Advertisement

Animal Models for the Study of Neurohumeral and Central Neural Control of the Cardiovascular System

  • David R. Gross
Chapter

Abstract

Studies investigating the integrative central control of the locomotor and cardiovascular system have mostly been conducted in rats. These studies have shown that control of cardiovascular responses is located in neurons in close proximity, if not overlapping or possibly identical to, neurons responsible for respiratory and locomotor control. In rats cardiorespiratory and locomotor centers have been identified in the periaqueductal gray (PAG), posterior hypothalamic area (PHA), nucleus tractus solitarius (NTS), rostral ventrolateral medulla (rVLM), and the cuneiform nucleus (CnF). Of these, the PH has been clearly identified as both a locomotor and cardiovascular center.1

The CnF, with the pedunculopontine nucleus, has been identified as the mesencephalic locomotor center.2,3 The spinal cord and the lateral tegmental field (LTF) have been identified as integration sites for cardiorespiratory and locomotor responses.4 Interestingly, exercise training induced attenuation of dendritic fields of neurons in the exercising rat model.1

Keywords

Carotid Body Nucleus Tractus Solitarius Sympathetic Outflow Medial Preoptic Area Nucleus Tractus Solitarius Neuron 
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.

References

  1. 1.
    Nelson AJ, Juraska JM, Musch TI, Iwamoto GA. Neuroplastic adaptations to exercise: Neuronal remodeling in cardiorespiratory and locomotor areas. J Appl Physiol. 2005;99:2312–2322.PubMedCrossRefGoogle Scholar
  2. 2.
    Plowey ED, Kramer JM, Beatty JA, Waldrop TG. In vivo electrophysiological responses of pedunculopontine neurons to static muscle contraction. Am J Physiol Regul Integr Comp Physiol. 2002;283:R1008–R1019.PubMedGoogle Scholar
  3. 3.
    Bedford TG, Loi PK, Crandall CC. A model of dynamic exercise: The decerebrate rat locomotor preparation. J Appl Physiol. 1992;72:121–127.PubMedGoogle Scholar
  4. 4.
    Kaufman MP, Forster HV. Reflexes controlling circulatory, ventilatory, and airway responses to exercise. In: Roweland LB, Shepherd JT, eds. Handbook of Physiology, Section 12: Exercise, Regulation and Integration of Multiple Systems. New York: Oxford University Press; 1996:381–446.Google Scholar
  5. 5.
    Iwamoto GA, Wappel SM, Fox GM, Buetow KA, Waldrop TG. Identification of diencephalic and brainstem cardiorespiratory areas activated during exercise. Brain Res. 1996;726:109–122.PubMedCrossRefGoogle Scholar
  6. 6.
    Ichiyama RM, Gilbert AB, Waldrop TG, Iwamoto GA. Changes in the exercise activation of diencephalic and brainstem cardiorespiratory areas after training. Brain Res. 2002;947:225–233.PubMedCrossRefGoogle Scholar
  7. 7.
    Nelson AJ, Iwamoto GA. Reversibility of exercise-induced dendritic attenuation in brain cardiorespiratory and locomotor areas following exercise detraining. J Appl Physiol. 2006;101:1243–1251.PubMedCrossRefGoogle Scholar
  8. 8.
    Bienkowski MS, Rinaman L. Noradrenergic inputs to the paraventricular hypothalamus contribute to hypothalamic-pituitary-adrenal axis and central fos activation in rats after acute systemic endotoxin exposure. Neuroscience. 2008;156:1093–1102.PubMedCrossRefGoogle Scholar
  9. 9.
    Varga T, Palkovits M, Usdin TB, Dobolyi A. The medial paralemniscal nucleus and its afferent neuronal connections in rat. J Comp Neurol. 2008;511:221–237.PubMedCrossRefGoogle Scholar
  10. 10.
    Ichiyama RM, Waldrop TG, Iwamoto GA. Neurons in and near insular cortex are responsive to muscular contraction and have sympathetic and/or cardiac-related discharge. Brain Res. 2004;1008:273–277.PubMedCrossRefGoogle Scholar
  11. 11.
    Vissing J, Iwamoto GA, Rybicki KJ, Galbo H, Mitchell JH. Mobilization of glucoregulatory hormones and glucose by hypothalamic locomotor centers. Am J Physiol. 1989;257:E722–E728.PubMedGoogle Scholar
  12. 12.
    Cai YL, Ma WL, Wang JQ, Li YQ, Li M. Excitatory pathways from the vestibular nuclei to the NTS and the PBN and indirect vestibulo-cardiovascular pathway from the vestibular nuclei to the RVLM relayed by the NTS. Brain Res. 2008;1240:96–104.PubMedCrossRefGoogle Scholar
  13. 13.
    Verberne AJ. Cuneiform nucleus stimulation produces activation of medullary sympathoexcitatory neurons in rats. Am J Physiol. 1995;268:R752–R758.PubMedGoogle Scholar
  14. 14.
    Choi DC, Furay AR, Evanson NK, et al. The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamic-pituitary-adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendocrinology. 2008;33:659–669.PubMedCrossRefGoogle Scholar
  15. 15.
