Download PDF
CC BY-NC-ND 4.0 · Arq Neuropsiquiatr 2021; 79(10): 871-878
DOI: 10.1590/0004-282X-ANP-2020-0549
Article

The alteration of neuronal activities of the cuneiform nucleus in non-hypovolemic and hypovolemic hypotensive conditions

Alterações da atividade neuronal no núcleo cuneiforme em condições hipovolêmicas e não hipovolêmicas
Reza Mohebbati 
1   Applied Biomedical Research Center, Mashhad University of Medical Sciences, Mashhad, Iran.
,
Hassan Abbassian 
2   Neuroscience Research Center, Mashhad University of Medical Sciences, Mashhad, Iran.
3   Sleep Clinic, Imam Reza Hospital, Mashhad University of Medical Sciences, Mashhad, Iran.
,
Mohammad Naser Shafei 
4   Department of Physiology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
,
Ali Gorji 
2   Neuroscience Research Center, Mashhad University of Medical Sciences, Mashhad, Iran.
5   Shefa Neuroscience Research Center, Khatam Alanbia Hospital, Tehran, Iran
6   Epilepsy Research Center, Department of Neurosurgery and Department of Neurology, Westfälische Wilhelms-Universität Münster, Münster, Germany.
,
Sajad Sahab Negah 
2   Neuroscience Research Center, Mashhad University of Medical Sciences, Mashhad, Iran.
5   Shefa Neuroscience Research Center, Khatam Alanbia Hospital, Tehran, Iran
› Author Affiliations
› Further Information
Also available at
   Permissions and Reprints

Abstract

Background: The cuneiform nucleus is located in the center of the circuit that mediates autonomic responses to stress. Hemorrhagic hypotension leads to chemoreceptor anoxia, which consequently results in the reduction of baroreceptor discharge and stimulation of the chemoreceptor. Objective: Using the single-unit recording technique, the neuronal activities of the cuneiform nucleus were investigated in hypotensive states induced by hemorrhage and administration of an anti-hypertensive drug (hydralazine). Methods: Thirty male rats were divided into the control, hemorrhage, and hydralazine groups. The femoral artery was cannulated for the recording of cardiovascular responses, including systolic blood pressure, mean arterial pressure, and heart rate. Hydralazine was administered via tail vein. The single-unit recording was performed from the cuneiform nucleus. Results: The maximal systolic blood pressure and the mean arterial pressure significantly decreased and heart rate significantly increased after the application of hydralazine as well as the following hemorrhage compared to the control group. Hypotension significantly increased the firing rate of the cuneiform nucleus in both the hemorrhage and hydralazine groups compared to the control group. Conclusions: The present data indicate that the cuneiform nucleus activities following hypotension may play a crucial role in blood vessels and vasomotor tone.

RESUMO

Antecedentes: O núcleo cuneiforme está localizado no centro do circuito que media as respostas autonômicas ao estresse. A hipotensão hemorrágica leva à anóxia dos quimiorreceptores, que, consequentemente, resulta na redução da descarga dos barorreceptores e estimulação do quimiorreceptor. Objetivo: Utilizando a técnica de registro em unidade única, as atividades neuronais do núcleo cuneiforme foram investigadas em estados de hipotensão induzida por hemorragia e administração de um anti-hipertensivo (hidralazina). Métodos: Trinta ratos machos foram divididos nos grupos controle, hemorragia e hidralazina. A artéria femoral foi canulada, para o registro de respostas cardiovasculares, incluindo pressão arterial sistólica, pressão arterial média e frequência cardíaca. A hidralazina foi administrada na veia da cauda. O registro de unidade única foi realizado a partir do núcleo cuneiforme. Resultados: A pressão arterial sistólica máxima e a pressão arterial média diminuíram significativamente, e a frequência cardíaca aumentou significativamente após a aplicação de hidralazina, bem como a hemorragia seguinte, em comparação com o grupo controle. A hipotensão aumentou significativamente a taxa de disparo da população do núcleo cuneiforme em ambos os grupos de hemorragia e hidralazina, em comparação com o grupo de controle. Conclusões: Os presentes dados indicam que as atividades do núcleo cuneiforme após hipotensão podem desempenhar um papel crucial nos vasos sanguíneos e no tônus vasomotor.

