Glutamate and GABA in the medial amygdala induce selective central sympathetic/ parasympathetic cardiovascular responses

Canadian Journal of Physiology and Pharmacology

Volumn 90, Issue 5, 2012, Pages 525-536

  Neckel, Helinton ^a,b   Quagliotto, Edson ^a,b   Casali, Karina R ^c   Montano, Nicola ^d   Lago, Pedro Dal ^a   Rasia Filho, Alberto A ^a,b  

^a UNIVERSIDADE FEDERAL DE CIÊNCIAS DA SAÚDE DE PORTO ALEGRE   (Brazil)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^c INSTITUTO DE CARDIOLOGIA DO RIO GRANDE DO SUL   (Brazil)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

Baroreceptor reflex; Blood pressure; Central cardiovascular control; Chemoreceptor reflex; Extended amygdala; Heart rate; Power spectral analysis; Symbolic analysis

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR PARAMETERS; CARDIOVASCULAR RESPONSE; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; ENTROPY; HEART RATE VARIABILITY; HEMODYNAMIC MONITORING; MALE; MEAN ARTERIAL PRESSURE; MEDIAL AMYGDALA; NONHUMAN; PARASYMPATHETIC FUNCTION; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; RAT; SYMPATHETIC FUNCTION;

AMYGDALA; ANIMALS; BAROREFLEX; BLOOD PRESSURE; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; CARDIOVASCULAR SYSTEM; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HEART RATE; HEMODYNAMICS; MALE; NEUROTRANSMITTER AGENTS; RATS; RATS, WISTAR; SYMPATHETIC NERVOUS SYSTEM;

EID: 84860803944     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/Y2012-024     Document Type: Article

References (71)

1. Adamec, R.E., and Morgan, H.D. 1994. The effect of kindling of different nuclei in the left and right amygdala on anxiety in the rat. Physiol. Behav. 55(1): 1-12. doi:10.1016/0031-9384(94)90002-7. PMID:8140150.
2. Bupesh, M., Legaz, I., Abellán, A., and Medina, L. 2011. Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J. Comp. Neurol. 519(8): 1505-1525. doi:10.1002/cne.22581. PMID:21452208.
3. Canteras, N.S., Simerly, R.B., and Swanson, L.W. 1995. Organization of projections from the medial nucleus of the amygdala: PHAL study in the rat. J. Comp. Neurol. 360(2): 213-245. doi:10.1002/ cne.903600203. PMID:8522644.
4. Casali, K.R., Casali, A.G., Montano, N., Irigoyen, M.C., Macagnan, F., Guzzetti, S., and Porta, A. 2008. Multiple testing strategy for the detection of temporal irreversibility in stationary time series. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 77(6): 066-204. doi:10.1103/PhysRevE.77.066204. PMID:18643347.
5. Choi, G.B., Dong, H.W., Murphy, A.J., Valenzuela, D.M., Yancopoulos, G.D., Swanson, L.W., and Anderson, D.J. 2005. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron, 46(4): 647-660. doi:10.1016/j.neuron.2005.04.011. PMID:15944132.
6. Cruz, J.C., and Machado, B.H. 2009. GABA and nitric oxide in the PVN are involved in arterial pressure control but not in the chemoreflex responses in rats. Auton. Neurosci. 146(1-2): 47-55. doi:10.1016/j.autneu.2008.11.011. PMID:19131279.
7. Cruz, J.C., Bonagamba, L.G., Machado, B.H., Biancardi, V.C., and Stern, J.E. 2008. Intermittent activation of peripheral chemoreceptors in awake rats induces Fos expression in rostral ventrolateral medulla-projecting neurons in the paraventricular nucleus of the hypothalamus. Neuroscience, 157(2): 463-472. doi:10.1016/j.neuroscience.2008.08.070. PMID:18838112.
