Oxytocin in the Central Amygdaloid Nucleus Modulates the Neuroendocrine Responses Induced by Hypertonic Volume Expansion in the Rat

The present study investigated the involvement of the oxytocinergic neurones that project into the central amygdala (CeA) in the control of electrolyte excretion and hormone secretion in unanaesthetised rats subjected to acute hypertonic blood volume expansion (BVE; 0.3 M NaCl, 2 ml/100 g of body weight over 1 min). Oxytocin and vasopressin mRNA expression in the paraventricular (Pa) and supraoptic nucleus (SON) of the hypothalamus were also determined using the real time‐polymerase chain reaction and in situ hybridisation. Male Wistar rats with unilaterally implanted stainless steel cannulas in the CeA were used. Oxytocin (1 μg/0.2 μl), vasotocin, an oxytocin antagonist (1 μg/0.2 μl) or vehicle was injected into the CeA 20 min before the BVE. In rats treated with vehicle in the CeA, hypertonic BVE increased urinary volume, sodium excretion, plasma oxytocin (OT), vasopressin (AVP) and atrial natriuretic peptide (ANP) levels and also increased the expression of OT and AVP mRNA in the Pa and SON. In rats pre‐treated with OT in the CeA, previously to the hypertonic BVE, there were further significant increases in plasma AVP, OT and ANP levels, urinary sodium and urine output, as well as in gene expression (AVP and OT mRNA) in the Pa and SON compared to BVE alone. Vasotocin reduced sodium, urine output and ANP levels, although no changes were observed in plasma AVP and OT levels or in the expression of the AVP and OT genes in both hypothalamic nuclei. The results of the present study suggest that oxytocin in the CeA exerts a facilitatory role in the maintenance of hydroelectrolyte balance in response to changes in extracellular volume and osmolality.

[1]  J. Antunes-Rodrigues,et al.  CB1 modulation of hormone secretion, neuronal activation and mRNA expression following extracellular volume expansion , 2010, Experimental Neurology.

[2]  J. Menani,et al.  Lateral parabrachial nucleus and central amygdala in the control of sodium intake , 2010, Neuroscience.

[3]  J. Antunes-Rodrigues,et al.  GABA in the central amygdaloid nucleus modulates the electrolyte excretion and hormonal responses to blood volume expansion in rats. , 2009, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[4]  J. Antunes-Rodrigues,et al.  Lateral parabrachial afferent areas and serotonin mechanisms activated by volume expansion , 2008, Journal of Neuroscience Research.

[5]  J. Antunes-Rodrigues,et al.  Glucocorticoid modulation of neuronal activity and hormone secretion induced by blood volume expansion , 2007, Experimental Neurology.

[6]  N. Garcia-Cairasco,et al.  Neuroanatomical and cellular substrates of hypergrooming induced by microinjection of oxytocin in central nucleus of amygdala, an experimental model of compulsive behavior , 2007, Molecular Psychiatry.

[7]  A. Giusti-Paiva,et al.  Neurochemical brain groups activated after an isotonic blood volume expansion in rats , 2005, Neuroscience.

[8]  M. G. Terenzi,et al.  Oxytocin-induced excitation of neurones in the rat central and medial amygdaloid nuclei , 2005, Neuroscience.

[9]  P. Veinante,et al.  Vasopressin and Oxytocin Excite Distinct Neuronal Populations in the Central Amygdala , 2005, Science.

[10]  C. Elias,et al.  Hypothalamic cocaine- and amphetamine-regulated transcript neurons project to areas expressing gonadotropin releasing hormone immunoreactivity and to the anteroventral periventricular nucleus in male and female rats , 2004, Neuroscience.

[11]  E. Stricker,et al.  Inhibition of salt appetite in rats by central oxytocin. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[12]  T. Petrov,et al.  Chemically defined collateral projections from the pons to the central nucleus of the amygdala and hypothalamic paraventricular nucleus in the rat , 1994, Cell and Tissue Research.

[13]  D. Pfaff,et al.  Quantitativein situ hybridization to measure single-cell changes in vasopressin and oxytocin mRNA levels after osmotic stimulation , 1990, Cellular and Molecular Neurobiology.

[14]  Jianfeng Feng,et al.  Responses of Magnocellular Neurons to Osmotic Stimulation Involves Coactivation of Excitatory and Inhibitory Input: An Experimental and Theoretical Analysis , 2001, The Journal of Neuroscience.

[15]  J. Antunes-Rodrigues,et al.  Hypothalamic atrial natriuretic peptide and secretion of oxytocin , 2001, Brain Research.

[16]  N. Toschi,et al.  Brain oxytocin inhibits the (re)activity of the hypothalamo–pituitary–adrenal axis in male rats: involvement of hypothalamic and limbic brain regions , 2000, Regulatory Peptides.

[17]  Y. Ulrich‐Lai,et al.  Rat Adrenal Transplants are Reinnervated: An Invalid Model of Denervated Adrenal Cortical Tissue , 2000, Journal of neuroendocrinology.

