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Neurophysiology of a Central Baroreceptor Pathway Projecting to Hypothalamic Vasopressin Neurons

Published online by Cambridge University Press:  18 September 2015

Jack H. Jhamandas*
Affiliation:
Neurosciences Unit, Montreal General Hospital and McGill University, 1650 Cedar Ave., Montreal, Quebec
Leo P. Renaud
Affiliation:
Neurosciences Unit, Montreal General Hospital and McGill University, 1650 Cedar Ave., Montreal, Quebec
*
Division of Neurology, Montreal General Hospital Research Inst., 1650 Cedar Avenue, Montreal, Quebec, Canada H3G 1A4
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Abstract:

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Controversy exists as to the neural network whereby peripheral arterial baroreceptor information is transmitted to vasopressin (VP)-secreting neurons of the hypothalamic supraoptic nucleus (s.o.n.). In vivo electrophysiological studies in the rat were undertaken to characterize the selective depression of VP cell activity consequent to activation of peripheral baroreceptors. Electrical stimulation of the diagonal band of Broca (DB) in the rat evoked a similar selective inhibition of vasopressinergic neurons of the s.o.n. Local application of bicuculline, a GABA antagonist, abolished both the DB-evoked and baroreceptor-induced inhibition of VP-secreting neurons. In addition, recordings from DB neurons antidromically activated from the s.o.n. displayed an increase in firing consequent to baroreceptor activation, coinciding with the suppression of firing in s.o.n. VP neurons. These observations collectively indicate that an intrinsic GABA projection arising in the DB cell group selectively inhibits vasopressinergic neurons of the s.o.n. and that this pathway mediates peripheral arterial baroreceptor activity that influences the release of VP in the neurohypophysis. These data may be of critical importance in our understanding the etiology of those forms of experimental hypertension where abnormalities in central baroreceptor pathways have been implicated but not proven.

Type
Original Articles
Copyright
Copyright © Canadian Neurological Sciences Federation 1987