8. Cruz, J.C., Bonagamba, L.G., Stern, J.E., and Machado, B.H. 2010. Fos expression in the NTS in response to peripheral chemoreflex activation in awake rats. Auton. Neurosci. 152(1-2): 27-34. doi:10.1016/j.autneu.2009.08.016. PMID:19783484.
9. Dall'Ago, P., Fernandes, T.G., Machado, U.F., Bello, A.A., and Irigoyen, M.C. 1997. Baroreflex and chemoreflex dysfunction in streptozotocin-diabetic rats. Braz. J. Med. Biol. Res. 30(1): 119-124. doi:10.1590/S0100-879X1997000100018. PMID:9222413.
10. Dall'Ago, P., D'Agord Schaan, B., da Silva, V.O., Werner, J., da Silva Soares, P.P., de Angelis, K., and Irigoyen, M.C. 2007. Parasympathetic dysfunction is associated with baroreflex and chemoreflex impairment in streptozotocin-induced diabetes in rats. Auton. Neurosci. 131(1-2): 28-35. doi:10.1016/j.autneu. 2006.06.005. PMID:16872914.
11. Dall'Oglio, A., Gehlen, G., Achaval, M., and Rasia-Filho, A.A. 2008a. Dendritic branching features of Golgi-impregnated neurons from the ventral medial amygdala subnuclei of adult male and female rats. Neurosci. Lett. 439(3): 287-292. doi:10.1016/j.neulet. 2008.05.025. PMID:18538473.
12. Dall'Oglio, A., Gehlen, G., Achaval, M., and Rasia-Filho, A.A. 2008b. Dendritic branching features of posterodorsal medial amygdala neurons of adult male and female rats: further data based on the Golgi method. Neurosci. Lett. 430(2): 151-156. doi:10.1016/j.neulet.2007.10.051. PMID:18078715.
13. Davern, P.J., and Head, G.A. 2011. Role of the medial amygdala in mediating responses to aversive stimuli leading to hypertension. Clin. Exp. Pharmacol. Physiol. 38(2): 136-143. doi:10.1111/j. 1440-1681.2010.05413.x. PMID:20528979.
14. Davern, P.J., Nguyen-Huu, T.P., La Greca, L., Abdelkader, A., and Head, G.A. 2009. Role of the sympathetic nervous system in Schlager genetically hypertensive mice. Hypertension, 54(4): 852-859. doi:10.1161/HYPERTENSIONAHA.109.136069. PMID: 19667247.
15. Dayas, C.V., Buller, K.M., and Day, T.A. 1999. Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala. Eur. J. Neurosci. 11(7): 312-2322. doi:10.1046/j.1460-9568.1999.00645.x. PMID: 10383620.
16. Dayas, C.V., Buller, K.M., and Day, T.A. 2001. Medullary neurones regulate hypothalamic corticotropin-releasing factor cell responses to an emotional stressor. Neuroscience, 105(3): 707-719. doi:10. 1016/S0306-4522(01)00213-5. PMID:11516835.
17. de Castilhos, J., Marcuzzo, S., Forti, C.D., Frey, R.M., Stein, D., Achaval, M., and Rasia-Filho, A.A. 2006. Further studies on the rat posterodorsal medial amygdala: dendritic spine density and effect of 8-OH-DPAT microinjection on male sexual behavior. Brain Res. Bull. 69(2): 131-139. doi:10.1016/j.brainresbull.2005.11.013. PMID:16533661.
18. de Castilhos, J., Forti, C.D., Achaval, M., and Rasia-Filho, A.A. 2008. Dendritic spine density of posterodorsal medial amygdale neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: a Golgi study. Brain Res. 1240: 73-81. doi:10.1016/j.brainres.2008.09.002. PMID:18809393.
19. de Olmos, J., Beltramino, C.A., and Alheid, G.F. 2004. Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. In The Rat Nervous System. Edited by G. Paxinos. Elsevier Academic Press, Amsterdam. Netherlands. pp. 509-603.
