Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog

Abstract

We have studied the three-dimensional arrangement of ventricular muscle cells and the associated extracellular connective tissue matrix in dog hearts. Four hearts were potassium-arrested, excised, and perfusion-fixed at zero transmural pressure. Full-thickness segments were cut from the right and left ventricular walls at a series of precisely located sites. Morphology was visualized macroscopically and with scanning electron microscopy in 1) transmural planes of section and 2) planes tangential to the epicardial surface. The appearance of all specimens was consistent with an ordered laminar arrangement of myocytes with extensive cleavage planes between muscle layers. These planes ran radially from endocardium toward epicardium in transmural section and coincided with the local muscle fiber orientation in tangential section. Stereological techniques were used to quantify aspects of this organization. There was no consistent variation in the cellular organization of muscle layers (48.4 +/- 20.4 microns thick and 4 +/- 2 myocytes across) transmurally or in different ventricular regions (23 sites in 6 segments), but there was significant transmural variation in the coupling between adjacent layers. The number of branches between layers decreased twofold from subepicardium to midwall, whereas the length distribution of perimysial collagen fibers connecting muscle layers was greatest in the midwall. We conclude that ventricular myocardium is not a uniformly branching continuum but a laminar hierarchy in which it is possible to identify three axes of material symmetry at any point.

Variability of the Human Cardiac Laminar Structure

“…The variability of the laminar sheet can be measured with the probability distribution of the intersection angle of the third eigenvector (i.e., of the laminar sheet normal). The intersection angle [16] is defined as the projected angle of the laminar sheet normal (in red in the right figure) onto a transverse plane (the vertical transmural plane in green in the right figure). A prolate ellipsoidal model of the heart [20] is fitted to the morphology of the statistical atlas to ease measurements in the prolate ellipsoidal coordinates.…”

“…The heart is a complex muscle that is composed with myocardial fibers organized as laminar sheets [25,16]. The cardiac fiber structures have an important role in electrophysiology [14] and in mechanical functions [6] of the heart.…”

Construction and validation of anisotropic and orthotropic ventricular geometries for quantitative predictive cardiac electrophysiology

“…Figure 2a shows a 30 mm magnetic resonance image of a short-axis section through a rat heart: individual cells are not discernible at this resolution, but cleavage planes are clearly visible. LeGrice et al [35] proposed an organization of the fibres into a laminar structure with cleavage planes that ran radially from the endocardium to the epicardium and, when viewed in a long-axis transmural plane, could be seen to shift from a base -apex direction near the apex through to an apex -base direction in basal regions. Three-dimensional histology has demonstrated that rat myocytes are grouped in layers three or four cells thick (referred to as sheets) separated by cleavage planes [36].…”

Cardiac Basal Metabolism.

“…These preparations have been employed for some time [73][74][75], but have undergone a recent resurgence by using improved technology [76][77][78]. Two major and related concerns have been addressed [75,77]: (1) What is the depth of damage because of cutting per se on each face of a tissue slice, and (2) given the complex microarchitecture of the heart [79], what fraction of myocytes has been severed because of their oblique orientation with respect to the plane of the slice? Quantitative uncertainty regarding these questions is compounded by qualitative uncertainty regarding the metabolic effect of either "error."…”