Keywords:

Hemorrhage - Blood Pressure - Cardiovascular System - Hydralazine - Electrophysiology

Palavras-chave:

Hemorragia - Pressão Sanguínea - Sistema Cardiovascular - Hidralazina - Eletrofisiologia

Authors’ contributions:

RM: conceptualization, data curation, investigation, methodology, project management, software and writing of the first draft; HA: investigation, methodology, software and validation; MNS: formal analysis, methodology, visualization and writing of the first draft; AG: funding acquisition, project management, supervision, validation, writing, reviewing and editing; SSN: conceptualization, data curation, investigation, supervision and writing, reviewing and editing.




Publication History

Received: 03 December 2020

Accepted: 05 March 2021

Article published online:
07 June 2023

© 2021. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil

 

  • References

  • 1 Barrett KE, Barman SM, Boitano S, Brooks HL. Ganong’s Review of Medical Physiology (Enhanced EB). Lange medical book. 23rd ed. New York: McGraw Hill Professional; 2009.
  • 2 Palkovits M. Interconnections between the neuroendocrine hypothalamus and the central autonomic system: Geoffrey Harris Memorial Lecture, Kitakyushu, Japan, October 1998. Front Neuroendocrinol. 1999 Oct;20(4):270-95. https://doi.org/10.1006/frne.1999.0186
  • 3 Carlson JD, Iacono RP, Maeda G. Nociceptive excited and inhibited neurons within the pedunculopontine tegmental nucleus and cuneiform nucleus. Brain Res. 2004 Jul;1013(2):182-7. https://doi.org/10.1016/j.brainres.2004.03.069
  • 4 Nasimi A, Shafei MN, Alaei H. Glutamate injection into the cuneiform nucleus in rat, produces correlated single unit activities in the Kolliker-Fuse nucleus and cardiovascular responses. Neuroscience. 2012 Oct;223:439-46. https://doi.org/10.1016/j.neuroscience.2012.07.041
  • 5 Korte SM, Jaarsma D, Luiten PGM, Bohus B. Mesencephalic cuneiform nucleus and its ascending and descending projections serve stress-related cardiovascular responses in the rat. J Auton Nerv Syst. 1992 Nov;41(1-2):157-76. https://doi.org/10.1016/0165-1838(92)90137-6
  • 6 Verberne AJ. Cuneiform nucleus stimulation produces activation of medullary sympathoexcitatory neurons in rats. Am J Physiol. 1995 Mar;268(3 Pt 2):R752-8. https://doi.org/10.1152/ajpregu.1995.268.3.R752
  • 7 Rossaint R, Cerny V, Coats TJ, Duranteau J, Fernández-Mondéjar E, Gordini G, et al. Key issues in advanced bleeding care in trauma. Shock. 2006 Oct;26(4):322-31. https://doi.org/10.1097/01.shk.0000225403.15722.e9
  • 8 Badin J, Boulain T, Ehrmann S, Skarzynski M, Bretagnol A, Buret J, et al. Relation between mean arterial pressure and renal function in the early phase of shock: a prospective, explorative cohort study. Crit Care. 2011;15(3):R135. https://doi.org/10.1186/cc10253
  • 9 Ahlgren J, Porter K, Hayward LF. Hemodynamic responses and c-Fos changes associated with hypotensive hemorrhage: standardizing a protocol for severe hemorrhage in conscious rats. Am J Physiol Regul Integr Comp Physiol. 2007 May;292(5):R1862-R71. https://doi.org/10.1152/ajpregu.00325.2006
  • 10 Farrokhi E, Shafei MN, Khajavirad A, Hosseini M, Bideskan ARE. Role of the nitrergic system of the cuneiform nucleus in cardiovascular responses in Urethane-Anesthetized male rats. Iran J Med Sci. 2017 Sep;42(5):473-80.