20. Del Arco, A., Segovia, G., Fuxe, K., and Mora, F. 2003. Changes in dialysate concentrations of glutamate anda GABA in the brain: an index of volume transmission mediated actions? J. Neurochem. 85(1): 23-33. doi:10.1046/j.1471-4159.2003.01692.x. PMID:12641724.
21. Donato, J., Jr, Cavalcante, J.C., Silva, R.J., Teixeira, A.S., Bittencourt, J.C., and Elias, C.F. 2010. Male and female odors induce Fos expression in chemically defined neuronal population. Physiol. Behav. 99(1): 67-77. doi:10.1016/j.physbeh.2009.10.012. PMID:19857504.
22. Fazan, R., Jr, de Oliveira, M., da Silva, V.J., Joaquim, L.F., Montano, N., Porta, A., et al. 2005. Frequency-dependent baroreflex modulation of blood pressure and heart rate variability in conscious mice. Am. J. Physiol. Heart Circ. Physiol. 289(5): H1968-H1975. doi:10.1152/ajpheart.01224.2004. PMID: 15951338.
23. Fillenz, M. 1995. Physiological release of excitatory amino acids. Behav. Brain Res. 71(1-2): 51-67. doi:10.1016/0166-4328(95) 00045-3. PMID:8747174.
24. Fukumori, R., Nishigori, Y., Goshima, Y., and Kubo, T. 2004. Contribution of the medial amygdaloid nucleus to the development of hypertension in spontaneously hypertensive rats. Neurosci. Lett. 365(2): 128-131. doi:10.1016/j.neulet.2004.04.066. PMID: 15245793.
25. Genest, S.-E., Balon, N., Laforest, S., Drolet, G., and Kinkead, R. 2007. Neonatal maternal separation and enhancement of the hypoxic ventilatory response in rat: the role of GABAergic modulation within the paraventricular nucleus of the hypothalamus. J. Physiol. 583(1): 299-314. doi:10.1113/jphysiol.2007. 135160. PMID:17569732.
26. Gören, Z., Aslan, N., Berkman, K., Oktay, S., and Onat, F. 1996. The role of amygdala and hypothalamus in GABAA antagonist bicuculline-induced cardiovascular responses in conscious rats. Brain Res. 722(1-2): 118-124. doi:10.1016/0006-8993(96)002016. PMID:8813356.
27. Gören, M.Z., Akici, A., Berkman, K., and Onat, F. 2000. Cardiovascular responses to NMDA injected into nuclei of hypothalamus or amygdala in conscious rats. Pharmacology, 61 (4): 257-262. doi:10.1159/000028410. PMID:11093078.
28. Gören, M.Z., Yananli, H.R., Berkman, K., Onat, F., and Aker, R. 2003. The influence of dorsomedial hypothalamic nucleus on contralateral paraventricular nucleus in NMDA-mediated cardiovascular responses. Brain Res. 968(2): 219-226. doi:10.1016/ S0006-8993(03)02241-8. PMID:12663091.
29. Guillamón, A., and Segovia, S. 1997. Sex differences in the vomeronasal system. Brain Res. Bull. 44(4): 377-382. doi:10. 1016/S0361-9230(97)00217-7. PMID:9370202.
30. Guzzetti, S., Borroni, E., Garbelli, P.E., Ceriani, E., Della Bella, P., Montano, N., et al. 2005. Symbolic dynamics of heart rate variability: a probe to investigate cardiac autonomic modulation. Circulation, 112(4): 465-470. doi:10.1161/CIRCULATIONAHA. 104.518449. PMID:16027252.
31. Hassel, B., and Dingledine, R. 2006. Glutamate. In Basic neurochemistry: molecular and medical aspects. 7th ed. Edited by G.J. Siegel, R.W. Albers, S.T. Brady, and D.L. Price. Elsevier Academic Press, New York, N.Y. 23, pp. 267-290.