    Stremel RW, Waldrop TG, Richard CA, Iwamoto GA. Cardiorespiratory responses to stimulation of the nucleus reticularis gigantocellularis. Brain Res Bull. 1990;24:1–6.PubMedCrossRefGoogle Scholar
  16. 16.
    Waldrop TG, Iwamoto GA. Point: Supraspinal locomotor centers do contribute significantly to the hyperpnea of dynamic exercise. J Appl Physiol. 2006;100:1077–1079.PubMedCrossRefGoogle Scholar
  17. 17.
    Xia CM, Shao CH, Xin L, et al. Effects of melatonin on blood pressure in stress-induced hypertension in rats. Clin Exp Pharmacol Physiol. 2008;35:1258–1264.PubMedCrossRefGoogle Scholar
  18. 18.
    Maximino JR, Ferrari MF, Coelho EF, Fior-Chadi DR. Time course analysis of tyrosine hydroxylase and angiotensinogen mRNA expression in central nervous system of rats submitted to experimental hypertension. Neurosci Res. 2006;55:292–299.PubMedCrossRefGoogle Scholar
  19. 19.
    Horiuchi J, McDowall LM, Dampney RA. Role of 5-HT(1A) receptors in the lower brainstem on the cardiovascular response to dorsomedial hypothalamus activation. Auton Neurosci. 2008;142:71–76.PubMedCrossRefGoogle Scholar
  20. 20.
    Maemura K, Takeda N, Nagai R. Circadian rhythms in the CNS and peripheral clock disorders: Role of the biological clock in cardiovascular diseases. J Pharmacol Sci. 2007;103:134–138.PubMedCrossRefGoogle Scholar
  21. 21.
    Verbalis JG. How does the brain sense osmolality? J Am Soc Nephrol. 2007;18:3056–3059.PubMedCrossRefGoogle Scholar
  22. 22.
    Swiatkowski K, Dellamano LM, Vissing J, Rybicki KJ, Kozlowski GP, Iwamoto GA. Differential effects from parapyramidal region and rostral ventrolateral medulla mediated by substance P. Am J Physiol. 1999;277:R1120–R1129.PubMedGoogle Scholar
  23. 23.
    Ruiz-Pesini P, Tome E, Balaguer L, Romano J, Yllera M. The projections to the medulla of neurons innervating the carotid sinus in the dog. Brain Res Bull. 1995;37:41–46.PubMedCrossRefGoogle Scholar
  24. 24.
    Iwamoto GA, Waldrop TG. Lateral tegmental field neurons sensitive to muscular contraction: A role in pressor reflexes? Brain Res Bull. 1996;41:111–120.PubMedCrossRefGoogle Scholar
  25. 25.
    Wei S, Lei M, Tong M, Ding J, Han Q, Xiao M. Acute baroreceptor unloading evokes fos expression in anesthetized rat brain. Brain Res Bull. 2008;76:63–69.PubMedCrossRefGoogle Scholar
  26. 26.
    Thomas CJ, McAllen RM, Salo LM, Woods RL. Restorative effect of atrial natriuretic peptide or chronic neutral endopeptidase inhibition on blunted cardiopulmonary vagal reflexes in aged rats. Hypertension. 2008;52:696–701.PubMedCrossRefGoogle Scholar
  27. 27.
    Ito K, Kimura Y, Hirooka Y, Sagara Y, Sunagawa K. Activation of rho-kinase in the brainstem enhances sympathetic drive in mice with heart failure. Auton Neurosci. 2008;142:77–81.PubMedCrossRefGoogle Scholar
  28. 28.
    Signolet IL, Bousquet PP, Monassier LJ. Improvement of cardiac diastolic function by long-term centrally mediated sympathetic inhibition in one-kidney, one-clip hypertensive rabbits. Am J Hypertens. 2008;21:54–60.PubMedCrossRefGoogle Scholar
  29. 29.
    Ono A, Kuwaki T, Kumada M, Fujita T. Differential central modulation of the baroreflex by salt loading in normotensive and spontaneously hypertensive rats. Hypertension. 1997;29:808–814.PubMedGoogle Scholar
  30. 30.
    Daly MD. Some reflex cardioinhibitory responses in the cat and their modulation by central inspiratory neuronal activity. J Physiol. 1991;439:559–577.PubMedGoogle Scholar
  31. 31.
    Alzoubi KH, Aleisa AM, Alkadhi KA. In vivo expression of ganglionic long-term potentiation in superior cervical ganglia from hypertensive aged rats. Neurobiol Aging. 2008 July 21 [Epub ahead of print].Google Scholar
  32. 32.
    Schultz HD, Li YL. Carotid body function in heart failure. Respir Physiol Neurobiol. 2007;157:171–185.PubMedCrossRefGoogle Scholar
  33. 33.
    Gross DR. Animal Models in Cardiovascular Research, 2nd Revised Edition. Boston, MA: Kluwer Academic; 1994.Google Scholar
  34. 34.