References

1.Poulain, DA, Wakerley, JB. Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin. Neuroscience 1982; 7: 773808.CrossRefGoogle ScholarPubMed
2.Brimble, MJ, Dyball, REJ. Characterization of responses of oxytocin-and vasopressin-secreting neurones in the supraoptic nucleus to osmotic stimulation. J Physiol (Lond) 1983; 271: 253271.CrossRefGoogle Scholar
3.Banks, D, Harris, MC. Lesions of the locus coeruleus abolish barore-ceptor induced depression of supraoptic neurons in the rat. J Physiol (Lond) 1984; 355: 383398.CrossRefGoogle ScholarPubMed
4.Day, TA, Renaud, LP. Electrophysiological evidence that norad-renergic afferents selectively facilitate the activity of supraoptic vasopressin neurons. Brain Res 1984; 303: 233240.CrossRefGoogle ScholarPubMed
5.Day, TA, Ferguson, AV. Facilitatory influences of noradrenergic afferents on the excitability of rat paraventricular nucleus neurosecretory cells. J Physiol (Lond) 1984; 355: 237249.CrossRefGoogle ScholarPubMed
6.Day, TA, Randle, JCR, Renaud, LP. Opposing alpha- and beta-adrenergic mechanisms mediate dose dependent actions of nor-adrenaline on supraoptic vasopressin neurons in vivo. Brain Res 1985; 358: 171179.CrossRefGoogle Scholar
7. Harris, MC. Effects of chemoreceptor and baroreceptor stimula-tion on the discharge of hypothalamic supraoptic neurones in rats. J Endocrinol 1979; 82: 115125.CrossRefGoogle Scholar
8.Meyer, DK, Oertel, WH, Brownstein, MJ. Deafferentiation studies on the glutamic acid decarboxylase content of the supraoptic nucleus of the rat. Brain Res 1980; 200: 165168.CrossRefGoogle Scholar
9.Perez de la Mora, M, Possani, LD, Tapia, R. Demonstration of central 7-aminobutyric-containing nerve terminals by means of antibodies against glutamate decarboxylase. Neuroscience 1981; 6: 875895.CrossRefGoogle ScholarPubMed
10.Bioulac, B, Gaffori, O, Harris, M. et al. Effects of acetylcholine sodium glutamate and GABA on the discharge of supraoptic neurons in the rat. Brain Res 1978; 154: 159162.CrossRefGoogle ScholarPubMed
11.Arnauld, E, Cirino, M, Layton, BS. et al. Contrasting actions of amino acids acetylcholine noradrenaline and leucine enkephalin on the excitability of supraoptic vasopressin-secreting neurons. Neuroendocrinol 1983; 36: 187196.CrossRefGoogle ScholarPubMed
12.Poulain, DA, Ellendorf, F, Vincent, JD. Septal connections with identified oxytocin and vasopressin neurones in the supraoptic nucleus of the rat. An electrophysiological investigation. Neuroscience 1980; 5: 379387.CrossRefGoogle ScholarPubMed
13.Cirino, M, Renaud, LP. Influence of lateral septum and amygdala stimulation of the excitability of hypothalamic supraoptic neurons. An electrophysiological study in the rat. Brain Res 1985; 326: 357361.CrossRefGoogle ScholarPubMed
14.Shibuki, K. Supraoptic neurosecretory cells: synaptic inputs from the nucleus accumbens in the rat. Exp Brain Res 1984; 53: 341348.CrossRefGoogle ScholarPubMed
15.Zaborszky, L, Leranth, C, Makara, GB, et al. Quantitative studies on the supraoptic nucleus in the rat. II Afferent fiberconnections. Exp Brain Res 1975; 22: 525540.CrossRefGoogle Scholar
16.Tribollet, E, Armstrong, WE, Dubois-Dauphin, M. et al. Extrahypothalamic afferent inputs to the supraoptic nucleus area of the rat as determined by retrograde and anterograde tracing techniques. Neuroscience 1985; 15: 135138.CrossRefGoogle Scholar
17.Krnjevic, K. Chemical nature of synaptic transmission in vertebrates. Physiol Rev 1974; 54: 418540.CrossRefGoogle Scholar
18.Tappaz, ML, Wassef, M, Oertel, WH. et al. Light- and electron microscopic immunocytochemistry of glutamic acid decarboxylase (GAD) in the basal hypothalamus: morphological evidence for neuroendocrine gamma-aminobutyrate (GABA). Neuroscience 1983; 9: 271287.CrossRefGoogle ScholarPubMed
19.Nagai, T, McGeer, PL, McGeer, EG. Distribution of GABA-T intensive neurons in the rat forebrain and midbrain. J Comp Neurol 1983; 218: 220238.CrossRefGoogle ScholarPubMed
20.Panula, P, Revuelta, AV, Cheney, DL. et al. An immunohistochemical study on the location of GABAergic neurons in rat septum. J Comp Neurol 1984; 222: 69180.CrossRefGoogle Scholar
21.Randle, JCR, Bourque, CW, Renaud, LP. Spontaneous and evoked IPSPs in rat supraoptic nucleus neurosecretory neurons in vitro. Proc Can Fed Biol Sci 1985; 28: 93.Google Scholar
22.Knepel, W, Nutto, D, Hertting, G. Evidence for involvement of a GABA-mediated inhibition in hypovolaemia-induced vasopressin release. Pflugers Arch 1980; 28: 177183.CrossRefGoogle Scholar
23.Yamashita, H. Effect of baro- and chemoreceptor activation on supraoptic nuclei neurons in the hypothalamus. Brain Res 1977; 126: 551556.CrossRefGoogle ScholarPubMed
24.Barker, JL, Crayton, JW, Nicoll, RA. Noradrenaline and acetylcholine responses of supraoptic neurosecretory cells. J Physiol (Lond) 1971; 218: 1932.CrossRefGoogle ScholarPubMed
25.Blessing, WW, Sved, AF, Reis, DJ. Destruction of noradrenergic neurons in rabbit brainstem elevates plasma vasopressin causing hypertension. Science 1982; 217: 661663.CrossRefGoogle ScholarPubMed
26.Sakai, K, Tourets, M, Salvert, D, et al. Afferents to the cat locus coeruleus and rostral raphe nuclei as visualized by horseradish peroxidase techniques. In: Grattini, SPujol, JF & Samarin, R. Brain New York: Raven Press 1978; 473478.Google Scholar
27.Sawchenko, PE, Swanson, LW. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res Rev 1982; 4: 275325.CrossRefGoogle Scholar
28.Jones, BE, Moore, RY. Ascending projections of the locus coeruleus in the rat. II Autoradiographic study. Brain Res 1977; 127: 2353.CrossRefGoogle ScholarPubMed
29.Ward, DG, Lefcourt, AM, Gann, DS. Neurons in the dorsal pons process information about changes in venous return and in arterial pressure. Brain Res 1980; 181: 7578.CrossRefGoogle ScholarPubMed
30.Jhamandas, JH, Renaud, LP. Diagonal band neurons may mediate arterial baroreceptor input to hypothalamic vasopressin-secreting neurons. Neurosci Lett 1986; 65: 214218.CrossRefGoogle ScholarPubMed
31.Rossi, NF, Schrier, RW. Role of arginine vasopressin in regulation of systemic arterial pressure. Ann Rev Med 1986; 37: 1320.CrossRefGoogle ScholarPubMed