lett. 2007, 174:18-24.
49. Pellis S.M., Field E.F., Smith L.K., Pellis V.C. Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neurosci. Biobehav. Rev. 1997, 21:105-120.
50. Peña Y., Prunell M., Rotllant D., Armario A., Escorihuela R.M. Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology 2009, 34:1390-1404.
51. Pickering C., Gustafsson L., Cebere A., Nylander I., Liljequist S. Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res. 2006, 1099:101-108.
52. Quidé Y., Witteveen A.B., El-Hage W., Veltman D.J., Olff M. Differences between effects of psychological versus pharmacological treatments on functional and morphological brain alternations in anxiety disorders and major depressive disorder: a systematic review. Neurosci. Biobehav. Rev. 2012, 36:626-644.
53. Ravenelle R., Byrnes E.M., Byrnes J.J., McInnis C., Park J.H., Donaldson S.T. Environmental enrichment effects on the neurobehavioral profile of selective outbred trait anxiety rats. Behav. Brain Res. 2013, 252:49-57.
54. Rosenfeld A., Weller A. Behavioral effects of environmental enrichment during gestation in WKY and Wistar rats. Behav. Brain Res. 2012, 233:245-255.
55. Sale A., Putignano E., Cancedda L., Landi S., Cirulli F., Berardi N., Maffei L. Enriched environment and acceleration of visual system development. Neuropharmacology 2004, 47:649-660.
56. Sanacora G., Treccani G., Popoli M. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 2012, 62:63-77.
57. Schneider T., Turczak J., Przewłocki R. Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: issues for a therapeutic approach in autism. Neuropsychopharmacology 2006, 31(1):36-46.
58. Segovia G., Yagüe A.G., García-Verugo J.M., Mora F. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res. Bull. 2006, 70:8-14.
59. Spencer S.J., Tilbrook A. Neonatal overfeeding alters adult anxiety and stress responsiveness. Psychoneuroendocrine 2009, 34:1133-1143.
60. Sustková-Fiserová M., Vávrová J., Krsiak M. Brain levels of GABA, glutamate and aspartate in sociable, aggressive and timid mice: an in vivo microdialysis study. Neuro Endorcinol. Lett. 2009, 30:79-84.
61. Vandershuren L.J.M.J., Niesink R.J.M., Spruijt B.M., Van Ree J.M. Influence of environmental factors on social play behavior of juvenile rats. Physiol. Behav. 1995, 58:119-123.
62. Venzala E., Garcia-Garcia A.L., Elizalde N., Tordera R.M. Social vs. environmental stress models of depression from a behavioural and neurochemical approach. Eur. J. Neuropsychopharmacol. 2013, 23:697-708.
63. Vivinetto A.L., Suárez M.M., Rivarola M.A. Neurobiological effects of neonatal maternal separation and post-weaning environmental enrichment. Behav. Brain Res. 2013, 240:110-118.
64. Welberg L., Thrivikraman K.V., Plotsky P.M. Combined pre- and postnatal environmental enrichment programs the HPA axis differentially in male and female rats. Psychoneuroendocrinology 2006, 31(5):553-564.
65. Wiener S.G., Levine S. Perinatal malnutrition and early handling: interactive effects on the development of the pituitary-adrenal system. Dev. Psychobiol. 1978, 11:335-352.
66. Wiley J.L., Evans R.L. To breed or not to breed? Empirical evaluation of drug effects in adolescent rats. Int. J. Dev. Neurosci. 2009, 27:9-20.
67. Wincott C.M., Abera S., Vunck S.A., Tirko N., Choi Y., Titcombe R.T., et al. cGMP-dependent protein kinase type II knockout mice exhibit working memory impairments, decreased repetitive behavior, and increased-anxiety-like traits. Neurobiol. Learn. Memory 2014, 114:32-39.
68. Wise C.D., Berger B.D., Stein L. Benzodiazepines: anxiety-reducing activity by reduction of serotonin turnover in the brain. Science 1972, 4044:180-183.
69. Woo C.C., Leon M. Environmental enrichment as an effective treatment for autism: a randomized controlled trial. Behav. Neurosci. 2013, 27(4):487-497.
70. Workman J.L., Fonken L.K., Gusfa J., Kassouf K.M., Nelson R.J. Post-weaning environmental enrichment alters affective responses and interacts with behavioral testing to alter nNos immunoreactivity. Pharmacol. Biochem. Behav. 2011, 100:25-32.
71. Xue X., Shai S., Li M., Shao F., Wang W. Maternal separation induces alterations of serotonergic system in different aged rats. Brain Res. Bull. 2013, 95:15-20.
72. Yuen E.Y., Liu W., Karatsoreos I.N., Feng J., McEwen B.S., Yan Z. Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14075-14079.