Taurine 8 pp 121-134 | Cite as

Perinatal Taurine Exposure Programs Patterns of Autonomic Nerve Activity Responses to Tooth Pulp Stimulation in Adult Male Rats

  • Sawita Khimsuksri
  • J. Michael Wyss
  • Atcharaporn Thaeomor
  • Jarin Paphangkorakit
  • Dusit Jirakulsomchok
  • Sanya RoysommutiEmail author
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 775)


Perinatal taurine excess or deficiency influences adult health and disease, especially relative to the autonomic nervous system. This study tests the hypothesis that perinatal taurine exposure influences adult autonomic nervous system control of arterial pressure in response to acute electrical tooth pulp stimulation. Female Sprague–Dawley rats were fed with normal rat chow with 3% β-alanine (taurine depletion, TD), 3% taurine (taurine supplementation, TS), or water alone (control, C) from conception to weaning. Their male offspring were fed with normal rat chow and tap water throughout the experiment. At 8–10 weeks of age, blood chemistry, arterial pressure, heart rate, and renal sympathetic nerve activity were measured in anesthetized rats. Age, body weight, mean arterial pressure, heart rate, plasma electrolytes, blood urea nitrogen, plasma creatinine, and plasma cortisol were not significantly different among the three groups. Before tooth pulp stimulation, low- (0.3–0.5 Hz) and high-frequency (0.5–4.0 Hz) power spectral densities of arterial pressure were not significantly different among groups while the power spectral densities of renal sympathetic nerve activity were significantly decreased in TD compared to control rats. Tooth pulp stimulation did not change arterial pressure, heart rate, renal sympathetic nerve, and arterial pressure power spectral densities in the 0.3–4.0 Hz spectrum or renal sympathetic nerve firing rate in any group. In contrast, perinatal taurine imbalance disturbed very-low-frequency power spectral densities of both arterial pressure and renal sympathetic nerve activity (below 0.1 Hz), both before and after the tooth pulp stimulation. The power densities of TS were most sensitive to ganglionic blockade and central adrenergic inhibition, while those of TD were sensitive to both central and peripheral adrenergic inhibition. The present data indicate that perinatal taurine imbalance can lead to aberrant autonomic nervous system responses in adult male rats.


Arterial Pressure Power Spectral Density Sympathetic Nerve Nerve Activity Renal Sympathetic Nerve Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Arterial pressure




Electrical tooth pulp stimulation


Heart rate


High frequency


Low frequency


Mean arterial pressure


Renal sympathetic nerve activity




Taurine depletion


Taurine supplementation



This study was supported by a grant from the Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand and by the US National Institutes of Health (NIH) grants AT 00477 and NS057098 (JMW).