32. ILAR (Institute of Laboratory Animal Resources). 1996. Guide for the care and use of laboratory animals. NIH Publication No. 85-23 (revised 1996). National Academy Press, Washington, D.C. Available from www.nap.edu/openbook.php?record_id=5140.
33. Jaenisch, R.B., Hentschke, V.S., Quagliotto, E., Cavinatto, P.R., Schmeing, L.A., Xavier, L.L., et al. 2011. Respiratory muscle training iproves hemodynamics, autonomic function, baroreceptors sensitivity and respiratory mechanics in rats with heart failure. J. Appl. Physiol. 111(6): 1664-1670. doi:10.1152/japplphysiol. 01245.2010. PMID:21903877.
34. Kubo, T., Okatani, H., Nishigori, Y., Hagiwara, Y., Fukumori, R., and Goshima, Y. 2004. Involvement of the medial amygdaloid nucleus in restraint stress-induced pressor responses in rats. Neurosci. Lett. 354(1): 84-86. doi:10.1016/j.neulet.2003.09.061. PMID: 14698487.
35. Lohman, R.J., Liu, L., Morris, M., and O'Brien, T.J. 2005. Validation of a method for localised microinjection of drugs into thalamic subregions in rats for epilepsy pharmacological studies. J. Neurosci. Methods, 146(2): 191-197. doi:10.1016/j.jneumeth. 2005.02.008. PMID:16054509.
36. Longhurst, J. 2008. Neural regulation of the cardiovascular system. In Fundamental Neuroscience. Edited by L. Squire, D. Berg, F. Bloom, S. Dulac, A. Ghosh, and N. Spitzer. Academic Press, Burlington, Mass. pp. 829-853.
37. Magrì, V., Trimarchi, G.R., Quattrone, G., Squadrito, F., Di Giorgio, R.M., Costa, G., and Caputi, A.P. 1984. Increased cardiovascular responsiveness to GABAergic stimulation in DOCA-salt hypertensive rats. Res. Commun. Chem. Pathol. Pharmacol. 45(1): 107-118. PMID:6433410.
38. Majchrzak, M., Brailowsky, S., and Will, B. 1992. Chronic infusion of GABA into the nucleus basalis magnocellularis or frontal cortex of rats: a behavioral and histological study. Exp. Brain Res. 88(3): 531-540. doi:10.1007/BF00228182. PMID:1587314.
39. Malliani, A., Pagani, M., Lombardi, F., and Cerutti, S. 1991. Cardiovascular neural regulation explored in the frequency domain. Circulation, 84(2): 482-492. PMID:1860193.
40. Marcuzzo, S., Dall'Oglio, A., Ribeiro, M.F., Achaval, M., and RasiaFilho, A.A. 2007. Dendritic spines in the posterodorsal medial amygdala after restraint stress and ageing in rats. Neurosci. Lett. 424(1): 16-21. doi:10.1016/j.neulet.2007.07.019. PMID: 17709204.
41. Meredith, M., and Westberry, J.M. 2004. Distinctive responses in the medial amygdala to same-species and different-species pheromones. J. Neurosci.24(25):5719-5725. doi:10.1523/ JNEUROSCI.1139-04.2004. PMID:15215294.
42. Montano, N., Ruscone, T.G., Porta, A., Lombardi, F., Pagani, M., and Malliani, A. 1994. Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt. Circulation, 90(4): 1826-1831. PMID: 7923668.
43. Montano, N., Porta, A., Cogliati, C., Costantino, G., Tobaldini, E., Casali, K.R., and Iellamo, F. 2009. Heart rate variability explored in the frequency domain: a tool to investigate the link between heart and behavior. Neurosci. Biobehav. Rev. 33(2): 71-80. doi:10. 1016/j.neubiorev.2008.07.006. PMID:18706440.
44. Newman, S.W. 1999. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. N. Y. Acad. Sci. 877: 242-257.doi:10.1111/j.1749- 6632.1999.tb09271.x. PMID:10415653.
