Form follows function: developmental and physiological view on ventricular myocardial architecture

Abstract

The arrangement of myocytes within the ventricle is critical for its contractile performance, as evidenced by significant functional impairment seen in cardiomyopathies associated with myofiber disarray or post-infarction remodeling. A review on this topic by Anderson and associates provides anatomical insight gained from a multitude of approaches, and concludes that the best concept is that of syncytial continuum with supporting collagenous matrix. The overall arrangement is in the form of several intertwined helices, and the authors find no support for a recently suggested ventricular myocardial band hypothesis. This commentary aims at providing a developmental and physiological perspective on this purely anatomical concept. Unlike some other organ systems, the developing heart has to function since very early stages to support the oxygen and nutrition demands of the growing embryo, thus putting some constraints on heart development. The ventricular myocardial architecture transforms from a single-layered tube through trabeculated stages into a mature form that relies on a multi-layered compact zone. The first evidence of helical patterns is found in trabeculated hearts during ventricular contraction, and layers with different helix pitch develop during later fetal stages as the compact zone thickens. The second major point determining ventricular contraction is the sequence of its electrical activation. The ventricular activation sequence changes concomitantly with its morphology, from slow peristaltoid through base-to-apex pattern found in looped trabeculated hearts, to mature apex-to-base direction. Thus, adult ventricular myocardial architecture is best understood when one also considers the way it developed together with its electrical activation sequence and contraction pattern.

Figure 1.

Development of ventricular myocardial architecture and is activation sequence. Top panels: The tubular heart. A cross section through embryonic day (ED) 2.5 chick ventricle reveals the outer myocardial mantle (Myo), separated from the endocardium (Endo) by cardiac jelly (CJ). Electrical activation at these stages proceeds in a slow and fairly isotropic fashion from the venous pole towards the aortic sac. Middle panels: Trabeculated pre-septation heart. Ventricular lumen at ED4.5 is filled with three-dimensional trabecular network in both left (LV) and right (RV) ventricles. The outside compact layer (CL) is very thin. Electrical activation of these ventricles is much more rapid in comparison with the previous stage, but still proceeds from the preferentially left-sided atrio-ventricular junction towards the right-sided outflow tract. The bottom panels show the mostly compacted nature of the left ventricular myocardium at ED10, although the three spiral layers are not yet very distinct. Activation proceeds in a mature apex-to-base pattern, revealing functionality of both bundle branches. Scale bars are 100 micrometers; asterisks mark the earliest activated ventricular region and arrows indicate the direction of electrical impulse propagation. Original data generated in context of studies cited in the text [5, 16, 19].