    Ma Y, Yang ZM, Kang YM. Brain renin-angiotensin-aldosterone system contributes to sympatho-excitation in heart failure. Sheng Li Ke Xue Jin Zhan. 2008;39:105–108.PubMedGoogle Scholar
  35. 35.
    Koganezawa T, Shimomura Y, Terui N. The role of the RVLM neurons in the viscero-sympathetic reflex: A mini review. Auton Neurosci. 2008;142:17–19.PubMedCrossRefGoogle Scholar
  36. 36.
    Iwamoto GA, Brtva RD, Waldrop TG. Cardiorespiratory responses to chemical stimulation of the caudal most ventrolateral medulla in the cat. Neurosci Lett. 1991;129:86–90.PubMedCrossRefGoogle Scholar
  37. 37.
    Campos RR, Carillo BA, Oliveira-Sales EB, et al. Role of the caudal pressor area in the regulation of sympathetic vasomotor tone. Braz J Med Biol Res. 2008;41:557–562.PubMedCrossRefGoogle Scholar
  38. 38.
    Yajima Y, Ito S, Komatsu K, Tsukamoto K, Matsumoto K, Hirayama A. Enhanced response from the caudal pressor area in spontaneously hypertensive rats. Brain Res. 2008;1227:89–95.PubMedCrossRefGoogle Scholar
  39. 39.
    Bauer RM, Iwamoto GA, Waldrop TG. Discharge patterns of ventrolateral medullary neurons during muscular contraction. Am J Physiol. 1990;259:R606–R611.PubMedGoogle Scholar
  40. 40.
    Pilowsky PM, Abbott SB, Burke PG, et al. Metabotropic neurotransmission and integration of sympathetic nerve activity by the rostral ventrolateral medulla in the rat. Clin Exp Pharmacol Physiol. 2008;35:508–511.PubMedCrossRefGoogle Scholar
  41. 41.
    Mandel DA, Schreihofer AM. Glutamatergic inputs to the CVLM independent of the NTS promote tonic inhibition of sympathetic vasomotor tone in rats. Am J Physiol Heart Circ Physiol. 2008;295:H1772–H1779.PubMedCrossRefGoogle Scholar
  42. 42.
    Nakamura T, Kawabe K, Sapru HN. Cold pressor test in the rat: Medullary and spinal pathways and neurotransmitters. Am J Physiol Heart Circ Physiol. 2008;295:H1780–H1787.PubMedCrossRefGoogle Scholar
  43. 43.
    Kashihara K, McMullan S, Lonergan T, Goodchild AK, Pilowsky PM. Neuropeptide Y in the rostral ventrolateral medulla blocks somatosympathetic reflexes in anesthetized rats. Auton Neurosci. 2008;142:64–70.PubMedCrossRefGoogle Scholar
  44. 44.
    Wang G, Milner TA, Speth RC, et al. Sex differences in angiotensin signaling in bulbospinal neurons in the rat rostral ventrolateral medulla. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1149–R1157.PubMedCrossRefGoogle Scholar
  45. 45.
    Liu D, Gao L, Roy SK, Cornish KG, Zucker IH. Role of oxidant stress on AT1 receptor expression in neurons of rabbits with heart failure and in cultured neurons. Circ Res. 2008;103:186–193.PubMedCrossRefGoogle Scholar
  46. 46.
    Alzamora AC, Santos RA, Campagnole-Santos MJ. Baroreflex modulation by angiotensins at the rat rostral and caudal ventrolateral medulla. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1027–R1034.PubMedCrossRefGoogle Scholar
  47. 47.
    Adams JM, McCarthy JJ, Stocker SD. Excess dietary salt alters angiotensinergic regulation of neurons in the rostral ventrolateral medulla. Hypertension. 2008;52:932–937.PubMedCrossRefGoogle Scholar
  48. 48.
    Patel D, Bohlke M, Phattanarudee S, Kabadi S, Maher TJ, Ally A. Cardiovascular responses and neurotransmitter changes during blockade of angiotensin II receptors within the ventrolateral medulla. Neurosci Res. 2008;60:340–348.PubMedCrossRefGoogle Scholar
  49. 49.
    Gao L, Wang WZ, Wang W, Zucker IH. Imbalance of angiotensin type 1 receptor and angiotensin II type 2 receptor in the rostral ventrolateral medulla: Potential mechanism for sympathetic overactivity in heart failure. Hypertension. 2008;52:708–714.PubMedCrossRefGoogle Scholar
  50. 50.
    Gao L, Wang W, Wang W, Li H, Sumners C, Zucker IH. Effects of angiotensin type 2 receptor overexpression in the rostral ventrolateral medulla on blood pressure and urine excretion in normal rats. Hypertension. 2008;51:521–527.PubMedCrossRefGoogle Scholar
  51. 51.
    Farnham MM, Li Q, Goodchild AK, Pilowsky PM. PACAP is expressed in sympathoexcitatory bulbospinal C1 neurons of the brain stem and increases sympathetic nerve activity in vivo. Am J Physiol Regul Integr Comp Physiol. 2008;294:R1304–R1311.PubMedCrossRefGoogle Scholar
  52. 52.
