The role of nitric oxide in the regulation of the systemic and pulmonary vasculature of the rattlesnake, Crotalus durissus terrificus

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SUMMARY Autonomic control of heart rate variability and the central location of vagal preganglionic neurones (VPN) were examined in the rattlesnake(Crotalus durissus terrificus), in order to determine whether respiratory sinus arrhythmia (RSA) occurred in a similar manner to that described for mammals. Resting ECG signals were recorded in undisturbed snakes using miniature datalogging devices, and the presence of oscillations in heart rate (fh) was assessed by power spectral analysis (PSA). This mathematical technique provides a graphical output that enables the estimation of cardiac autonomic control by measuring periodic changes in the heart beat interval. At fh above 19 min-1spectra were mainly characterised by low frequency components, reflecting mainly adrenergic tonus on the heart. By contrast, at fhbelow 19 min-1 spectra typically contained high frequency components, demonstrated to be cholinergic in origin. Snakes with a fh >19 min-1 may therefore have insufficient cholinergic tonus and/or too high an adrenergic tonus acting upon the heart for respiratory sinus arrhythmia (RSA) to develop. A parallel study monitored fh simultaneously with the intraperitoneal pressures associated with lung inflation. Snakes with a fh<19 min-1 exhibited a high frequency (HF) peak in the power spectrum,which correlated with ventilation rate (fv). Adrenergic blockade by propranolol infusion increased the variability of the ventilation cycle, and the oscillatory component of the fh spectrum broadened accordingly. Infusion of atropine to effect cholinergic blockade abolished this HF component, confirming a role for vagal control of the heart in matching fh and fv in the rattlesnake. A neuroanatomical study of the brainstem revealed two locations for vagal preganglionic neurones (VPN). This is consistent with the suggestion that generation of ventilatory components in the heart rate variability (HRV)signal are dependent on spatially distinct loci for cardiac VPN. Therefore,this study has demonstrated the presence of RSA in the HRV signal and a dual location for VPN in the rattlesnake. We suggest there to be a causal relationship between these two observations.

Section: Discussionsupporting

confidence: 87%

Evidence for a respiratory component, similar to mammalian respiratory sinus arrhythmia, in the heart rate variability signal from the rattlesnake,Crotalus durissus terrificus

Campbell

Leite

Wang

et al. 2006

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“…The effect of NO on the venous circulation of reptiles, however, has not been investigated in vivo. In rattlesnakes, SNP decreased P sys , R sys and VS tot as previously shown in this species (Galli et al, 2005a) and caused marked decreases in P CV and MCFP, which indicate that NO has a marked effect on the veins in this species. In trout, injection of SNP had no effect on either P CV or VS and only slightly decreased MCFP (Olson et al, 1997), whereas in toads, SNP caused dilatation of the central veins (Broughton and Donald, 2005).…”

Section: The Effect Of No On the Venous Systemsupporting

confidence: 82%

“…It is well established that SNP reduces systemic resistance in reptiles (Crossley et al, 2000;Galli et al, 2005a;Skovgaard et al, in press) and dilates central veins from Elaphe in vitro (Conklin et al, 1996). The effect of NO on the venous circulation of reptiles, however, has not been investigated in vivo.…”

Section: The Effect Of No On the Venous Systemmentioning

confidence: 99%

Venous tone and cardiac function in the South American rattlesnakeCrotalus durissus: mean circulatory filling pressure during adrenergic stimulation in anaesthetised and fully recovered animals

Skals

Skovgaard

Abe

et al. 2005

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venous tone, adrenaline as well as phenylephrine and isoproterenol (␣ ␣-and ␤ ␤-adrenergic agonists, respectively) were infused as bolus injections (2 and 10· g·kg -1 ). Adrenaline and phenylephrine caused large increases in MCFP and P CV , whereas isoproterenol decreased both parameters. This was also the case in fully recovered snakes. Therefore, adrenaline affects venous tone through both ␣ ␣-and ␤ ␤-adrenergic receptors, but the ␣ ␣-adrenergic receptor dominates at the dosages used in the present study. Injection of the nitric oxide donor SNP caused a significant decrease in P CV and MCFP. Thus, nitric oxide seems to affect venous tone.

“…Many studies in non-mammalian vertebrates (birds, reptiles, amphibians and teleost fishes) have shown that NO mediates vasorelaxation (Olson and Villa, 1991;Knight and Burnstock, 1993;Knight and Burnstock, 1996;Nilsson and Soderstrom, 1997; Martinez-Lemus et al, 1999; Crossley et al, 2000; Axelsson et al, 2001;Broughton and Donald, 2002;Jennings et al, 2004;Broughton and Donald, 2005;Galli et al, 2005;Skovgaard et al, 2005), but there is some controversy as to whether the vascular endothelium synthesises and releases NO in fishes and amphibians. A number of studies have provided evidence that endothelial NO signalling is present in the vasculature of fishes (Mustafa and Agnisola, 1998;Fritsche et al, 2000;Pellegrino et al, 2002) and amphibians (Rumbaut et al, 1995;Knight and Burnstock, 1996).…”

Section: Introductionmentioning

confidence: 99%

Dual mechanisms for nitric oxide control of large arteries in the estuarine crocodile Crocodylus porosus

Broughton

Donald

2007

SUMMARY In reptiles, accumulating evidence suggests that nitric oxide (NO) induces a potent relaxation in the systemic vasculature. However, very few studies have examined the source from which NO is derived. Therefore, the present study used both anatomical and physiological approaches to establish whether NO-mediated vasodilation is via an endothelial or neural NO pathway in the large arteries of the estuarine crocodile Crocodylus porosus. Specific endothelial nitric oxide synthase (NOS) staining was observed in aortic endothelial cells following nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) histochemistry and endothelial NOS immunohistochemistry (IHC), suggesting that an endothelial NO pathway is involved in vascular control. This finding was supported by in vitroorgan bath physiology, which demonstrated that the relaxation induced by acetylcholine (10-5 mol l-1) was abolished in the presence of the NOS inhibitor, N-omega-nitro-l-arginine(l-NNA; 10-4 mol l-1), the soluble guanylyl cyclase inhibitor, 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ;10-5 mol l-1), or when the endothelium was removed. Interestingly, evidence for a neural NO pathway was also identified in large arteries of the crocodile. Neural NOS was located in perivascular nerves of the major blood vessels following NADPH-d histochemistry and neural NOS IHC and in isolated aortic rings, l-NNA and ODQ, but not the removal of the endothelium, abolished the relaxation effect of the neural NOS agonist,nicotine (3×10-4 mol l-1). Thus, we conclude that the large arteries of C. porosus are potentially regulated by NO-derived from both endothelial and neural NOS.