Venous tone and cardiac function in the South American rattlesnake<i>Crotalus durissus</i>: mean circulatory filling pressure during adrenergic stimulation in anaesthetised and fully recovered animals

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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 mobilization of unstressed volume is primarily caused by venoconstriction, as the venous circulation holds approximately two-thirds of the total blood volume (Rothe, 1993;Sandblom and Axelsson, 2007). As the veins in pythons and other vertebrates are under adrenergic control, the shift from inactive to active blood volume is likely to reflect an increased sympathetic tone, consistent with studies on rattlesnakes, various fish and mammals that report an increase in both P CV and MCFP because of an α-adrenergic stimulation (Lillywhite, 1987;Pang, 2001;Sandblom and Axelsson, 2007;Skals et al, 2005). In addition to a sympathetic regulation of venous tone, it is an intriguing possibility that the expansion of the stomach upon ingestion of the large prey may reduce unstressed volume by squeezing the veins.…”

Section: Discussionsupporting

confidence: 75%

“…Pentobarbital anaesthesia does, however, mute autonomic regulation in reptiles (e.g. Crossley et al, 1998;Skals et al, 2005), and the typical withdrawal of parasympathetic tone is likely to explain the higher f H of the anaesthetized pythons than in previous studies on fully recovered pythons (Enok et al, 2012;Skovgaard et al, 2009). The lack of body movement during anaesthesia may also affect venous return, but will do so similarly in both groups and therefore have little effect on a comparison of cardiovascular parameters.…”

Section: Discussionmentioning

confidence: 93%

“…These barostatic mechanisms, including vascular constriction (Pang, 2001), are rapidly activated in mammals and trout (Guyton, 1981;Sandblom and Axelsson, 2007), but seem delayed in rattlesnakes (Skals et al, 2005) and will result in overestimates of MCFP. This overestimation is likely to be most pronounced in the fasting snakes because of the longer time course for equilibration, and would therefore tend to reduce the reported difference in MCFP between fasting and digesting snakes.…”

Section: Discussionmentioning

confidence: 99%

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Improved cardiac filling facilitates the postprandial elevation of stroke volume inPython regius

Enok

Leite

et al. 2016

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To accommodate the pronounced metabolic response to digestion, pythons increase heart rate and elevate stroke volume, where the latter has been ascribed to a massive and fast cardiac hypertrophy. However, numerous recent studies show that heart mass rarely increases, even upon ingestion of large meals, and we therefore explored the possibility that a rise in mean circulatory filling pressure (MCFP) serves to elevate venous pressure and cardiac filling during digestion. To this end, we measured blood flows and pressures in anaesthetized Python regius. The anaesthetized snakes exhibited the archetypal tachycardia as well as a rise in both venous pressure and MCFP that fully account for the approximate doubling of stroke volume. There was no rise in blood volume and the elevated MCFP must therefore stem from increased vascular tone, possibly by means of increased sympathetic tone on the veins. Furthermore, although both venous pressure and MCFP increased during volume loading, there was no evidence that postprandial hearts were endowed with an additional capacity to elevate stroke volume. In vitro measurements of force development of paced ventricular strips also failed to reveal signs of increased contractility, but the postprandial hearts had higher activities of cytochrome oxidase and pyruvate kinase, which probably serves to sustain the rise in cardiac work during digestion.

“…Sandblom et al, 2005;Skals et al, 2005Skals et al, , 2006Enok et al, 2016). By mobilizing blood from the veins, preload pressure may be maintained, or even increased, despite the increased heart rate during activity (Sandblom et al, 2005;Skals et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Autoregulation of cardiac output is overcome by adrenergic stimulation in the anaconda heart

Joyce

Axelsson

Wang

2016

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Most vertebrates increase cardiac output during activity by elevating heart rate with relatively stable stroke volume. However, several studies have demonstrated 'intrinsic autoregulation' of cardiac output where artificially increased heart rate is associated with decreased stroke volume, leaving cardiac output unchanged. We explored the capacity of noradrenaline to overcome autoregulation in the anaconda heart. Electrically pacing in situ perfused hearts from the intrinsic heart rate to the maximum attainable resulted in a proportional decrease in stroke volume. However, noradrenaline, which increased heart rate to the same frequency as pacing, maintained stroke volume and thus increased cardiac output. In atrial and ventricular preparations, noradrenaline significantly increased the force of contraction and contraction kinetics. Thus, the increased contractility associated with adrenergic stimulation ameliorates filling limitations at high heart rates. Although heart rate appears the primary regulated variable during activity, this may only be achieved with compensatory amendments in myocardial contractility provided by adrenergic stimulation.