    Orer HS, Gebber GL, Barman SM. Role of serotonergic input to the ventrolateral medulla in expression of the 10-Hz sympathetic nerve rhythm. Am J Physiol Regul Integr Comp Physiol. 2008;294:R1435–R1444.PubMedCrossRefGoogle Scholar
  53. 53.
    Xia CM, Chen J, Wang J, et al. Differential expressions of nNOS and iNOS in the rostral ventrolateral medulla induced by electroacupuncture in acute myocardial ischemia rats. Sheng Li Xue Bao. 2008;60:453–461.PubMedGoogle Scholar
  54. 54.
    Powers-Martin K, Barron AM, Auckland CH, et al. Immunohistochemical assessment of cyclic guanosine monophosphate (cGMP) and soluble guanylate cyclase (sGC) within the rostral ventrolateral medulla. J Biomed Sci. 2008;15:801–812.PubMedCrossRefGoogle Scholar
  55. 55.
    Kung LC, Chan SH, Wu KL, Ou CC, Tai MH, Chan JY. Mitochondrial respiratory enzyme complexes in rostral ventrolateral medulla as cellular targets of nitric oxide and superoxide interaction in the antagonism of antihypertensive action of eNOS transgene. Mol Pharmacol. 2008;74:1319–1332.PubMedCrossRefGoogle Scholar
  56. 56.
    Ally A, Maher TJ. Endothelial NOS expression within the ventrolateral medulla can affect cardiovascular function during static exercise in stroked rats. Brain Res. 2008;1196:33–40.PubMedCrossRefGoogle Scholar
  57. 57.
    O’Leary KT, Loughlin SE, Chen Y, Leslie FM. Nicotinic acetylcholine receptor subunit mRNA expression in adult and developing rat medullary catecholamine neurons. J Comp Neurol. 2008;510:655–672.PubMedCrossRefGoogle Scholar
  58. 58.
    Hirooka Y. Role of reactive oxygen species in brainstem in neural mechanisms of hypertension. Auton Neurosci. 2008;142:20–24.PubMedCrossRefGoogle Scholar
  59. 59.
    Ma HJ, Cao YK, Liu YX, Wang R, Wu YM. Microinjection of resveratrol into rostral ventrolateral medulla decreases sympathetic vasomotor tone through nitric oxide and intracellular Ca2+ in anesthetized male rats. Acta Pharmacol Sin. 2008;29:906–912.PubMedCrossRefGoogle Scholar
  60. 60.
    Potts JT, Waldrop TG. Discharge patterns of somatosensitive neurons in the nucleus tractus solitarius of the cat. Neuroscience. 2005;132:1123–1134.PubMedCrossRefGoogle Scholar
  61. 61.
    Toney GM, Mifflin SW. Sensory modalities conveyed in the hindlimb somatic afferent input to nucleus tractus solitarius. J Appl Physiol. 2000;88:2062–2073.PubMedGoogle Scholar
  62. 62.
    Bantikyan A, Song G, Feinberg-Zadek P, Poon CS. Intrinsic and synaptic long-term depression of NTS relay of nociceptin- and capsaicin-sensitive cardiopulmonary afferents hyperactivity. Pflugers Arch. 2009;457:1147–1159.PubMedCrossRefGoogle Scholar
  63. 63.
    Andresen MC, Peters JH. Comparison of baroreceptive to other afferent synaptic transmission to the solitary tract nucleus. Am J Physiol Heart Circ Physiol. 2008;295:H2032–H2042.PubMedCrossRefGoogle Scholar
  64. 64.
    Yilmaz MS, Goktalay G, Millington WR, Myer BS, Cutrera RA, Feleder C. Lipopolysaccharide-induced hypotension is mediated by a neural pathway involving the vagus nerve, the nucleus tractus solitarius and alpha-adrenergic receptors in the preoptic anterior hypothalamic area. J Neuroimmunol. 2008;203:39–49.PubMedCrossRefGoogle Scholar
  65. 65.
    Benedetti M, Rorato R, Castro M, Machado BH, Antunes-Rodrigues J, Elias LL. Water deprivation increases fos expression in hypothalamic corticotropin-releasing factor neurons induced by right atrial distension in awake rats. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1706–R1712.PubMedCrossRefGoogle Scholar
  66. 66.
    Rogers RC, Hermann GE. Mechanisms of action of CCK to activate central vagal afferent terminals. Peptides. 2008;29:1716–1725.PubMedCrossRefGoogle Scholar
  67. 67.
    Endoh T, Sato D, Wada Y, et al. Nerve growth factor and brain-derived neurotrophic factor attenuate angiotensin-II-induced facilitation of calcium channels in acutely dissociated nucleus tractus solitarii neurons of the rat. Arch Oral Biol. 2008;53:1192–1201.PubMedCrossRefGoogle Scholar
  68. 68.
    Geerling JC, Chimenti PC, Loewy AD. Phox2b expression in the aldosterone-sensitive HSD2 neurons of the NTS. Brain Res. 2008;1226:82–88.PubMedCrossRefGoogle Scholar
  69. 69.