  1. Aerts L, Van Assche FA (2002) Taurine and taurine-deficiency in the perinatal period. J Perinat Med 30:281–286PubMedCrossRefGoogle Scholar
  2. Allen GV, Pronych SP (1997) Trigeminal autonomic pathways involved in nociception-induced reflex cardiovascular responses. Brain Res 754:269–278PubMedCrossRefGoogle Scholar
  3. Andrew D, Matthews B (2002) Properties of single nerve fibres that evoke blood flow changes in cat dental pulp. J Physiol 542:921–928PubMedCrossRefGoogle Scholar
  4. Brotman DJ, Golden SH, Wittstein IS (2007) The cardiovascular toll of stress. Lancet 370: 1089–1100PubMedCrossRefGoogle Scholar
  5. DiBona GF (2005a) Dynamic analysis of patterns of renal sympathetic nerve activity: implications for renal function. Exp Physiol 90:159–161PubMedCrossRefGoogle Scholar
  6. DiBona GF (2005b) Physiology in perspective: the wisdom of the body. Neural control of the kidney. Am J Physiol Regul Integr Comp Physiol 289:R633–R641PubMedCrossRefGoogle Scholar
  7. DiBona GF, Sawin LL (1999) Renal hemodynamic effects of activation of specific renal sympathetic nerve fiber groups. Am J Physiol 276:R539–R549PubMedGoogle Scholar
  8. Drummond PD (1995) Lacrimation induced by thermal stress in patients with a facial nerve lesion. Neurology 45:1112–1114PubMedCrossRefGoogle Scholar
  9. Franconi F et al (2004) Taurine administration during lactation modifies hippocampal CA1 neurotransmission and behavioural programming in adult male mice. Brain Res Bull 63:491–497PubMedCrossRefGoogle Scholar
  10. Furlan R, Piazza S, Dell’Orto S, Gentile E, Cerutti S, Pagani M, Malliani A (1993) Early and late effects of exercise and athletic training on neural mechanisms controlling heart rate. Cardiovasc Res 27:482–488PubMedCrossRefGoogle Scholar
  11. Godfrey KM, Barker DJ (2001) Fetal programming and adult health. Public Health Nutr 4: 611–624PubMedCrossRefGoogle Scholar
  12. Guyenet PG, Schreihofer AM, Stornetta RL (2001) Regulation of sympathetic tone and arterial pressure by the rostral ventrolateral medulla after depletion of C1 cells in rats. Ann N Y Acad Sci 940:259–269PubMedCrossRefGoogle Scholar
  13. Hanson MA, Gluckman PD (2008) Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol 102:90–93PubMedCrossRefGoogle Scholar
  14. Kemppainen P, Forster C, Handwerker HO (2001) The importance of stimulus site and intensity in differences of pain-induced vascular reflexes in human orofacial regions. Pain 91:331–338PubMedCrossRefGoogle Scholar
  15. Madden CJ, Sved AF (2003) Rostral ventrolateral medulla C1 neurons and cardiovascular regulation. Cell Mol Neurobiol 23:739–749PubMedCrossRefGoogle Scholar
  16. Malliani A, Lombardi F, Pagani M (1994) Power spectrum analysis of heart rate variability: a tool to explore neural regulatory mechanisms. Br Heart J 71:1–2PubMedCrossRefGoogle Scholar
  17. Montebugnoli L, Servidio D, Miaton RA, Prati C (2004) Heart rate variability: a sensitive parameter for detecting abnormal cardiocirculatory changes during a stressful dental procedure. J Am Dent Assoc 135:1718–1723PubMedGoogle Scholar
  18. Mozaffari MS, Roysommuti S, Wyss JM (1996) Contribution of the sympathetic nervous system to hypertensive response to insulin excess in spontaneously hypertensive rats. J Cardiovasc Pharmacol 27:539–544PubMedGoogle Scholar
  19. Ninomiya I, Irisawa A, Nisimaru N (1973) Nonuniformity of sympathetic nerve activity to the skin and kidney. Am J Physiol 224:256–264PubMedGoogle Scholar
  20. Ninomiya I, Irisawa H (1975) Non-uniformity of the sympathetic nerve activity in response to baroreceptor inputs. Brain Res 87:313–322PubMedCrossRefGoogle Scholar
  21. Pagani M et al (1984) Power spectral density of heart rate variability as an index of sympatho-vagal interaction in normal and hypertensive subjects. J Hypertens Suppl 2:S383–S385PubMedGoogle Scholar
  22. Parati G, Saul JP, Di RM, Mancia G (1995) Spectral analysis of blood pressure and heart rate variability in evaluating cardiovascular regulation. A critical appraisal. Hypertension 25:1276–1286PubMedCrossRefGoogle Scholar
  23. Persson PB, Stauss H, Chung O, Wittmann U, Unger T (1992) Spectrum analysis of sympathetic nerve activity and blood pressure in conscious rats. Am J Physiol 263:H1348–H1355PubMedGoogle Scholar
  24. Renno WM, Alkhalaf M, Mousa A, Kanaan RA (2008) A comparative study of excitatory and inhibitory amino acids in three different brainstem nuclei. Neurochem Res 33:150–159PubMedCrossRefGoogle Scholar
  25. Roysommuti S, Suwanich A, Jirakulsomchok D, Wyss JM (2009a) Perinatal taurine depletion increases susceptibility to adult sugar-induced hypertension in rats. Adv Exp Med Biol 643: 123–133PubMedCrossRefGoogle Scholar
  26. Roysommuti S, Suwanich A, Lerdweeraphon W, Thaeomor A, Jirakulsomchok D, Wyss JM (2009b) Sex dependent effects of perinatal taurine exposure on the arterial pressure control in adult offspring. Adv Exp Med Biol 643:135–144PubMedCrossRefGoogle Scholar
  27. Roysommuti S, Thaewmor A, Lerdweeraphon W, Khimsuksri S, Jirakulsomchok D, Schaffer SW (2011) Perinatal taurine exposure alters neural control of arterial pressure via the renin-angiotensin system but not estrogen in rats. Amino Acids 41:S84PubMedCrossRefGoogle Scholar
  28. Satoh-Kuriwada S, Sasano T, Date H, Karita K, Izumi H, Shoji N, Hashimoto K (2003) Centrally mediated reflex vasodilation in the gingiva induced by painful tooth-pulp stimulation in sympathectomized human subjects. J Periodontal Res 38:218–222PubMedCrossRefGoogle Scholar
  29. Schaller B (2004) Trigeminocardiac reflex. A clinical phenomenon or a new physiological entity? J Neurol 251:658–665PubMedCrossRefGoogle Scholar
  30. Sousa LO, Lindsey CJ (2009) Cardiovascular and baroreceptor functions of the paratrigeminal nucleus for pressor effects in non-anaesthetized rats. Auton Neurosci 147:27–32PubMedCrossRefGoogle Scholar
  31. Suge R, Hosoe N, Furube M, Yamamoto T, Hirayama A, Hirano S, Nomura M (2007) Specific timing of taurine supplementation affects learning ability in mice. Life Sci 81:1228–1234PubMedCrossRefGoogle Scholar
  32. Terada T, Hara K, Haranishi Y, Sata T (2011) Antinociceptive effect of intrathecal administration of taurine in rat models of neuropathic pain. Can J Anaesth 58:630–637PubMedCrossRefGoogle Scholar
  33. Thaeomor A, Wyss JM, Jirakulsomchok D, Roysommuti S (2010) High sugar intake via the renin-angiotensin system blunts the baroreceptor reflex in adult rats that were perinatally depleted of taurine. J Biomed Sci 17(Suppl 1):S30PubMedCrossRefGoogle Scholar
  34. Zhang S, Rattanatray L, McMillen IC, Suter CM, Morrison JL (2011) Periconceptional nutrition and the early programming of a life of obesity or adversity. Prog Biophys Mol Biol 106:307–314PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Sawita Khimsuksri
    • 1
    • 2
  • J. Michael Wyss
    • 3
  • Atcharaporn Thaeomor
    • 4
  • Jarin Paphangkorakit
    • 5
  • Dusit Jirakulsomchok
    • 1
  • Sanya Roysommuti
    • 1
    Email author
  1. 1.Department of Physiology, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand
  2. 2.Department of Oral Biology, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand
  3. 3.Department of Cell, Developmental and Integrative Biology, School of MedicineUniversity of Alabama at BirminghamBirminghamUSA
  4. 4.School of Physiology, Institute of ScienceSuranaree University of TechnologyNakhonratchasimaThailand
  5. 5.Department of Oral Biology, Faculty of DentistryKhon Kaen UniversityKhon KaenThailand

Personalised recommendations