Abstract
Midbrain periaqueductal grey (PAG) provokes the defense reaction when stimulated. The present study was conducted to determine whether, and how, the PAG produces baroreflex inhibition, a feature characterizing the hypothalamic defense reaction. In chloralose-urethane anaesthetized rats, baroreflex vagal bradycardia and baroreflex hypotension were provoked by aortic depressor nerve stimulation. When the PAG was electrically stimulated baroreflex vagal bradycardia was remarkably suppressed; suppression of baroreflex hypotension was observed following bilateral vagotomy. In contrast, chemical stimulation of the PAG by d,l-homocysteic acid microinjection markedly suppressed baroreflex vagal bradycardia but only minimally suppressed baroreflex hypotension. These findings suggest that whereas overall PAG stimulation inhibits not only cardiac but also vascular components of baroreflexes, inhibition of the latter component either depends largely on activation of passing fibers or requires recruitment of a larger number of PAG cell bodies. PAG inhibition of baroreflex vagal bradycardia was not affected following spinal cord transection at C1, indicating that the inhibition was exclusively central in origin and not due to peripheral, prejunctional inhibition of vagal acetylcholine release by increased cardiac sympathetic nerve activities. The PAG inhibition of baroreflexes was greatly attenuated following electrolytic as well as chemical destruction of the parabrachial region. On the other hand, when the PAG was extensively lesioned, baroreflex inhibition produced by hypothalamic defense area stimulation was markedly diminished. PAG excitation thus causes powerful inhibition of arterial baroreflexes which is mediated by the parabrachial region; the PAG also mediates a major fraction of hypothalamic inhibition of the baroreflexes.
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References
Bandler R (1982) Induction of ‘rage’ following microinjections of glutamate into midbrain but not hypothalamus of cats. Neurosci Lett 30:183–188
Bandler R, Depaulis A (1991) Midbrain periaqueductal gray control of defensive behavior in the cat and the rat. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and neurochemical organization. Plenum, New York, pp 175–198
Bauer RM, Vela MB, Simon T, Waldrop TG (1988) A GABA-ergic mechanism in the posterior hypothalamus modulates baroreflex bradycardia. Brain Res Bull 20:633–641
Beitz AJ (1982) The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 7:133–159
Carrive P, Bandler R (1991) Viscerotropic organization of neurons subserving hypotensive reactions within the midbrain periaqueductal grey: a correlative functional and anatomical study. Brain Res 541:206–215
Carrive P, Bandler R, Dampney RAL (1989) Somatic and autonomic integration in the midbrain of the unanesthetized decerebrate cat: a distinctive pattern evoked by excitation of neurones in the subtentorial portion of the midbrain periaqueductal grey. Brain Res 483:251–258
Coote JH, Hilton SM, Perez-Gonzalez JH (1979) Inhibition of the baroreceptor reflex on stimulation in the brain stem defence centre. J Physiol (Lond) 288:549–560
Donoghue S, Felder RB, Gilbey MP, Jordan D, Spyer KM (1985) Postsynaptic activity evoked in the nucleus tractus solitarius by carotid sinus and aortic nerve afferents in the cat. J Physiol (Lond) 360:261–273
Felder RB, Mifflin SW (1988) Modulation of carotid sinus afferent input to nucleus solitarius by parabrachial nucleus stimulation. Circ Res 63:35–49
Fulwiler CE, Saper CB (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res Rev 7: 229–259
Gabriel MH, Seller H (1970) Interaction of baroreceptor afferents from carotid sinus and aorta at the nucleus tractus solitarii. Pflügers Arch 318:7–20
Gebber GL, Snyder DW (1969) Hypothalamic control of baroreceptor reflexes. Am J Physiol 218:124–131
Heymans C, Neil E (1958) Reflexogenic areas of the cardiovascular system. Little, Brown, Boston, pp 95–100
