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

TLDR

The authors examined the three‑dimensional arrangement of ventricular myocytes and connective tissue in four potassium‑arrested dog hearts, using perfusion fixation, full‑thickness sectioning, macroscopic and scanning electron microscopy in transmural and epicardial planes, and stereological quantification. They found that ventricular myocardium displays an ordered laminar architecture with radial cleavage planes, uniform cell‑layer thickness but variable inter‑layer coupling, a two‑fold reduction in branching from subepicardium to midwall, and longest perimysial collagen fibers in the midwall, indicating a laminar hierarchy with three material‑symmetry axes.

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.