Muscle microvasculature's structural and functional specializations facilitate muscle metabolism

Abstract

We review the evolving findings from studies that examine the relationship between the structural and functional properties of skeletal muscle's vasculature and muscle metabolism. Unique aspects of the organization of the muscle microvasculature are highlighted. We discuss the role of vasomotion at the microscopic level and of flowmotion at the tissue level as modulators of perfusion distribution in muscle. We then consider in some detail how insulin and exercise each modulate muscle perfusion at both the microvascular and whole tissue level. The central role of the vascular endothelial cell in modulating both perfusion and transendothelial insulin and nutrient transport is also reviewed. The relationship between muscle metabolic insulin resistance and the vascular action of insulin in muscle continues to indicate an important role for the microvasculature as a target for insulin action and that impairing insulin's microvascular action significantly affects body glucose metabolism.

Keywords: endothelium; flowmotion; insulin resistance; muscle microvasculature; vasomotion.

Fig. 1.

Schematic representation of muscle's vascular architecture. Left: arterioles branch off primary arteries down to terminal arterioles; these are oriented perpendicular to muscle fibers. Top right: 2 muscle fibers and their microvascular units, with terminal arterioles (red) feeding multiple capillaries (red to blue) as the smallest unit of control and lymph vessels (green) ascending along arterioles and venules (blue). In resting muscle (top fiber), the microvasculature is intermittently and not equally perfused. Insulin and exercise can each stimulate muscle (bottom fiber) and induce vasodilation at the level of the terminal arterioles and enhance perfusion. Bottom right: magnification of a capillary embedded in a sarcolemma “channel,” thereby expanding the contact area between myocytes and endothelial cells. Myocyte mitochondria cluster along the embedded capillary, thereby reducing the distance oxygen and nutrients need to diffuse. Illustration provided by MediCorporate bv/D & L Graphics (www.dlgraphics.nl).

Fig. 2.

Top: contrast-enhanced ultrasound images of rat thigh muscle as a function of time after a high-energy ultrasound pulse with the muscle at rest or given a 1-Hz electrical stimulation. Bottom: greater plateau video intensity (red) corresponding to a larger number of microbubbles in the imaged volume of the stimulated muscle.