    Wan S, Browning KN. Glucose increases synaptic transmission from vagal afferent central nerve terminals via modulation of 5-Ht3 receptors. Am J Physiol Gastrointest Liver Physiol. 2008;295:G1050–G1057.PubMedCrossRefGoogle Scholar
  70. 70.
    Jacobsson G, Meister B. Hexokinase I messenger RNA in the rat central nervous system. Mol Cell Neurosci. 1994;5:658–677.PubMedCrossRefGoogle Scholar
  71. 71.
    da Silva LG, Dias AC, Furlan E, Colombari E. Nitric oxide modulates the cardiovascular effects elicited by acetylcholine in the nts of awake rats. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1774–1781.PubMedCrossRefGoogle Scholar
  72. 72.
    Mansour A, Fox CA, Burke S, et al. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: An in situ hybridization study. J Comp Neurol. 1994;350:412–438.PubMedCrossRefGoogle Scholar
  73. 73.
    Mansour A, Fox CA, Thompson RC, Akil H, Watson SJ. Mu-opioid receptor mRNA expression in the rat CNS: Comparison to mu-receptor binding. Brain Res. 1994;643:245–265.PubMedCrossRefGoogle Scholar
  74. 74.
    Ibuki T, Okamura H, Miyazaki M, Yanaihara N, Zimmerman EA, Ibata Y. Comparative distribution of three opioid systems in the lower brainstem of the monkey (macaca fuscata). J Comp Neurol. 1989;279:445–456.PubMedCrossRefGoogle Scholar
  75. 75.
    Hsiao M, Lu PJ, Huang HN, et al. Defective phosphatidylinositol 3-kinase signaling in central control of cardiovascular effects in the nucleus tractus solitarii of spontaneously hypertensive rats. Hypertens Res. 2008;31:1209–1218.PubMedCrossRefGoogle Scholar
  76. 76.
    Ho LK, Chen K, Ho IC, et al. Adrenomedullin enhances baroreceptor reflex response via cAMP/PKA signaling in nucleus tractus solitarii of rats. Neuropharmacology. 2008;55:729–736.PubMedCrossRefGoogle Scholar
  77. 77.
    Cui H, Kohsaka A, Waki H, et al. Adrenomedullin 2 microinjection into the nucleus tractus solitarius elevates arterial pressure and heart rate in rats. Auton Neurosci. 2008;142:45–50.PubMedCrossRefGoogle Scholar
  78. 78.
    Zhang W, Carreno FR, Cunningham JT, Mifflin SW. Chronic sustained and intermittent hypoxia reduce the function of ATP-sensitive potassium channels in the nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1555–R1562.PubMedCrossRefGoogle Scholar
  79. 79.
    Buniel M, Glazebrook PA, Ramirez-Navarro A, Kunze DL. Distribution of voltage-gated potassium and hyperpolarization-activated channels in sensory afferent fibers in the rat carotid body. J Comp Neurol. 2008;510:367–377.PubMedCrossRefGoogle Scholar
  80. 80.
    Wang WZ, Gao L, Wang HJ, Zucker IH, Wang W. Interaction between cardiac sympathetic afferent reflex and chemoreflex is mediated by the NTS AT1 receptors in heart failure. Am J Physiol Heart Circ Physiol. 2008;295:H1216–H1226.PubMedCrossRefGoogle Scholar
  81. 81.
    Gouty S, Regalia J, Helke CJ. Attenuation of the afferent limb of the baroreceptor reflex in streptozotocin-induced diabetic rats. Auton Neurosci. 2001;89:86–95.PubMedCrossRefGoogle Scholar
  82. 82.
    Waki H, Gouraud SS, Maeda M, Paton JF. Gene expression profiles of major cytokines in the nucleus tractus solitarii of the spontaneously hypertensive rat. Auton Neurosci. 2008;142:40–44.PubMedCrossRefGoogle Scholar
  83. 83.
    Waki H, Gouraud SS, Maeda M, Paton JF. Specific inflammatory condition in nucleus tractus solitarii of the SHR: Novel insight for neurogenic hypertension? Auton Neurosci. 2008;142:25–31.PubMedCrossRefGoogle Scholar
  84. 84.
    Bardet SM, Martinez-de-la-Torre M, Northcutt RG, Rubenstein JL, Puelles L. Conserved pattern of OTP-positive cells in the paraventricular nucleus and other hypothalamic sites of tetrapods. Brain Res Bull. 2008;75:231–235.PubMedCrossRefGoogle Scholar
  85. 85.
    Tauchi M, Zhang R, D’Alessio DA, Stern JE, Herman JP. Distribution of glucagon-like peptide-1 immunoreactivity in the hypothalamic paraventricular and supraoptic nuclei. J Chem Neuroanat. 2008;36:144–149.PubMedCrossRefGoogle Scholar
  86. 86.
    Powers-Martin K, Phillip JK, Biancardi VC, Stern JE. Heterogeneous distribution of basal cyclic guanosine monophosphate within distinct neuronal populations in the hypothalamic paraventricular nucleus. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1341–R1350.PubMedCrossRefGoogle Scholar
  87. 87.
