Contractile properties of the functionally divided python heart: Two sides of the same matter

doi:10.1016/j.cbpa.2006.10.015

Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology

Volume 146, Issue 2, February 2007, Pages 163-173

https://doi.org/10.1016/j.cbpa.2006.10.015 Get rights and content

Abstract

The heart of Python regius is functionally divided so that systemic blood pressure is much higher than pulmonary pressure (6.6 ± 1.0 and 0.7 ± 0.1 kPa, respectively). The present study shows that force production of cardiac strips from the cavum arteriosum and cavum pulmonale exhibits similar force production when stimulated in vitro. The high systemic blood pressure is caused, therefore, by a thicker ventricular wall surrounding the cavum arteriosum rather than differences in the intrinsic properties of the cardiac tissues. Similarly, there were no differences between the contractile properties of right and left atria. Force production was similar in atria and ventricle but the atria contracted and relaxed much faster than the ventricle. Graded hypoxia markedly reduced twitch force of all four cardiac tissues, and this was most pronounced when PO₂ was below 40 kPa. In contrast, the four cardiac tissues were insensitive to acidosis during normoxia although acidosis increased the sensitivity to hypoxia. Adrenergic stimulation increased twitch force of all cardiac tissues, while cholinergic stimulation only affected the atria and reduced twitch force markedly. In spite of the different oxygen availability of the two sides of the heart, the biochemical and functional properties are alike and the differences may instead be overcome by the coronary blood supply.

Introduction

The heart of most non-crocodilian reptiles consists of two separate atria and an incompletely divided ventricle causing equal pressures in the systemic and pulmonary arteries (e.g. Hicks, 1998). Varanid lizards and Burmese python are exceptions to this general pattern. In these animals the muscular ridge that separates the two sides of the ventricle is exceptionally well-developed and provides a functional separation of blood flows and pressures, so that systemic blood pressure can greatly exceed pulmonary pressure (Burggren and Johansen, 1982, Wang et al., 2002, Wang et al., 2003a). The functional separation entails that the left side of the ventricle, the cavum arteriosum (CA), generates more work than the right side of the ventricle, the cavum pulmonale (CP). This correlates with a thicker ventricular wall surrounding the CA (Farrell et al., 1998), but it is not known whether there is also a fundamental difference in the contractile and biochemical capacity or sensitivity to neurotransmitters between the two sides of the heart. A central purpose of the present study was to investigate such putative differences in intrinsic performance.

As an additional consequence of the functional separation of the ventricle, the CP only receives deoxygenated blood from the systemic circulation, while CA receives oxygenated blood returning from the lung. The difference in oxygen availability is a likely explanation to why CA consists partly of a spongeous endocardium devoid of coronary supply, while CP exclusively consists of compact, coronary supplied cardiac tissue (Farrell et al., 1998). Nevertheless, a well-developed coronary system supplies the compact layer on both sides of the heart with oxygenated blood (MacKinnon and Heatwole, 1981). Given the difference in cardiac anatomy and possible differences in oxygen levels of the two sides, we investigated whether the CP and the right atrium (RAt) differ from the CA and the left atrium (LAt) with respect to their tolerance to hypoxia and acidosis.

The present study evaluates cardiac performance of the royal python, Python regius, in terms of functional and biochemical differences of the LAt, RAt, CA and CP. This was done by measurements of: (1) in vivo blood pressures of unanaesthetised snakes; (2) in vitro isometrically force-developing muscle strips of the four different cardiac tissues during control conditions, graded hypoxia and acidosis; (3) adrenergic and cholinergic influence on force-development, and (4) capacities of ATP production and ATP-buffering assessed from in vitro activities of key enzymes.

