Abstract
Various hindbrain nuclei have been demonstrated to be involved in the control of the cardiovascular reflexes elicited by both non-noxious and noxious gastric distension, through parasympathetic and sympathetic activation. The different role played by the branches of autonomic nervous system in exerting these effects and their crosstalk in relation to low-/high-pressure distension rate has not been examined yet. Therefore, in the present work, monolateral and bilateral vagotomy and splanchnicotomy were performed in anesthetised rats to analyse the involvement of hindbrain nuclei in haemodynamic changes caused by gastric distension at high (80 mmHg) and low (15 mmHg) pressure. The analysis of c-Fos expression in neuronal areas involved in cardiovascular control allowed us to examine their recruitment in response to various patterns of gastric distension and the crosstalk between vagal and splanchnic systems. The results obtained show that the low-pressure (non-noxious) gastric distension increases both heart rate and arterial blood pressure. In addition, the vagus nerve and hindbrain nuclei, such as nucleus ambiguous, ventrolateral medulla and lateral reticular nucleus, appear to be primarily involved in observed responses. In particular, we have found that although vagus nerve plays a central role in exerting those cardiovascular reflex changes at low gastric distension, for its functional expression an intact splanchnic system is mandatory. Hence, the absence of splanchnic input attenuates pressor responses or turns them into depressor responses. Instead at high-pressure (noxious) gastric distension, the splanchnic nerve represents the primary component in regulating the reflex cardiovascular effects.
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14 February 2024
This article has been retracted. Please see the Retraction Notice for more detail: https://doi.org/10.1007/s00221-024-06803-0
References
Aronow WS, Ahn C (1997) Association of postprandial hypotension with incidence of falls, syncope, coronary events, stroke, and total mortality at 29-month follow-up in 499 older nursing home resident. J Am Geriatr Soc 45:1051–1053
Barber WD, Burks TF (1983) Brain stem response to phasic gastric distension. Am J Physiol 251:G169–G327
Berthoud HR (2008) The vagus nerve, food intake and obesity. Regul Pept 149:15–25
Broussard DL, Altschuler SM (2000) Brainstem viscerotopic organization of afferents and afferents involved in the control of swallowing. Am J Med 108(Suppl 4a):79S–86S
Ciriello J, Calaresu FR (1977) Lateral reticular nucleus: a site of somatic and cardiovascular integration in the cat. Am J Physiol 233:R100–R109
Ciriello J, Caverson M (1986) Bidirectional cardiovascular connections between ventrolateral medulla and nucleus of the solitary tract. Brain Res 367:273–281
Dampney RAL (1981) Brain stem mechanisms in the control of arterial pressure. Clin Exp Hypertens 3:379–391
Dampney RAL (1994) Functional organization of central pathways regulating the cardiovascular system. Cardiovasc Syst Physiol Rev 74:323–364
Deguchi K, Ikeda K, Sasaki I, Shimamura M, Urai Y, Tsukaguchi M, Touge T, Takeuchi H, Kuriyama S (2007) Effects of daily water drinking on orthostatic and postprandial hypotension in patients with multiple system atrophy. J Neurol 254:735–740
Dogan MD, Kulchitsky VA, Patel S, Pétervári E, Széleky M, Romanovsky AA (2003) Bilateral splanchnicotomy does not affect lipopolysaccharide-induced fever in rats. Brain Res 993:227–229
Granata AR (1994) Rostral Ventrolateral medulla descending neurons excited by nucleus tractus solitarii inputs. Brain Res 648:299–305
Grundy D (2002) Neuroanatomy of visceral nociception: vagal and splanchnic afferent. Gut 51:i2–i5
Grundy D, Davison JS (1981) Cardiovascular changes in elicited by vagal gastric afferents in the rat. Q J Exp Physiol 66:307–310
Harris JA, Guglielmotti V, Bentivoglio M (1996) Diencephalic asymmetries. Neurosci Biobehav Rev 20:637–642
Henderson LA, Macefield VG (2013) Functional imaging of the human brainstem during somatosensory input and autonomic output. Front Hum Neurosci 7:1–8
Irving JT, McSwiney BA, Suffolk AS (1937) Afferent fibres from the stomach and small intestines. J Physiol 89:407–420
Jansen RWMM, Lipsitz LA (1995) Postprandial hypotension: epidemiology, pathophysiology and clinical management. Ann Intern Med 122:286–295
Janss AJ, Gebhart GF (1988) Quantitative characterization and spinal pathway mediating inhibition of spinal nociceptive transmission from the lateral reticular nucleus in the rat. J Neurophysiol 59:226–247
Kawai Y, Senba E (2000) Electrophysiological and morphological characteristics of nucleus of tractus solitarii neurons projecting to the ventrolateral medulla. Brain Res 877:374–378
