Autonomic regulation of the heart during digestion and aerobic swimming in the European sea bass (Dicentrarchus labrax)

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Abstract

The autonomic regulation of the heart was studied in European sea bass (Dicentrarchus labrax) during digestion and aerobic exercise by measuring cardiac output (Q), heart rate (fH), stroke volume (Vs) and oxygen consumption (MO2) before and after pharmacological blockade by intraperitoneal injections of atropine and propranolol. The significant rise in MO2 (134 ± 14 to 174 ± 14 mg kg1 h1) 6 h after feeding (3% body mass) caused a significant tachycardia (47.7 ± 10.9 to 72.6 ± 7.2 beats min1), but only a small elevation of Q. MO2 of fasting fish increased progressively with swimming speed (0.7–2.1 BL s1) causing a significant tachycardia (43 ± 6 to 61 ± 4 mL min1 kg1) and increased Q but Vs did not change. Inactive fish were characterized by a high vagal tone (98.3 ± 21.7%), and the tachycardia during digestion and exercise was exclusively due to a reduction of vagal tone, while the adrenergic tone remained low during all conditions. Intrinsic fH, revealed after double autonomic blockade, was not affected by digestion (71 ± 4 and 70 ± 6 min1, respectively), indicating that non-adrenergic, non-cholinergic (NANC) factors do not contribute to the tachycardia during digestion in sea bass.

Introduction

Teleost fish regulate the heart and the circulatory system to provide adequate amounts of oxygen and nutrients to all tissues and organ systems, and the increased metabolic demands of the gastrointestinal organs during digestion, or the red muscle during sustained aerobic exercise, are met by a rise in cardiac output (Q) (Jones and Randall, 1978, Olson and Farrell, 2006, Altimiras et al., 2008). The rise in Q can result from elevations in heart rate (fH) and/or stroke volume (Vs) that, by en large, are controlled by the autonomic nervous system (e.g. Olson and Farrell, 2006, Cameron, 1978). Although early studies indicated that teleosts lack a sympathetic excitatory innervation of the heart, it is now widely accepted that teleosts are the earliest group of vertebrates to have evolved double innervation of the heart (e.g. Donald and Campbell, 1982, Taylor et al., 1999), where the parasympathetic cholinergic innervation using acetylcholine as transmitter slows fH (Young, 1936, Randall, 1966, Cameron, 1978, Holmgren, 1977, Holmgren, 1981), while the sympathetic innervation elicits positive chronotropic and inotropic effects via β-adrenoceptors (Holmgren, 1977, Cameron and Brown, 1981, Davies and Kubin, 1986). Thus, increased fH and Q could follow an increase in sympathetic nerve activity or a withdrawal of the inhibitory vagal innervation. In addition, there is beat-to-beat modulation by the respiratory cycle, which also contributes to the autonomic control of the heart (Taylor, 1992, Taylor et al., 2006). Circulating catecholamines released from the chromaffin tissue may also contribute to the tachycardia during exercise (Cameron, 1978). Furthermore, non-adrenergic, non-cholinergic (NANC) factors, released from the digestive organs, may also contribute to postprandial tachycardia (e.g. Wang et al., 2001, Skovgaard et al., 2009), but this possibility has not been addressed in fish.

The European sea bass (Dicentrarchus labrax), a perciform fish of the family Moronidae, is an athletic predator that can forage and migrate over long distances. It can consume large prey items, which it catches by pursuit (Pickett and Pawson, 1994). The sea bass shows pronounced increases in oxygen uptake (MO2) and Q after feeding (Axelsson et al., 2002, Altimiras et al., 2008, Dupont-Prinet et al., 2009) and during sustained aerobic exercise (Chatelier et al., 2005, Chatelier et al., 2006, Sandblom et al., 2005). Because these variations in Q are almost exclusively due to changes in fH rather than Vs (Chatelier et al., 2005, Chatelier et al., 2006, Sandblom et al., 2005, Altimiras et al., 2008, Dupont-Prinet et al., 2009), the sea bass is an interesting species to study autonomic regulation of heart rate in response to increased metabolic demands. Our objective, therefore, was to investigate autonomic control of the heart during digestion and incremental aerobic exercise. Sea bass were instrumented with flow probes to measure Q, fH and Vs, and the contribution of the sympathetic and parasympathetic systems to the cardiovascular responses was assessed by autonomic blockade with the β-adrenergic antagonist propranolol and the muscarinic antagonist atropine. This permitted calculation of cholinergic and adrenergic tones and revealed whether NANC factors contributed to cardiac control after feeding. Simultaneous measurements were made of oxygen uptake (MO2) to confirm that cardiac changes were directly related to increased metabolic demand, and to compare these relationships between feeding and exercise.

Section snippets

Experimental animals

Twenty-five European sea bass (D. labrax, Linneaus, 1758) of both sexes with a mean body mass of 379 ± 16 g were obtained from Extramer SrL (Salses le Chateau, Roussillon, France). They were transported to Station Méditerranéenne de l'Environnement Littoral in Séte (France), where they were kept in large tanks with recirculating, aerated and biofiltered seawater at 22 °C, a salinity of 35‰ and a natural photoperiod. They were fed with dry fish pellets every 24 h, but fasted for 48 h prior to surgery

Results

The cardiovascular variables and MO2 of inactive and digesting fish are summarised in Table 1. Atropine caused the expected rise in fH in inactive fish, and a significant rise in Q, although Vs decreased. β-adrenergic blockade had opposite effects, causing Q and fH to decline while Vs rose. fH of double-blocked fish remained significantly higher than untreated fish. Despite these marked cardiovascular effects, autonomic blockade had no significant effects on MO2 of inactive fish. The

Discussion

Our study demonstrates that release of an inhibitory cholinergic tone is the primary mechanism for adjusting fH when metabolism increases during digestion or sustained aerobic exercise in sea bass, while the adrenergic tone remained low during all conditions. Consistent with this dominance of cholinergic tone, the variation in fH among individual inactive fish could be explained by differences in the inhibitory tonus (Fig. 2), indicating that vagal control of the heart mediates most of the fH

Acknowledgements

This research was supported by the Centre National de la Recherche Scientifique (CNRS), the Danish Research Council and the Université Montpellier 2 (UM2). AD-P was supported by a doctoral grant from the CNRS and the Région Languedoc-Roussillon (RLR). TW was a visiting scientist at the UM2, in receipt of a fellowship from the RLR. The Ambassade de France in Copenhagen contributed to the travel costs of NKI and TW.

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