Neural modulation of transcapillary exchange of fluid and solutes in whole-organ preparations

Abstract

Activation of sympathetic adrenergic postganglionic fibers that release norepinephrine at the neuromuscular junction can influence resistance, capacitance, and exchange functions in the microcirculation. Although the predominant response is an increase in precapillary resistance that reduces blood flow through the tissue (at constant pressure perfusion), there are two distinct components that can be separated into an initial (1-2 minute) and late (2-15-minute) response. The initial (1-2-minute) response is a decrease in venous and capillary pressures in passive response to decreased flow promoted by an increase in precapillary resistance. Venous pressures are reduced even though postcapillary resistance is increased. The decrease in capillary pressure promotes absorption of fluid from tissue to plasma. Venous constriction results in a translocation of blood from the terminal venous system into the larger venous conduits toward the heart. Total blood volume in an isolated organ system decreases and is manifested as a decrease in volume (plethysmographic) or weight (gravimetric). The decrease in volume is a result of three interrelated factors: 1) decrease in flow through the organ, 2) active venoconstriction and a translocation of blood out of the organ, and 3) absorption of fluid from tissue to plasma, which flows out of the organ with venous drainage. With continued sympathetic nervous system stimulation, the late response (3-15 minutes) is a gradual decrease in precapillary resistance that increases blood flow through the organ. Venous and capillary pressures passively increase in association with increases in flow. The mechanism of the decrease in precapillary resistance, which has been labelled sympathetic or autoregulatory 'escape,' has never been clearly identified but has been attributed to the accumulation of vasodilator metabolites. Precapillary resistance decreases and approaches control in skeletal muscle and skin, returns to control rapidly in the intestine, and appears to be reasonably well maintained in adipose tissue. As measured by filtration coefficients, capillary surface area appears to be unaffected or increased in skeletal muscle and skin, remains decreased in the intestine, and may be increased in adipose tissue. This demonstrates that precapillary sphincters (or terminal arterioles) controlling flow to the capillary exchange surface area respond to a sympathetic neural stimulus different than other precapillary resistance vessels. In every organ, except adipose tissue, in which measurements have been made, the transcapillary exchange of solutes is decreased during sympathetic neural stimulation. This results from a decrease in flow and a decrease in delivery of solute to the exchange surface area. Decreased exchange may also result from a decrease in surface area available for exchange by mechanisms that alter the distribution of flow to those tissue elements where exchange does not readily occur. The exact mechanisms relating to this complex response have not been clearly defined. In adipose tissue only, it appears that sympathetic neural stimulation may alter capillary membrane structure to cause an increase in capillary permeability to solutes.