Electrophysiological studies on initiation and reversal of the heart beat in Ciona intestinalis.

The heart of the tunicate Ciona intestinalis is a simple tube composed of epithelial muscle cells which—though isolated from any neural connexions—is capable of producing repeated contractions at reasonably constant frequency. It is thus a myogenic pacemaker system in which spontaneous rhythmic activity is derived from some intrinsic source. The simplicity of this system makes it a useful preparation for the study of pacemaker activity. The cells appear morphologically homogeneous; they are arranged in a single layer, and consequently activity initiates in and is propagated along the surface of a cylinder. The tubular nature of the heart makes analysis of the directionality of contractile events convenient, and it permits morphological and physiological characterization of the two ends. The tunicate heart exhibits a reversal phenomenon in which a-series of peristaltic contractile waves initiated at one end and conducted to the other is followed by a new series of contractions initiated at the previously passive end and conducted in the opposite direction. This phenomenon, which occurs intermittently and apparently without pattern, was first noted by van Hasselt (1824) and has puzzled workers for over 100 years. Several hypotheses have been developed to explain it (back pressure: Haywood & Moon (1950,1953), Kriebel(i964); pacemaker fatigue: Krijgsman(i956), Krijgsman & Krijgsman (1957); extrasystole: Mislin (1964, 1965), Mislin & Krause (1964); CO2 concentration: Brocas et al. (1966a, b); these will be considered later in light of data obtained in the present study. Millar (1953a) and Krijgsman (1956) have reviewed the observations made by early workers. In an effort to elucidate their organization and functional characteristics, cellular elements of the heart of Ciona intestinalis have been studied by extracellular and intracellular recording techniques. The results, together with light-microscopic and electron-microscopic observations, are used to construct a model of the interactions between cells and groups of cells that explains the mechanical phenomena observed.