Transitions in ventricular activation revealed by two‐dimensional optical mapping

Abstract

While cardiac function in the mature heart is dependent on a properly functioning His-Purkinje system, the early embryonic tubular heart efficiently pumps blood without a distinct specialized conduction system. Although His-Purkinje system precursors have been identified using immunohistological techniques in the looped heart, little is known whether these precursors function electrically. To address this question, we used high-resolution optical mapping and fluorescent dyes with two CCD cameras to describe the motion-corrected activation patterns of 76 embryonic chick hearts from tubular stages (stage 10) to mature septated hearts (stage 35). Ventricular activation in the tubular looped heart (stages 10 -17) using both calcium-sensitive fluo-4 and voltage-sensitive di-4-ANEPPS shows sequentially uniform propagation. In late looped hearts (stages 18 -22), domains of the dorsal and lateral ventricle are preferentially activated before spreading to the remaining myocardium and show alternating regions of fast and slow propagation. During stages 22-26, action potentials arise from the dorsal ventricle. By stages 27-29, action potential breakthrough is also observed at the right ventricle apex. By stage 31, activation of the heart proceeds from foci at the apex and dorsal surface of the heart. The breakthrough foci correspond to regions where putative conduction system precursors have been identified immunohistologically. To date, our study represents the most detailed electrophysiological characterization of the embryonic heart between the looped and preseptated stages and suggests that ventricular activation undergoes a gradual transformation from sequential to a mature pattern with right and left epicardial breakthroughs. Our investigation suggests that cardiac conduction system precursors may be electrophysiologically distinct and mature gradually throughout cardiac morphogenesis in the chick.

Atrioventricular Ring Reentry in Embryonic Mouse Hearts

“…In E10.5 and E11.5 hearts, however, the earliest ventricular activation occurred at the apex, consistent with a maturing conduction system, as suggested previously ( Figure 3 for E9.5 and E10.5, Figure 2 for E11.5). 1,2,6,7 The close agreement between activation sequences in voltage and Ca 2ϩ maps 7 validates the use of Ca 2ϩ transients to map activation sequence.…”

How does the tubular embryonic heart work? Looking for the physical mechanism generating unidirectional blood flow in the valveless embryonic heart tube

“…Corresponding observations were made in intact embryonic chick heart tubes in which the segments were electrically isolated from each other by the placement of ligatures around the tube (Pickering, 1893;Johnstone, 1924). Optical mapping of the electrical activity of the myocardium of the tubular embryonic chick heart has uncovered spatiotemporal sequences of periodic electrical activation that correspond to the propagation pattern of its traveling contractile waves (Chuck et al, 2004;Sedmera et al, 2004). In view of the fact that myocardial contraction is coupled to electric activation, this observation may be regarded as a strong evidence for an active nature of the traveling contractile waves.…”

Persistence of Functional Atrioventricular Accessory Pathways in Postseptated Embryonic Avian Hearts

“…11 Ultimately, however, ventricular activation shifts from this immature base-to-apex sequence to a mature apex-to-base pattern. [12][13][14][15][16][17][18] This transition in ventricular activation pattern reflects maturation of the His-Purkinje system (HPS) and coincides with completion of ventricular septation. 12,16 Importantly, and almost simultaneously, the existing AV myocardial continuity, which is present on the entire circumference of the AV junction in the looped embryonic heart, disappears because of formation of the fibrous annulus.…”