Early maternal separation has mild effects on cardiac autonomic balance and heart structure in adult male rats

Stress

Volumn 15, Issue 4, 2012, Pages 457-470

  Trombini, M ^a   Hulshof, H J ^b   Graiani, G ^a   Carnevali, L ^a   Meerlo, P ^b   Quaini, F ^a   Sgoifo, A ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Biological rhythms; Heart rate variability; Heart remodeling; Maternal separation; Parasympathetic nervous system; Restraint

Indexed keywords

ATENOLOL; SCOPOLAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; HEART AUTOMATICITY; HEART HYPERTROPHY; HEART MUSCLE FIBROSIS; HEART RATE VARIABILITY; HEART RHYTHM; HEART STRESS; IMMOBILIZATION STRESS; MALE; MATERNAL DEPRIVATION; NONHUMAN; PARASYMPATHETIC FUNCTION; PRIORITY JOURNAL; RAT; SINUS NODE;

ANIMALS; ANIMALS, NEWBORN; ATENOLOL; AUTONOMIC NERVOUS SYSTEM; CIRCADIAN RHYTHM; HEART; HEART RATE; MALE; MATERNAL DEPRIVATION; MYOCARDIUM; RATS; RATS, WISTAR; RESTRAINT, PHYSICAL; SCOPOLAMINE HYDROBROMIDE; STRESS, PSYCHOLOGICAL;

EID: 84861860822     PISSN: 10253890     EISSN: 16078888     Source Type: Journal    
DOI: 10.3109/10253890.2011.639414     Document Type: Article

References (68)