    Watson AM, McKinley MJ, May CN. Effect of central urotensin II on heart rate, blood pressure and brain fos immunoreactivity in conscious rats. Neuroscience. 2008;155:241–249.PubMedCrossRefGoogle Scholar
  88. 88.
    Sonner PM, Filosa JA, Stern JE. Diminished A-type potassium current and altered firing properties in presympathetic PVN neurones in renovascular hypertensive rats. J Physiol. 2008;586:1605–1622.PubMedCrossRefGoogle Scholar
  89. 89.
    Orlov SN, Mongin AA. Salt-sensing mechanisms in blood pressure regulation and hypertension. Am J Physiol Heart Circ Physiol. 2007;293:H2039–H2053.PubMedCrossRefGoogle Scholar
  90. 90.
    Menegon LF, Zaparolli A, Boer PA, de Almeida AR, Gontijo JA. Long-term effects of intracerebroventricular insulin microinjection on renal sodium handling and arterial blood pressure in rats. Brain Res Bull. 2008;76:344–348.PubMedCrossRefGoogle Scholar
  91. 91.
    Behbehani MM. Functional characteristics of the midbrain periaqueductal gray. Prog Neurobiol. 1995;46:575–605.PubMedCrossRefGoogle Scholar
  92. 92.
    Keay KA, Bandler R. Anatomical evidence for segregated input from the upper cervical spinal cord to functionally distinct regions of the periaqueductal gray region of the cat. Neurosci Lett. 1992;139:143–148.PubMedCrossRefGoogle Scholar
  93. 93.
    Santos JM, Macedo CE, Brandao ML. Gabaergic mechanisms of hypothalamic nuclei in the expression of conditioned fear. Neurobiol Learn Mem. 2008;90:560–568.PubMedCrossRefGoogle Scholar
  94. 94.
    Miguel TT, Nunes-de-Souza RL. Anxiogenic-like effects induced by NMDA receptor activation are prevented by inhibition of neuronal nitric oxide synthase in the periaqueductal gray in mice. Brain Res. 2008;1240:39–46.PubMedCrossRefGoogle Scholar
  95. 95.
    Moraes CL, Bertoglio LJ, Carobrez AP. Interplay between glutamate and serotonin within the dorsal periaqueductal gray modulates anxiety-related behavior of rats exposed to the elevated plus-maze. Behav Brain Res. 2008;194:181–186.PubMedCrossRefGoogle Scholar
  96. 96.
    Cezario AF, Ribeiro-Barbosa ER, Baldo MV, Canteras NS. Hypothalamic sites responding to predator threats - The role of the dorsal premammillary nucleus in unconditioned and conditioned antipredatory defensive behavior. Eur J Neurosci. 2008;28:1003–1015.PubMedCrossRefGoogle Scholar
  97. 97.
    Figueira RJ, Peabody MF, Lonstein JS. Oxytocin receptor activity in the ventrocaudal periaqueductal gray modulates anxiety-related behavior in postpartum rats. Behav Neurosci. 2008;122:618–628.PubMedCrossRefGoogle Scholar
  98. 98.
    Chaitoff KA, Patel D, Ally A. Effects of endothelial NOS antagonism within the periaqueductal gray on cardiovascular responses and neurotransmission during mechanical, heat, and cold nociception. Brain Res. 2008;1236:93–104.PubMedCrossRefGoogle Scholar
  99. 99.
    de Menezes RC, Zaretsky DV, Sarkar S, Fontes MA, Dimicco JA. Microinjection of muscimol into the periaqueductal gray suppresses cardiovascular and neuroendocrine response to air jet stress in conscious rats. Am J Physiol Regul Integr Comp Physiol. 2008;295:R881–R890.PubMedCrossRefGoogle Scholar
  100. 100.
    Loyd DR, Murphy AZ. Androgen and estrogen (alpha) receptor localization on periaqueductal gray neurons projecting to the rostral ventromedial medulla in the male and female rat. J Chem Neuroanat. 2008;36:216–226.PubMedCrossRefGoogle Scholar
  101. 101.
    Wang Z, Bradesi S, Maarek JM, et al. Regional brain activation in conscious, nonrestrained rats in response to noxious visceral stimulation. Pain. 2008;138:233–243.PubMedCrossRefGoogle Scholar
  102. 102.
    Allen AM, O’Callaghan EL, Hazelwood L, et al. Distribution of cells expressing human renin-promoter activity in the brain of a transgenic mouse. Brain Res. 2008;1243:78–85.PubMedCrossRefGoogle Scholar
  103. 103.
    Abdelalim EM, Masuda C, Bellier JP, et al. Distribution of natriuretic peptide receptor-C immunoreactivity in the rat brainstem and its relationship to cholinergic and catecholaminergic neurons. Neuroscience. 2008;155:192–202.PubMedCrossRefGoogle Scholar
  104. 104.