Section snippets

Animals

Thirteen P. regius of undetermined sex (five adult and eight neonate snakes with the mass of 466 ± 61 g and 102 ± 18 g, respectively) were obtained from commercial suppliers and housed in temperature controlled (23–28 °C) terrariums at The University of Aarhus. Each terrarium was equipped with a heating lamp to allow for behavioural thermoregulation on a 12/12 h day/night cycle. The snakes were fed mice or rats regularly and had free access to clean water. Food was withheld for more than four days

In vivo blood pressures in the systemic and pulmonary circulations

Fig. 2A shows a typical recording of simultaneous measurements of P_sys and P_pul in a resting snake. P_sys was, on average, nine times higher than P_pul (Fig. 2B; 6.6 ± 1.0 and 0.7 ± 0.1 kPa, respectively), and the pressure separation between the two circuits persisted throughout the cardiac cycle (Fig. 2A). Average heart rate of the four undisturbed snakes was 21.6 ± 3.5 beats min^− 1.

In vitro measurements of isometric contractions of cardiac tissues

The cross-sectional areas of the cardiac strips, calculated from weight and length, were 1.15 ± 0.18 mm² for CA, 0.96 ±

Discussion

Systemic blood pressure of unanaesthetised P. regius exceeded pulmonary pressure by approximately nine times, which is similar to the blood pressures recorded in the closely related Python molurus (Wang et al., 2003a). Although high P_sys has been measured in other snakes (Johansen, 1959, Lillywhite and Seymour, 1978, Wang et al., 2001), the profound pressure separation is unusual for reptiles, so pythons, together with varanid lizards, are exceptional in their capacities to maintain low P_pul

Conclusion

The heart of P. regius exhibits pronounced pressure separation, but the almost ten-fold higher cardiac work of the systemic side of the ventricle is not reflected in measurable differences in the inherent contractile and biochemical properties. It seems, therefore, that the ability to produce different blood pressures in vivo is achieved by a difference in thickness of the ventricular walls surrounding the two main ventricular chambers. Also, the sensitivity to hypoxia was remarkably similar on

Acknowledgements

This study was supported by The Novo Fund and The Danish Research Council. We appreciate Dr. Johnnie Andersen and Miss Gina Galli for comments that improved the manuscript.

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Contractile properties of the functionally divided python heart: Two sides of the same matter

Abstract

Introduction

Section snippets

Animals

In vivo blood pressures in the systemic and pulmonary circulations

In vitro measurements of isometric contractions of cardiac tissues

Discussion

Conclusion

Acknowledgements

Anim. Behav.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

J. Mol. Cell. Cardiol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol. A

Acidosis counteracts the negative inotropic effects of K+ on contractile properties of ventricular muscle strips from the toad Bufo marinus

Physiol. Biochem. Zool.

Cardiac excitation–contraction coupling

Nature

Ventricular haemodynamics in the monitor lizard Varanus exanthematicus: pulmonary and systemic pressure separation

J. Exp. Biol.

Vertebrate cardiovascular systems

Effects of detraining on enzymes of energy metabolism in individual human muscle fibers

Am. J. Physiol.

Creatine kinase, energy-rich phosphates and energy metabolism in heart muscle of different vertebrates

J. Comp. Physiol. B

Isoproterenol directly stimulates the Na+–K+ pump in isolated cardiac myocytes

Am. J. Physiol.

Energy metabolism and contractility in ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature

Physiol. Rev.

Matching of vertebrate cardiac energy demand to energy metabolism

Am. J. Physiol.

Comparative aspects of heart morphology

The adrenergic innervation of the cardio-vascular system of the lizard Trachysaurus rugosus

Z. Zellforsch.

Inotropic responses to drugs of isolated heart strips from a snake

Acta Physiol. Scand.

Cardiac shunting in reptiles: mechanisms, regulation, and physiological functions

Thermoregulation in a brooding female Indian python, Python molurus bivittatus

Science

Circulation in the three-chambered snake heart

Circ. Res.

Acidosis counteracts the negative inotropic effects of K⁺ on contractile properties of ventricular muscle strips from the toad Bufo marinus

Isoproterenol directly stimulates the Na⁺–K⁺ pump in isolated cardiac myocytes