The persistently beating hagfish heart

Abstract

To elucidate the evolution of autonomic cardiac reflexes in primitive chordates, we measured isometric force and trans-gap action potentials in ventricular and atrial strips (diameter 0.6-0.8 mm) from the systemic heart of the Atlantic hagfish, Myxine glutinosa. All parts of the heart paced spontaneously with a frequency, that at all temperatures was ∼30% faster for atrial than for ventricular tissue. Active force development increased with stretch, and remained high as passive force rose concurrently. In spite of the low blood pressure of hagfish, the maximal contractile force (∼60 mN/mm2) was comparable to that of higher vertebrates. Electrical stimulation at frequencies higher than the inherent, demonstrated capture and refractoriness consistent with the atrial pacing observed in the intact heart. The isometric twitches that developed during the long lasting plateaus of the action potentials were relatively insensitive to [Na+]o, [Ca2+]o, epinephrine, and carbachol, but were promptly abolished by depolarization by [K+]o. Beat kinetics showed no indication of releasable intracellular Ca2+ stores. KCl-contractures developed extremely slowly and were insensitive to epinephrine. In addition, we report a partial sequencing (1077 bp) of the cardiac Na+-Ca2+ exchanger using degenerate CODEHOP primers determined from known marine species Na+-Ca2+ exchangers. It was surprising, therefore, that the sequencing of the Na+-Ca2+ exchanger showed both a putative PKA site and indication of the typical “cardiac” splicing pattern of NCX1 (exon pattern ACDEF). The results are compared to similar measurements from tunicates, sharks, and higher vertebrates. The most surprising finding is the ability of all parts of the heart to generate pacemaker activity at a frequency close to that of the heart in situ.