Hilton SM, Redfern WS (1986) A search for brain stem cell groups integrating the defence reaction in the rat. J Physiol (Lond) 378:213–228
Hockman CH, Talesnik J (1971) Central nervous modulation of baroceptor input. Am J Physiol 221:515–519
Hockman CH, Talesnik J, Livingstone KE (1969) Central nervous system modulation of baroceptor reflexes. Am J Physiol 217:1681–1689
Horst GJ ter, Luiten PGM, Kuipers F (1984) Descending pathways from hypothalamus to dorsal motor vagus and ambiguus nuclei in the rat. J Auton Nerv Syst 11:59–75
Jhamandas JH, Aipersbach SE, Harris KH (1991) Cardiovascular influence on rat parabrachial nucleus: an electrophysiological study. Am J Physiol 260:R225-R231
Jones RO, Kirkman E, Little RA (1990) The involvement of the midbrain periaqueductal grey in the cardiovascular response to injury in the conscious and anaesthetized rat. Exp Physiol 75:483–495
Lovick TA (1991) Central nervous system integration of pain control and autonomic function. News Physiol Sci 6:82–86
Lovick TA (1992) Inhibitory modulation of the cardiovascular defence response by the ventrolateral periaqueductal grey matter in rats. Exp Brain Res 89:133–139
Mancia G, Zanchetti A (1981) Hypothalamic control of autonomic functions. In: Morgane PJ, Panksepp J (eds) Handbook of the hypothalamus, vol 3, part B, Behavioral studies of the hypothalamus. Dekker, New York, pp 147–201
Meller ST, Dennis BJ (1986) Afferent projections to the periaqueductal gray in the rabbit. Neuroscience 19:927–964
Mifflin SW, Spyer KM, Withington-Wray DJ (1988) Baroreceptor inputs to the nucleus tractus solitarius in the cat: modulation by the hypothalamus. J Physiol (Lond) 399:369–387
Moga MM, Herbert H, Hurley KM, Yasui Y, Gray TS, Saper CB (1990) Organization of cortical, basal forebrain, and hypothalamic afferents to the parabrachial nucleus in the rat. J Comp Neurol 295:624–661
Nosaka S (1976) Responses of rat brainstem neurons to carotid occlusion. Am J Physiol 231:20–27
Nosaka S, Nakase N, Murata K (1989) Somatosensory and hypothalamic inhibitions of baroreflex vagal bradycardia in rats. Pflügers Arch 413:656–666
Nosaka S, Murase S, Murata K (1991) Arterial baroreflex inhibition by gastric distension in rats: mediation by splanchnic afferents. Am J Physiol 260:R985-R994
Palkovits M, Zabolszky L (1979) Neural connections of the hypothalamus. In: Morgan PJ, Panksepp J (eds) Handbook of the hypothalamus, vol 1, Anatomy of the hypothalamus. Dekker, New York, pp 379–504
Paton JFR, Silva-Carvalho L, Thompson CS, Spyer KM (1990) Nucleus tractus solitarius as mediator of evoked parabrachial cardiovascular responses in the decerebrate rabbit. J Physiol (Lond) 428:693–705
Revington ML, McCloskey DI (1990) Sympathetic-parasympathetic interactions at the heart, possibly involving neuropeptide Y, in anaesthetized dogs. J Physiol (Lond) 428:359–370
Revington M, Potter E, McCloskey DI (1990) Prolonged inhibition of cardiac vagal action following sympathetic stimulation and galanin in anaesthetized cats. J Physiol (Lond) 431:495–503
Siegel A, Edinger H (1981) Neural control of aggression and rage behavior. In: Morgan PI, Panksepp J (eds) Handbook of hypothalamus, vol 3, part B, Behavioral studies of the hypothalamus. Dekker, New York, pp 203–240
Tolivia J, Tolivia D (1985) A new technique for differential and simultaneous staining of nerve cells and fibers. J Neurosci Methods 13:305–311
Varberne AJM, Guyenet PG (1992) Midbrain central gray: influence on medullary sympathoexcitatory neurons and the baroreflex in rats. Am J Physiol 263:R24-R33
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Nosaka, S., Murata, K., Inui, K. et al. Arterial baroreflex inhibition by midbrain periaqueductal grey in anaesthetized rats. Pflügers Arch. 424, 266–275 (1993). https://doi.org/10.1007/BF00384352
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DOI: https://doi.org/10.1007/BF00384352