    Taylor CP, Garrido R. Immunostaining of rat brain, spinal cord, sensory neurons and skeletal muscle for calcium channel alpha2-delta (alpha2-delta) type 1 protein. Neuroscience. 2008;155:510–521.PubMedCrossRefGoogle Scholar
  105. 105.
    Fink GD, Bruner CA, Mangiapane ML. Area postrema is critical for angiotensin-induced hypertension in rats. Hypertension. 1987;9:355–361.PubMedGoogle Scholar
  106. 106.
    Monosikova J, Herichova I, Mravec B, Kiss A, Zeman M. Effect of upregulated renin-angiotensin system on per2 and bmal1 gene expression in brain structures involved in blood pressure control in TGR(mREN-2)27 rats. Brain Res. 2007;1180:29–38.PubMedCrossRefGoogle Scholar
  107. 107.
    Kolaj M, Coderre E, Renaud LP. Orexin peptides enhance median preoptic nucleus neuronal excitability via postsynaptic membrane depolarization and enhancement of glutamatergic afferents. Neuroscience. 2008;155:1212–1220.PubMedCrossRefGoogle Scholar
  108. 108.
    Ployngam T, Collister JP. Role of the median preoptic nucleus in chronic angiotensin II-induced hypertension. Brain Res. 2008;1238:75–84.PubMedCrossRefGoogle Scholar
  109. 109.
    Alloway KD, Aaron GB. Adaptive changes in the somatotopic properties of individual thalamic neurons immediately following microlesions in connected regions of the nucleus cuneatus. Synapse. 1996;22:1–14.PubMedCrossRefGoogle Scholar
  110. 110.
    Margatho LO, Godino A, Oliveira FR, Vivas L, Antunes-Rodrigues J. Lateral parabrachial afferent areas and serotonin mechanisms activated by volume expansion. J Neurosci Res. 2008;86:3613–3621.PubMedCrossRefGoogle Scholar
  111. 111.
    Martini M, Di Sante G, Collado P, Pinos H, Guillamon A, Panzica GC. Androgen receptors are required for full masculinization of nitric oxide synthase system in rat limbic-hypothalamic region. Horm Behav. 2008;54:557–564.PubMedCrossRefGoogle Scholar
  112. 112.
    Xue B, Zhao Y, Johnson AK, Hay M. Central estrogen inhibition of angiotensin II-induced hypertension in male mice and the role of reactive oxygen species. Am J Physiol Heart Circ Physiol. 2008;295:H1025–H1032.PubMedCrossRefGoogle Scholar
  113. 113.
    Milner TA, Lubbers LS, Alves SE, McEwen BS. Nuclear and extranuclear estrogen binding sites in the rat forebrain and autonomic medullary areas. Endocrinology. 2008;149:3306–3312.PubMedCrossRefGoogle Scholar
  114. 114.
    Gerrits PO, Kortekaas R, Veening JG, et al. Estrous cycle-dependent neural plasticity in the caudal brainstem in the female golden hamster: Ultrastructural and immunocytochemical studies of axo-dendritic relationships and dynamic remodeling. Horm Behav. 2008;54:627–639.PubMedCrossRefGoogle Scholar
  115. 115.
    Milner TA, Mitterling KL, Iadecola C, Waters EM. Ultrastructural localization of extranuclear progestin receptors relative to C1 neurons in the rostral ventrolateral medulla. Neurosci Lett. 2008;431:167–172.PubMedCrossRefGoogle Scholar
  116. 116.
    Xu Q, Hamada T, Kiyama R, Sakuma Y, Wada-Kiyama Y. Site-specific regulation of gene expression by estrogen in the hypothalamus of adult female rats. Neurosci Lett. 2008;436:35–39.PubMedCrossRefGoogle Scholar
  117. 117.
    Jansen HT, Popiela CL, Jackson GL, Iwamoto GA. A re-evaluation of the effects of gonadal steroids on neuronal activity in the male rat. Brain Res Bull. 1993;31:217–223.PubMedCrossRefGoogle Scholar
  118. 118.
    Carlson SH, Wyss JM. Neurohormonal regulation of the sympathetic nervous system: New insights into central mechanisms of action. Curr Hypertens Rep. 2008;10:233–240.PubMedCrossRefGoogle Scholar
  119. 119.
    Watts SW. Henry pickering bowditch award the love of a lifetime: 5-HT in the cardiovascular system. Am J Physiol Regul Integr Comp Physiol 2009 Feb; 296(2):R252–R256.Google Scholar
  120. 120.
    Watts SW, Rondelli C, Thakali K, et al. Morphological and biochemical characterization of remodeling in aorta and vena cava of DOCA-salt hypertensive rats. Am J Physiol Heart Circ Physiol. 2007;292:H2438–H2448.PubMedCrossRefGoogle Scholar
  121. 121.
    Ramage AG, Villalon CM. 5-hydroxytryptamine and cardiovascular regulation. Trends Pharmacol Sci. 2008;29:472–481.PubMedCrossRefGoogle Scholar
  122. 122.
    O’Donaughy TL, Qi Y, Brooks VL. Central action of increased osmolality to support blood pressure in deoxycorticosterone acetate-salt rats. Hypertension. 2006;48:658–663.PubMedCrossRefGoogle Scholar
  123. 123.
