Angiotensin II Pressor Activity Depends on Medial and Lateral Anterior Hypothalamic Pathways

Abstract

The preoptic region of hypothalamus was disconnected from caudal structures with two different-size knife cuts in rats to investigate the pathway responsible for the effects of intracerebroventricular (ICV) and intravenous (IV) angiotensin II (ang II) on blood pressure and arginine vasopressin (AVP) release. Seven days after surgery ICV ang II (125 ng) in sham-operated (sham) rats increased mean arterial pressure (MAP) (+23 ±3 mmHg) and decreased heart rate (HR) (-58 ± 5 beats/minute). However, ICV ang II had no effect on MAP or HR of rats with a large (preoptic-hypothalamic disconnection) cut. Both the pressor response (+12 ±2 mmHg) and the bradycardia (-39 ±6 beats/minute) were significantly reduced by a small (medial preoptic-hypothalamic disconnection) cut. The increased plasma AVP to ICV ang II in sham rats (9.8 ±3.6 pg/mL) was abolished in large-cut rats and attenuated in small-cut rats (3.2 ±0.7 pg/mL). IV bolus injection of ang II (125 ng) in sham rats increased MAP by 43 mmHg, whereas large-cut rats showed a blunted (25%) pressor response. The pressor response to IV infusion of ang II (8 ng/20 μL/minute for 15 minutes) was diminished in large-cut rats (+4 ±1 mmHg) as compared with that in sham rats (+ 19 ± 2 mmHg).

Both cuts transected the projection between the periventricular tissue surrounding the anteroventral third ventricle and supraoptic nucleus, but the supraoptic-neurohy pophyseal pathway was severed only by the large cut. By examining the location of microknife cuts, the authors conclude that the connectivity of the preoptic region with more caudal sites is necessary for the expression of the central and peripheral pressor activity of ang II, probably involving a key role of supraoptic nucleus and its connections.

Get full access to this article

View all access options for this article.

References

Ferrario CM , Gildenberg PL , McCubbin JW : Cardiovascular effects of angiotensin mediated by the central nervous system . Circ Res 30:257-262, 1972.

Broadwell RD , Brightman MW : Entry of peroxidase into neurons of the central and peripheral nervous systems from extracerebral and cerebral blood . J Comp Neurol 166:257-284, 1976.

Felix D. , Schlegel W. : Angiotensin receptive neurones in the subfornical organ. Structure-activity relations. Brain Res 149:107-116, 1978.

Mangiapane ML , Simpson JB : Subfornical organ: Forebrain site of pressor and dipsogenic action of angiotensin II. Am J Physiol 239:R382-R389, 1980.

Mangiapane ML , Simpson JB : Subfomical organ lesions reduce the pressor effect of systemic angiotensin II. Neuroendocrinology 31:380-384, 1980.

Vanhouten M. , Schiffrin EL , Mann Jfe , et al: Radioautographic localization of specific binding sites for blood-borne angiotensin II in the rat brain. Brain Res 186:480-485, 1980.

Bealer SL : Hypothalamic knife cuts attenuate the pressor responses to angiotensin II . Neuroendocrinology 35:1-7, 1982.

Hartle DK , Brody MJ : The angiotensin II pressor system of the rat forebrain. Circ Res 54:355-366, 1984.

Hartle DK , Lind RW , Johnson AK , et al: Localization of the anterior hypothalamic angiotensin II pressor system. Hypertension 4:II-159-II-165, 1982.

10.

Fink GD , Buggy J. , Haywood JR , et al: Hemodynamic effects of electrical stimulation of forebrain angiotensin and osmosensitive sites. Am J Physiol 235:H445-H451, 1978.

11.

Knuepfer MM , Gordon FJ , Johnson AK , et al: Identification of descending cardiovascular pathways from the anteroventricular third ventricle . Fed Proc 38:1446, 1979.

12.

Kawabe H. , Lopes OU , Chernicky CL , et al: Effects of large and small transections of the preoptic-hypothalamic region on hydromineral regulation in rats. Endocrine J 40:249-256, 1993.

13.

Kawabe H. , Brosnihan KB , Diz DI , et al: Role of brain dopamine in centrally evoked angiotensin II responses in conscious rats. Hypertension 8 (suppl I):I-84-I-89, 1986.

14.

Marson O. , Chernicky CL , Barnes KL , et al: The anteroventral third ventricle region. Participation in the regulation of blood pressure in conscious dogs. Hypertension 7 (suppl I):I-80-I-87, 1985 .

15.

Johnson AK , Bealer SL , McNeil JR , et al: The influence of the periventricular tissue of the anteroventral third ventricle (AV3V) on the release of vasopressin. Neurosci Abst 6:696, 1980.

16.

Carithers J. , Bealer SL , Brody MJ , et al: Fine structural evidence of degeneration in supraoptic nucleus and subfornical organ of rats with lesions in the anteroventral third ventricle. Brain Res 201:1-12, 1980.

17.

Wilkin LD , Druber KA , Johnson AK : Changes in magnocellular-neurohypophyseal vasopressin following anteroventral third ventricle (AV3V) lesions. J Cardiovasc Pharm 8 (suppl 7):S70-S75, 1986.

18.

Bickerton RK , Buckley JP : Evidence for a central mechanism in angiotensin induced hypertension. Proc Soc Exp Biol Med 106:834-836, 1961.

19.

Severs WB , Summy-Long J. , Taylor JS , et al: A central effect of angiotensin: Release of pituitary pressor material. J Pharmacol Exp Ther 174:27-34, 1970.

20.

Gilbert TM , Blatteis CM : Hypothalamic thermoregulatory pathways in the rat. J Appl Physiol 43:770-777, 1977.

21.

Goldstein BM , Brody MJ : Pressor response to intravertebral angiotensin II: abolition by central catecholamine depletion. In: Regulation of Blood Pressure by the Central Nervous System, ed. by Onesti G , Fernandes M , Kim K. New York: Grune & Stratton, 1976, pp 183-189.

22.

Buggy J. , Fink GD , Johnson AK , et al: Prevention of the development of renal hypertension by anteroventral third ventricular tissue lesions. Circ Res 40 (suppl 1):I-110-I-117, 1977 .