[18]  J. Ludbrook,et al.  Activation of brain neurons following central hypervolaemia and hypovolaemia: contribution of baroreceptor and non-baroreceptor inputs , 1999, Neuroscience.

[19]  M. Palkovits Interconnections between the Neuroendocrine Hypothalamus and the Central Autonomic System Geoffrey Harris Memorial Lecture, Kitakyushu, Japan, October 1998 , 1999, Frontiers in Neuroendocrinology.

[20]  J. Olmos,et al.  The Extended Amygdala and Salt Appetite , 1999, Annals of the New York Academy of Sciences.

[21]  S. Mccann,et al.  Atrial natriuretic peptide and oxytocin induce natriuresis by release of cGMP. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Ludwig,et al.  Dendritic Release of Vasopressin and Oxytocin , 1998, Journal of neuroendocrinology.

[23]  A. Moreira,et al.  Effect of plasma osmolality on pituitary-adrenal responses to corticotropin-releasing hormone and atrial natriuretic peptide changes in central diabetes insipidus. , 1997, The Journal of clinical endocrinology and metabolism.

[24]  E. Tribollet,et al.  Vasopressin and oxytocin receptors in the central nervous system. , 1996, Critical reviews in neurobiology.

[25]  S. Mccann,et al.  Oxytocin mediates atrial natriuretic peptide release and natriuresis after volume expansion in the rat. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Mccann,et al.  Participation of the ascending serotonergic system in the stimulation of atrial natriuretic peptide release. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[27]  P. Veinante,et al.  Correlation between oxytocin neuronal sensitivity and oxytocin-binding sites in the amygdala of the rat: electrophysiological and histoautoradiographic study , 1994, Brain Research.

[28]  E. Stricker,et al.  Central oxytocin inhibition of food and salt ingestion: a mechanism for intake regulation of solute homeostasis , 1993, Regulatory Peptides.

[29]  T. Petrov,et al.  The hypothalamic paraventricular and lateral parabrachial nuclei receive collaterals from raphe nucleus neurons: A combined double retrograde and immunocytochemical study , 1992, The Journal of comparative neurology.

[30]  A. N. Epstein,et al.  Deficits in NaCl ingestion after damage to the central nucleus of the amygdala in the rat , 1992, Brain Research Bulletin.

[31]  J. Han,et al.  Serotonergic projections from the nucleus raphe dorsalis to the amygdala in the rat , 1991, Neuroscience Letters.

[32]  E. Stricker,et al.  Oxytocin produces natriuresis in rats at physiological plasma concentrations. , 1991, Endocrinology.

[33]  T. Gray,et al.  Direct projections from the central amygdaloid nucleus to the hypothalamic paraventricular nucleus: possible role in stress-induced adrenocorticotropin release. , 1989, Neuroendocrinology.

[34]  M. Morris,et al.  Baroreceptor Influences on Oxytocin and Vasopressin Secretion , 1989, Hypertension.

[35]  T. Hedner,et al.  Haemodynamics and plasma ANP (atrial natriuretic peptide) after acute blood volume expansion in normotensive and spontaneously hypertensive rats. , 1988, Acta physiologica Scandinavica.

[36]  Stanley J. Watson,et al.  The rat brain in stereotaxic coordinates (2nd edn) by George Paxinos and Charles Watson, Academic Press, 1986. £40.00/$80.00 (264 pages) ISBN 012 547 6213 , 1987, Trends in Neurosciences.

[37]  F. Calaresu,et al.  Cardiovascular responses to chemical and electrical stimulation of amygdala in rats. , 1987, The American journal of physiology.

[38]  Joseph E. LeDoux,et al.  Cardiovascular responses elicited by stimulation of neurons in the central amygdaloid nucleus in awake but not anesthetized rats resemble conditioned emotional responses , 1987, Brain Research.

[39]  H. V. Van Tol,et al.  Oxytocin gene expression in discrete hypothalamic magnocellular cell groups is stimulated by prolonged salt loading. , 1987, Endocrinology.

[40]  J. Dave,et al.  Circulating atrial natriuretic peptides in conscious rats: regulation of release by multiple factors. , 1986, Science.

[41]  M. Cantin,et al.  Direct radioimmunoassay of atrial natriuretic factor. , 1984, Biochemical and biophysical research communications.

[42]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[43]  R. Buijs,et al.  The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum , 1983, Brain Research.

[44]  L. Swanson,et al.  The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat , 1983, The Journal of comparative neurology.

[45]  M. Sofroniew Morphology of vasopressin and oxytocin neurones and their central and vascular projections. , 1983, Progress in brain research.

[46]  M. R. Covian,et al.  The control of sodium chloride intake: Functional relationship between hypothalamic inhibitory areas and amygdaloid complex stimulating areas , 1981, Brain Research Bulletin.

[47]  C. Saper,et al.  Efferent connections of the parabrachial nucleus in the rat , 1980, Brain Research.

[48]  S. Ojeda,et al.  A rapid and simple procedure for chronic cannulation of the rat jugular vein. , 1974, Journal of applied physiology.