Lane RD, Schwartz GE (1987) Induction of lateralized sympathetic input to the heart by the CNS during emotional arousal: a possible neurophysiologic trigger of sudden cardiac death. Psychosom Med 49:274–284
Longhurst JC, Spilker HL, Ordway GA (1981) Cardiovascular reflexes elicited by passive gastric distension in anesthetized cats. Am J Physiol 240:H539–H545
Massari VJ, Johnson TA, Gatti PJ (1995) Cardiotropic organization of the nucleus ambiguous? An anatomical and physiological analysis of neurons regulating atrioventricular conduction. Brain Res 679:227–240
Mathis C, Moran TH, Schwartz GJ (1998) Load-sensitive rat gastric vagal afferents encode volume but not gastric nutrients. Am J Physiol 274:R280–R286
McCann MJ, Rogers R (1992) Impact of antral mechanoreceptor activation on the vago-vagal reflex in the rat: functional zonation of responses. J Physiol 453:401–411
McKitrick DJ, Calaresu FR (1996) Nucleus ambiguus inhibits activity of cardiovascular units in RVLM. Brain Res 742:203–210
McKitrick DJ, Calaresu FR (1997) Reciprocal connection between nucleus ambiguous and caudal ventrolateral medulla. Brain Res 770:2213–2220
Menezes RCA, Fontes MAP (2007) Cardiovascular effects produced by activation of GABA receptors in the rostral ventrolateral medulla of conscious rats. Neuroscience 144:336–343
Mertz H (2002) Role of the brain and pathways in gastrointestinal sensory disorders in humans. Gut 51(Suppl I):i29–i33
Molinari C, Sabbatini M, Grossini E, Mary DASG, Cannas M, Vacca G (2006) Cardiovascular effects and c-Fos expression in the rat hindbrain in response to innocuous stomach distension. Brain Res Bull 69:140–146
Mravec B, Ondicova K, Tillinger A, Pecenak J (2015) Subdiaphragmatic vagotomy enhances stress-induced epinephrine release in rats. Auton Neurosci 190:20–25
Ozaki N, Gebhart GF (2001) Characterization of mechanosensitive splanchnic nerve afferent fibers innervating the rat stomach. Am J Physiol 281:G1449–G1459
Ozaki N, Sengupta JN, Gebhart GF (1999) Mechanosensitive properties of gastric vagal afferent fibers in the rat. J Neurophysiol 82:2210–2220
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, Orlando
Powley TL, Phillips RJ (2004) Gastric satiation is volumetric, intestinal satiation is nutritive. Physiol Behav 82:69–74
Sabbatini M, Molinari C, Grossini E, Mary DASG, Vacca G, Cannas M (2004) The pattern of c-Fos immunoreactivity in the hindbrain of the rat following stomach distension. Exp Brain Res 157:315–323
Sabbatini M, Molinari C, Grossini E, Piffanelli V, Mary DASG, Vacca G, Cannas M (2008) GABA(A) receptors expression pattern in rat brain following low pressure distension of the stomach. Neuroscience 152:449–458
Scott EM, Greenwood JP, Gilbey SG, Stoker JB, Mary DASG (2001) Water ingestion increases sympathetic vasoconstrictor discharge in normal subjects. Clin Sci 100:335–342
Sengupta JN, Gebhart GF (1994) Characterization of mechanosensitive pelvic nerve afferent fibres innervating the colon of the rat. J Neurophysiol 71:2046–2060
Timofeeva E, Baraboi ED, Richard D (2005) Contribution of the vagus nerve and lamina terminalis to brain activation induced by refeeding. Eur J Neurosci 22:1489–1501
Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4:37–48
Traub RJ, Lim F, Sengupta JN, Meller ST, Gebhart GF (1994) Noxious distension of viscera results in differential c-Fos expression in second order sensory neurons receiving sympathetic or parasympathetic input. Neurosci Lett 180:71–75
Traub RJ, Sengupta JN, Gebhart GF (1996) Differential c-fos expression in the nucleus of the solitary tract and spinal cord following noxious gastric distension. Neuroscience 74:873–884
Willing AE, Berthoud HR (1997) Gastric distension-induced c-fos expression in catecholaminergic neurons of rat dorsal vagal complex. Am J Physiol 272:R59–R67
Xavier CH, Nalivaiko E, Beig MI, Menezes GB, Cara DC, Campagnole-Santos MJ, Fontes MAP (2009) Functional asymmetry in the descending cardiovascular pathways from dorsomedial hypothalamic nucleus. Neuroscience 164:1360–1368
Zhang X, Jiang C, Tan Z, Fogel R (2002) Vagal motor neurons in rats respond to noxious and physiological gastrointestinal distension differentially. Eur J Neurosci 16:2027–2038
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Sabbatini, M., Grossini, E., Molinari, C. et al. RETRACTED ARTICLE: Gastric distension causes changes in heart rate and arterial blood pressure by affecting the crosstalk between vagal and splanchnic systems in anesthetised rats. Exp Brain Res 235, 1081–1095 (2017). https://doi.org/10.1007/s00221-016-4819-x
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DOI: https://doi.org/10.1007/s00221-016-4819-x