  • 11 Shafei MN, Nasimi A. Effect of glutamate stimulation of the cuneiform nucleus on cardiovascular regulation in anesthetized rats: Role of the pontine Kolliker–Fuse nucleus. Brain Res. 2011 Feb;1385:135-43. https://doi.org/1016/j.brainres.2011.02.046
  • 12 Shafei MN, Niazmand S, Hosseini M, Daloee MH. Pharmacological study of cholinergic system on cardiovascular regulation in the cuneiform nucleus of rat. Neurosci Lett. 2013 Aug;549:12-7. https://doi.org/10.1016/j.neulet.2013.05.046
  • 13 Mohebbati R, Hosseini M, Khazaei M, Rad AK, Shafei MN. Involvement of the 5-HT1A receptor of the cuneiform nucleus in the regulation of cardiovascular responses during normal and hemorrhagic conditions. Iran J Basic Med Sci. 2020 Jul;23(7):858-64. https://doi.org/10.22038/ijbms.2020.40453.9579
  • 14 Mohebbati R, Rad AK, Hosseini M, Shafei MN. Effect of opioid receptors of the cuneiform nucleus on cardiovascular responses in normotensive and hypotensive hemorrhagic rats. Neurosci Lett. 2021 Feb;745:135582. https://doi.org/10.1016/j.neulet.2020.135582
  • 15 Nasimi A, Kafami M. Vasopressin and sympathetic system mediate the cardiovascular effects of the angiotensin II in the bed nucleus of the stria terminalis in rat. Neurosci Res. 2016 Jul;108:34-9. https://doi.org/10.1016/j.neures.2016.01.003
  • 16 Paxinos G, Watson C. The rat brain in stereotaxic coordinates. San Diego: Elsevier Academic Press; 2005.
  • 17 Mohebbati R, Hosseini M, Khazaei M, Shafei MN. Cardiovascular effect of cuneiform nucleus during hemorrhagic hypotension. Basic Clin Neurosci. 2020 May-Jun;11(3):251-9. https://doi.org/10.32598/bcn.11.2.84.4
  • 18 Badoer E, McKinley MJ, Oldfield BJ, McAllen RM. A comparison of hypotensive and non-hypotensive hemorrhage on Fos expression in spinally projecting neurons of the paraventricular nucleus and rostral ventrolateral medulla. Brain Res. 1993 May;610(2):216-23. https://doi.org/10.1016/0006-8993(93)91403-F
  • 19 Cavun S, Resch GE, Evec AD, Rapacon-Baker MM, Millington WR. Blockade of delta opioid receptors in the ventrolateral periaqueductal gray region inhibits the fall in arterial pressure evoked by hemorrhage. JPET. 2001 May;297(2):612-9.
  • 20 Dampney RAL, Horiuchi J. Functional organisation of central cardiovascular pathways: studies using c-fos gene expression. Prog Neurobiol. 2003 Dec;71(5):359-84. https://doi.org/10.1016/j.pneurobio.2003.11.001
  • 21 Graham JC, Hoffman GE, Sved AF. c-Fos expression in brain in response to hypotension and hypertension in conscious rats. J Auton Nerv Syst 1995 Oct;55(1):92-104. https://doi.org/10.1016/0165-1838(95)00032-S
  • 22 Haghparast A, Gheitasi IP, Lashgari R. Involvement of glutamatergic receptors in the nucleus cuneiformis in modulating morphine-induced antinociception in rats. Eur J Pain. 2007 Nov;11(8):855-62. https://doi.org/10.1016/j.ejpain.2006.12.010
  • 23 Margeta-Mitrovic M, Mitrovic I, Riley RC, Jan LY, Basbaum AI. Immunohistochemical localization of GABAB receptors in the rat central nervous system. J Comp Neurol. 1999 Mar;405(3):299-321. https://doi.org/10.1002/(SICI)1096-9861(19990315)405:3<299::AID-CNE2>3.0.CO;2-6
  • 24 Behbehani MM, Zemlan FP. Response of nucleus raphe magnus neurons to electrical stimulation of nucleus cuneiformis: role of acetylcholine. Brain Res. 1986 Mar;369(1-2):110-8. https://doi.org/10.1016/0006-8993(86)90518-4