45. Nitecka, L., and Ben-Ari, Y. 1987. Distribution of GABA-like immunoreactivity in the rat amygdaloid complex. J. Comp. Neurol. 266(1): 45-55.doi:10.1002/cne.902660105. PMID: 3429715.
46. Nollo, G., Porta, A., Faes, L., Del Greco, M., Disertori, M., and Ravelli, F. 2001. Causal linear parametric model for baroreflex gain assessment in patients with recent myocardial infarction. Am. J. Physiol. Heart Circ. Physiol. 280(4): H1830-H1839. PMID: 11247798.
47. Olsen, R.W., and Betz, H. 2006. GABA and glycine. In Basic Neurochemistry: Molecular, Cellular and Medical Aspects. 7th ed. Edited by G.J. Siegel, R.W. Albers, S.T. Brady, and D.L. Price. Elsevier Academic Press, New York, N.Y. pp. 291-301.
48. Pagani, M., Montano, N., Porta, A., Malliani, A., Abboud, F.M., Birkett, C., and Somers, V.K. 1997. Relationship between spectral components of cardiovascular variabilities and direct measures of muscle sympathetic nerve activity in humans. Circulation, 95(6): 1441-1448. PMID:9118511.
49. Paré, D., Royer, S., Smith, Y., and Lang, E.J. 2003. Contextual inhibitory gating of impulse traffic in the intra-amygdaloid network. Ann. N. Y. Acad. Sci. 985(1): 78-91.doi:10.1111/j. 1749-6632.2003.tb07073.x. PMID:12724150.
50. Paxinos, G., and Watson, C. 1998. The rat brain in stereotaxic coordinates. Academic Press, San Diego,Calif.
51. Petrovich, G.D., Canteras, N.S., and Swanson, L.W. 2001. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Brain Res. Rev. 38(1-2): 247-289.doi:10.1016/S0165-0173(01)00080-7. PMID:11750934.
52. Porta, A., Tobaldini, E., Guzzetti, S., Furlan, R., Montano, N., and Gnecchi-Ruscone, T. 2007. Assessment of cardiac autonomic modulation during graded head-up tilt by symbolic analysis of heart rate variability. Am. J. Physiol. Heart Circ. Physiol. 293(1): H702-H708. doi:10.1152/ajpheart.00006.2007. PMID:17308016.
53. Porta, A., Casali, K.R., Casali, A.G., Gnecchi-Ruscone, T., Tobaldini, E., Montano, N., et al. 2008. Temporal asymmetries of short-term heart period variability are linked to autonomic regulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(2): R550-R557.doi:10.1152/ajpregu.00129.2008. PMID:18495836.
54. Quagliotto, E., Neckel, H., Riveiro, D.F., Casali, K.R., Mostarda, C., Irigoyen, M.C., et al. 2008. Histamine in the posterodorsal medial amygdala modulates cardiovascular reflex responses in awake rats. Neuroscience, 157(4): 709-719.doi:10.1016/j.neuroscience.2008. 09.053. PMID:18955117.
55. Quagliotto, E., Casali, K.R., Dal Lago, P., and Rasia-Filho, A.A. 2012. Neurotransmitter and neuropeptidergic modulation of cardiovascular responses evoked by the posterodorsal medial amygdala of adult male rats. In More from the amygdala: structure, functions and implications for disorders. Edited by D. Yilmazer- Hanke. Nova Science Publishers, Hauppauge, N.Y. In press.
56. Rasia-Filho, A.A. 2006. Is there anything autonomous in the nervous system? Adv. Physiol. Educ. 30(1): 9-12.doi:10.1152/ advan.00022.2005. PMID:16481602.
57. Rasia-Filho, A.A., and Lucion, A.B. 1996. Effects of 8-OH-DPAT on sexual behavior of male rats castrated at different ages. Horm. Behav. 30(3): 251-258.doi:10.1006/hbeh.1996.0030. PMID:8918681.