1. Aisa B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ. 2007. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32: 256-266.
2. Anversa P, Olivetti G, Loud AV. 1980. Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. I. Hypertrophy, hyperplasia, and binucleation of myocytes. Circ Res 46(4):495-502.
3. Aubert AE, Ramaekers D, Beckers F, Breem R, Denef C, Van der Werf F, Ector H. 1999. The analysis of heart rate variability in unrestrained rats. Validation of method and results. Comp Met Program Biomed 60:197-213.
4. Beltrami CA, Finato N, Rocco M, Feruglio GA, Puricelli C, Cigola E, Quaini F, Sonnenblick EH, Olivetti G, Anversa P. 1994. Structural basis of end-stage failure in ischemic cardiomyopathy in humans. Circulation 89:151-163.
5. Brook RD, Julius S. 2000. Autonomic imbalance, hypertension and cardiovascular risk. Am J Hypertens 13:112S-122S.
6. Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, de Kloet ER, Joels M, Krugers H. 2008. Maternal care and hippocampal plasticity: Evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci 28: 6037-6045.
7. Chess GF, Tam RMK, Calarescu FR. 1975. Influence of cardiac neural inputs on rhythmic variations of heart period in the cat. Am J Physiol 228:775-780.
8. Chiladakis JA, Pashalis A, Patsouras N, Manolis AS. 2001. Autonomic patterns preceding and following accelerated idioventricular rhythm in acute myocardial infarction. Cardiology 96:24-31.
9. Cirulli F, Francia N, Berry A, Aloe L, Alleva E, Suomi SJ. 2009. Early life stress as a risk factor for mental health: Role of neurotrophins from rodents to non-human primates. Neurosci Biobehav Rev 33:573-585.
10. Claycomb WC. 1976. Biochemical aspects of cardiac muscle differentiation. Possible control of deoxyribonucleic acid synthesis and cell differentiation by adrenergic innervation and cyclic adenosine 30:50-monophosphate. J Biol Chem 251(19): 6082-6089.
11. Costoli T, Bartolomucci A, Graiani G, Stilli D, Laviola G, Sgoifo A. 2004. Effects of chronic psychosocial stress on cardiac autonomic responsiveness and myocardial structure in mice. Am J Physiol Heart Circ Physiol 286:H2133-H2140.
12. Dodge HT, BaxleyWA. 1969. Left ventricular volume and mass and their significance in heart disease. Am J Cardiol 23:528-537.
13. Dong M, Giles WH, Felitti VJ, Dube SR, Williams JE, Chapman DP, Anda RF. 2004. Insights into casual pathways for ischemic heart disease: Adverse childhood experiences study. Circulation 110:1761-1766.
14. Eckeberg DL. 1991. Sympathovagal balance: A critical appraisal. Circulation 96(9):3224-3232.
15. Ewing DJ, Martin CN, Young RJ, Chrke BF. 1985. The value cardiovascular autonomic function tests: 10 years experience in diabetes. Diabetes Care 8(5):491-498.
16. Faturi CB, Tiba PA, Kawakami SE, Catallani B, Kerstens M, Suchecki D. 2010. Disruptions of the mother-infant relationship and stress-related behaviours: Altered corticosterone secretion does not explain everything. Neurosci Biobehav Rev 34(6):821-834.
17. Francis D, Diorio J, Liu D, Meaney MJ. 1999. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155-1158.
18. Gluckman PD, Hanson MA, Beedle AS. 2007. Early life events and their consequences for latter disease: A life history and evolutionary perspective. Am J Hum Biol 19:1-19.
19. Heim C, Nemeroff CB. 2001. The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biol Psychiatry 49:1023-1039.
20. Heiming RS, Jansen F, Lewejohann L, Kaiser S, Schmitt A, Lesch KP, Sachser N. 2009. Living in a dangerous world: The shaping of behavioral profile by early environment and 5-HTT genotype. Front Behav Neurosci 3(26):1-11.
21. Hopkins SF, McCutcheon EP, Wekstein DR. 1973. Postnatal changes in rat ventricular function. Circ Res 32:685-691.
22. Hulshof HJ, Novati A, Sgoifo A, Luiten PGM, den Boer JA, Meerlo P. 2011. Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effects on stress sensitivity and anxiety in adult Wistar rats. Behav Brain Res 216(2):552-560.
23. Huot RL, Plotsky PM, Lenox RH, McNamara RK. 2002. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res 950:52-63.
24. Husum H, Termeer E, Mathé AA, Bolwig TG, Ellenbroek BA. 2002. Early maternal deprivation alters hippocampal levels of neuropeptide Y and calcitonin-gene related peptide in adult rats. Neuropharmacology 42:798-806.
25. Japundzic N, Grichois ML, Zitoun P, Laude D, Elghozi JL. 1990. Spectral analysis of blood pressure and heart rate in conscious rats: Effects of autonomic blockers. J Auton Nerv Syst 30(2): 91-100.
26. Kaiser S, Sachser N. 2005. The effects of prenatal social stress on behaviour: Mechanism and function. Neurosci Biobehav Rev 29:283-294.
27. Kajstura J, Mansukhani M, ChengW, Krajewski S, Reed JC, Quaini F, Sonnenblick EH, Anversa P. 1995. Programmed cell death and expression of the protooncogene bcl-2 in myocytes during postnatal maturation of the heart. Exper Cell Res 219:110-121.
28. Kleiger RE, Bosner MS, Rottmans JN, Stein PK. 1993. Time domain measurements of heart rate variability. J AMB Mon 6: 1-18.
29. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E. 2011. Stress revisited: A critical evaluation of the stress concept. Neurosci Biobehav Rev 35:1291-1301.
30. La Rovere M, Bigger J, Marcus F, Mortara A, Schwartz P. 1998. Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. Lancet 351: 478-484.
31. Larson SK, Porges SW. 1982. The ontogeny of heart period patterning in the rat. Dev Psychobiol 15(6):519-528.
32. Lehmann J, Feldon J. 2000. Long-term biobehavioral effects of maternal separation in the rat: Consistent or confusing? Rev Neurosci 11:383-408.
33. Leon M, Croskerry PG, Smith GK. 1978. Thermal control of mother-young contact in rats. Physiol Behav 21:793-811.
34. Levine S. 1957. Infantile experience and resistance to physiological stress. Science 126:405-406.
35. Levine S. 2001. Primary social relationships influence the development of the hypothalamus-pituitary-adrenal axis in the rat. Physiol Behav 73(3):255-260.
