Shortening Heat In Cardiac Muscle

Abstract

The ‘heat of shortening’ in muscle was first demonstrated by Fenn (1923). Tectanically‐contracting skeletal muscle, released to shorten at a fixed afterload, was shown to produce heat at a rate in excess of the steady‐state isometric heat rate. Subsequent studies in the following decades have provided ample evidence to support the existence of shortening heat in skeletal muscle. The situation is much less clear in cardiac muscle. Using the ‘latency release’ method, Holroyd and Gibbs (1992) showed that no heat was liberated when cardiac muscle was shortened against zero afterload. Adding legitimacy to the latency release protocol, its use showed the existence of shortening heat in both fast‐twitch and slow‐twitch hind‐limb muscles of the rat. (Holroyd et al., 1996). Since that time, the existence of shortening heat in cardiac muscle seems not to have been further investigated, leaving the field in the curious situation that shortening heat is present in skeletal muscle but not in cardiac muscle, despite their micro‐structural similarities. Since it must be imagined that shortening heat is the thermal accompaniment of cross‐bridge cycling, and its attendant thermogenic ATP hydrolysis, we undertake a re‐examination of the issue. We do so using two independent approaches.Firstly, we quantify shortening heat in isolated preparations (right ventricular trabeculae carneae) from rat hearts. Trabeculae were dissected from the left ventricles of 14–16 week old male Sprague‐Dawley rats and mounted in a flow‐through microcalorimeter at 32 °C, as previously described (Taberner et al., 2011). The muscle was subjected to a series of steady‐state trains of isotonic contractions at progressively diminishing afterloads, and isometric contractions at progressively diminishing muscle lengths. Shortening heat is defined as the difference in twitch heat between these two modes of contractions at a given afterload. Secondly, experimental findings are complemented by predictions of cross‐bridge ATP hydrolysis from a thermodynamically‐constrained, mathematical model of cardiac muscle mechano‐energetics (Tran et al., 2010). In both cases we exploit the difference of enthalpy‐load relations between isometric and isotonic contractions, while ensuring that comparisons are performed at the same peak force.Our experimental results confirm the existence of shortening heat in rat trabeculae. The magnitude of shortening heat was inversely related to the afterload and was a monotonically‐increasing function of the ‘extent of shortening’. Computational simulations reveal that the heat of shortening arises from the cycling of cross‐bridges, and that, even at very low afterloads where no external work is done, there is always a component of energy that is dissipated as heat.