58. Rasia-Filho, A.A., Fabian, C., Rigoti, K.M., and Achaval, M. 2004. Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience, 126(4): 839-847.doi:10.1016/j.neuroscience.2004. 04.009. PMID:15207319.
59. Rasia-Filho, A.A., Brusco, J., and Moreira, J.E. 2009. Spine plasticity in the rat medial amygdala. In Dendritic spines: biochemistry, modeling and properties. Edited by L.R. Baylog. Nova Science Publishers, Hauppauge, N.Y. pp. 67-90.
60. Saha, S. 2005. Role of the central nucleus of the amygdala in the control of blood pressure: descending pathways to medullary cardiovascular nuclei. Clin. Exp. Pharmacol. Physiol. 32(5-6): 450-456.doi:10. 1111/j.1440-1681.2005.04210.x. PMID:15854157.
61. Simmons, D.A., and Yahr, P. 2003. GABA and glutamate in mating- activated cells in the preoptic area and medial amygdala of male gerbils. J. Comp. Neurol. 459(3): 290-300.doi:10.1002/cne. 10605. PMID:12655511.
62. Stauss, H.M. 2007. Identification of blood pressure control mechanisms by power spectral analysis. Clin. Exp. Pharmacol. Physiol. 34 (4): 362-368.doi:10.1111/j.1440-1681.2007.04588.x. PMID: 17324151.
63. Stefanova, N., and Ovtscharoff, W. 2000. Sexual dimorphism of the bed nucleus of the stria terminalis and the amygdala. Adv. Anat. Embryol. Cell Biol. 158: III-X, 1-78. PMID:11131840.
64. 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(5): 1043-1065.doi:10. 1161/01.CIR.93.5.1043. PMID:8598068.
65. Timmerman, W., and Westerink, B.H. 1997. Brain microdialysis of GABA and glutamate: what does it signify? Synapse, 27(3): 242-261.doi:10.1002/(SICI)1098-2396(199711)27:3<242::AIDSYN9>3.0.CO;2-D. PMID:9329159.
66. Tobaldini, E., Montano, N., Wei, S.G., Zhang, Z.H., Francis, J., Weiss, R.M., et al. 2009a. Autonomic cardiovascular modulation. IEEE Eng. Med. Biol. Mag. 28(6): 79-85.doi:10.1109/MEMB. 2009.934620. PMID:19914892.
67. Tobaldini, E., Porta, A., Wei, S.G., Zhang, Z.H., Francis, J., Casali, K.R., et al. 2009b. Symbolic analysis detects alterations of cardiac autonomic modulation in congestive heart failure rats. Auton. Neurosci. 150(1-2): 21-26.doi:10.1016/j.autneu.2009.03.009. PMID:19403339.
68. van Leeuwen, P., Cysarz, D., Lange, S., Geue, D., and Groenemeyer, D. 2007a. Quantification of fetal heart rate regularity using symbolic dynamics. Chaos, 17(1): 015119.doi:10.1063/1. 2431703. PMID:17411276.
69. van Leeuwen, P., Lange, S., Geue, D., and Gronemeyer, D. 2007b. Heart rate variability in the fetus: a comparison of measures. Biomed. Tech. (Berl.), 52(1): 61-65.doi:10.1515/BMT.2007.012. PMID:17313336.
70. Yoshida, S., Matsubara, T., Uemura, A., Iguchi, A., and Hotta, N. 2002. Role of medial amygdala in controlling hemodynamics via GABA(A) receptor in anesthetized rats. Circ. J. 66(2): 197-203.doi:10.1253/circj.66.197. PMID:11999648.
71. Zhang, W., Zhang, N., Sakurai, T., and Kuwaki, T. 2009. Orexin neurons in the hypothalamus mediate cardiorespiratory responses induced by disinhibition of the amygdala and bed nucleus of the stria terminalis. Brain Res. 1262: 25-37.doi:10.1016/j.brainres. 2009.01.022. PMID:19368849.