36. Levine S, Haltmeyer GC, Karas GG, Denenberg VH. 1967. Physiological and behavioral effects of infantile stimulation. Physiol Behav 2:55-59.
37. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ. 1997. Maternal care, hippocampal glucorticoid receptors, and hypothalamicpituitary-adrenal responses to stress. Science 277:1659-1662.
38. Loria AS, D'angelo G, Pollock DM, Pollock JS. 2010a. Early life stress downregulates endhotelin receptor expression and enhances acute stress-mediated blood pressure responses in adult rats. Am J Physiol Integr Comp Physiol 299:R185-R191.
39. Loria AS, Pollock DM, Pollock JS. 2010b. Early life stress sensitizes to angiotensin II-induced hypertension and vascular inflammation in adult life. Hypertension 55(Part 2):494-499.
40. Maestri R, Milia AF, Salis MB, Graiani G, Lagrasta C, Monica M, CorradiD, Emanueli C, Madeddu P. 2003. Cardiac hypertrophy and microvascular deficit in kinin B2 receptor knockout mice. Hypertension 41:1151-1155.
41. Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C, Sharma S, Seckl JR, Plotsky PM. 1996. Early environmental regulation of forebrain glucocorticoid receptor gene expression: Implications for adrenocortical responses to stress. Dev Neurosci 18:49-72.
42. Meerlo P, Horvath KM, Nagy GM, Bohus B, Koolhaas JM. 1999. The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. J Neuroendocrinol 11(12): 925-933.
43. Mezzacappa ES, Kelsey RM, Katkin ES, Sloan RP. 2001. Vagal rebound and recovery from psychological stress. Psychosom Med 63(4):650-657.
44. Ngampramuan S, Baumert M, Beig MI, Kotchabhakdi N, Nalivaiko E. 2008. Activation of 5-HT1A receptors attenuates tachycardia induced by restraint stress in rats. Am J Physiol Integr Comp Physiol 294:R132-R141.
45. Olivetti G, Anversa P, Loud AV. 1980. Morphometric study of postnatal development in the left and right ventricular myocardium of the rat. II. Tissue composition, capillary growth, and sarcoplasmic alterations. Circ Res 46:503-512.
46. Plotsky PM, Meaney MJ. 1993. Early, postnatal experience alters hypothalamic corticotrophin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18:195-200.
47. Plotsky PM, Thrivikraman KV, Nemeroff CB, Caldji C, Sharma S, Meaney MJ. 2005. Long-term consequences of neonatal rearing on central corticotrophin- releasing factor system in adult male rat offspring. Neuropsychopharmacology 30:2192-2204.
48. Rots NY, de Jong J, Workel JO, Levine S, Cools AR, De Kloet ER. 1996. Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J Neuroendocrinol 8(7):501-506.
49. Sadoshima J, Izumo S. 1993. Molecular characterization of angiotensin II-induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ Res 73(3):413-423.
50. Safa-Tisseront V, Ponchon P, Laude D, Elghozi JL. 1998. Contribution of the autonomic nervous system to blood pressure and heart rate variability changes in early experimental hyperthyroidism. Eur J Pharmacol 352(2-3):247-255.
51. Sanders BJ, Anticevic A. 2007. Maternal separation enhances neuronal activation and cardiovascular responses to acute stress in borderline hypertensive rats. Behav Brain Res 183:25-30.
52. Sant'Ana JE, Pereira MG, Dias da Silva VJ, Dambró s C, Costa-Neto CM, Souza HC. 2011. Effect of the duration of daily aerobic physical training on cardiac autonomic adaptations. Auton Neurosci 159(1-2):32-37.
53. Schmidt I, Barone A, Carlisle HJ. 1986. Diurnal cycle of core temperature in huddling, week-old rat pups. Physiol Behav 37(1):105-109.
54. Sgoifo A, De Boer SF, Buwalda B, Korte-Bouws G, Tuma J, Bohus B, Zaagsma J, Koolhaas JM. 1998. Vulnerability to arrhythmias during social stress in rats with different sympathovagal balance. Am J Physiol 275:H460-H466.
55. Sgoifo A, Pozzato C, Costoli T, Manghi M, Stilli D, Ferrari PF, Ceresini G, Musso E. 2001. Cardiac autonomic responses to intermittent social conflict in rats. Physiol Behav 73:334-343.
56. Sgoifo A, Stilli D, Medici D, Gallo P, Aimi B, Musso E. 1996. Electrode positioning for reliable telemetry ECG recordings during social stress in unrestrained rats. Physiol Behav 60: 1397-1401.
57. Slotten HA, Kalinichev M, Hagan JJ, Marsden CA, Fone KC. 2006. Long-lasting changes in behavioral and neuroendocrine indices in the rat following neonatal maternal separation: Genderdependent effects. Brain Res 1097(1):123-132.
58. Souza HC, De Araujo JE, Martins-Pinge MC, Cozza IC, Martins-Dias DP. 2009. Nitric oxide synthesis blockade reduced the baroflex sensitivity in trained rats. Autonom Neurosci 158: 38-44.
59. Stein PK, Bosner MS, Kleiger RE, Conger BM. 1994. Heart rate variability: A measure of cardiac autonomic tone. Am Heart J 127:1376-1381.
60. Stern JM, Johnson SK. 1990. Ventral somatosensory determinants of nursing behavior in Norway rats. I. Effects of variations in the quality and quantity of pup stimuli. Physiol Behav 47:993-1011.
61. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology 1996. Heart rate variability. Standards of measurement, physiological interpretation and clinical use. Circulation 93:1043-1065.
62. Thayer JF, Friedman BH, Borkovec TD. 1996. Autonomic characteristics of generalized anxiety disorder and worry. Biol Psychiatry 39:255-266.
63. Thayer JF, Yamamoto SS, Brosschot JF. 2010. The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int J Cardiol 141:122-131.
64. Tucker DC. 1985. Components of functional sympathetic control of heart rate in neonatal rats. Am J Physiol 248(5 Pt 2): R601-R610.
65. Tucker DC, Bhatnagar RK, Johnson AK. 1984. Genetic and environmental influences on developing autonomic control of heart rate. Am J Physiol 246(4 Pt 2):R578-R586.
66. Tucker DC, Johnson AK. 1984a. Development of autonomic control of heart rate in genetically hypertensive and normotensive rats. Am J Physiol 246(4 Pt 2):R570-R577.
67. Tucker DC, Johnson AK. 1984b. Influence of neonatal handling on blood pressure, locomotor activity, and preweanling heart rate in spontaneously hypertensive and Wistar Kyoto rats. Dev Psychobiol 17(6):587-600.
68. Wigger A, Neumann ID. 1999. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 66(2):293-302.