    Pietranera L, Saravia FE, Roig P, Lima A, De Nicola AF. Protective effects of estradiol in the brain of rats with genetic or mineralocorticoid-induced hypertension. Psychoneuroendocrinology. 2008;33:270–281.PubMedCrossRefGoogle Scholar
  124. 124.
    Van Huysse JW. Endogenous brain na pumps, brain ouabain-like substance and the alpha2 isoform in salt-dependent hypertension. Pathophysiology. 2007;14:213–220.PubMedGoogle Scholar
  125. 125.
    Huang BS, Cheung WJ, Wang H, Tan J, White RA, Leenen FH. Activation of brain renin-angiotensin-aldosterone system by central sodium in wistar rats. Am J Physiol Heart Circ Physiol. 2006;291:H1109–H1117.PubMedCrossRefGoogle Scholar
  126. 126.
    Komjati K, Velkei-Harvich M, Toth J, Dallos G, Nyary I, Sandor P. Endogenous opioid mechanisms in hypothalamic blood flow autoregulation during haemorrhagic hypotension and angiotensin-induced acute hypertension in cats. Acta Physiol Scand. 1996;157:53–61.PubMedCrossRefGoogle Scholar
  127. 127.
    Hill-Pryor C, Dunbar JC. The effect of high fat-induced obesity on cardiovascular and physical activity and opioid responsiveness in conscious rats. Clin Exp Hypertens. 2006;28:133–145.PubMedCrossRefGoogle Scholar
  128. 128.
    Iwamoto GA, Mitchell JH, Sadeq M, Kozlowski GP. Localization of tyrosine hydroxylase and phenylethanolamine N-methyltransferase immunoreactive cells in the medulla of the dog. Neurosci Lett. 1989;107:12–18.PubMedCrossRefGoogle Scholar
  129. 129.
    Stafford JM, Yu F, Printz R, Hasty AH, Swift LL, Niswender KD. Central nervous system neuropeptide Y signaling modulates VLDL triglyceride secretion. Diabetes. 2008;57:1482–1490.PubMedCrossRefGoogle Scholar
  130. 130.
    da Silva AA, Tallam LS, Liu J, Hall JE. Chronic antidiabetic and cardiovascular actions of leptin: Role of CNS and increased adrenergic activity. Am J Physiol Regul Integr Comp Physiol. 2006;291:R1275–R1282.PubMedCrossRefGoogle Scholar
  131. 131.
    Sanders JD, Szot P, Weinshenker D, Happe HK, Bylund DB, Murrin LC. Analysis of brain adrenergic receptors in dopamine-β-hydroxylase knockout mice. Brain Res. 2006;1109:45–53.PubMedCrossRefGoogle Scholar
  132. 132.
    Ye P, Kenyon CJ, Mackenzie SM, et al. Effects of ACTH, dexamethasone, and adrenalectomy on 11β-hydroxylase (CYP11B1) and aldosterone synthase (CYP11B2) gene expression in the rat central nervous system. J Endocrinol. 2008;196:305–311.PubMedCrossRefGoogle Scholar
  133. 133.
    Su J, Lei Z, Zhang W, Ning H, Ping J. Distribution of orexin B and its relationship with GnRH in the pig hypothalamus. Res Vet Sci. 2008;85:315–323.PubMedCrossRefGoogle Scholar
  134. 134.
    Papakonstantinou P, Tziris N, Kesisoglou I, et al. The effect of porcine orexin A on insulin plasma concentrations in pigs. J Biol Regul Homeost Agents. 2007;21:115–124.PubMedGoogle Scholar
  135. 135.
    Yamanaka A, Muraki Y, Ichiki K, et al. Orexin neurons are directly and indirectly regulated by catecholamines in a complex manner. J Neurophysiol. 2006;96:284–298.PubMedCrossRefGoogle Scholar
  136. 136.
    Jegou S, Cartier D, Dubessy C, et al. Localization of the urotensin II receptor in the rat central nervous system. J Comp Neurol. 2006;495:21–36.PubMedCrossRefGoogle Scholar
  137. 137.
    Dubessy C, Cartier D, Lectez B, et al. Characterization of urotensin II, distribution of urotensin II, urotensin II-related peptide and UT receptor mRNAs in mouse: Evidence of urotensin II at the neuromuscular junction. J Neurochem. 2008;107:361–374.PubMedCrossRefGoogle Scholar
  138. 138.
    Sartor DM, Verberne AJ. Abdominal vagal signalling: A novel role for cholecystokinin in circulatory control? Brain Res Rev. 2008;59:140–154.PubMedCrossRefGoogle Scholar
  139. 139.
    Ruiz-Gayo M, Gonzalez MC, Fernandez-Alfonso S. Vasodilatory effects of cholecystokinin: New role for an old peptide? Regul Pept. 2006;137:179–184.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • David R. Gross
    • 1
  1. 1.Department of Veterinary BiosciencesUniversity of Illinois, Urbana Champaign College of Veterinary MedicineUrbanaUSA

Personalised recommendations