Muscle length directs sympathetic nerve activity and vasomotor tone in resistance vessels of hamster retractor.

Abstract

Increased resistance to blood flow with muscle extension has been explained by the deformation of vessels within the muscle. In the present study, we developed a novel preparation of the hamster retractor muscle to investigate whether passive changes in skeletal muscle length elicit active vasomotor responses through a range of motion (85% to 130% of in vivo length; sarcomere length, 2.69 +/- 0.02 to 4.05 +/- 0.01 microns) encompassing the classic length-tension relationship. Arterioles (diameter, 32 +/- 3 microns) and feed arteries (diameter, 75 +/- 4 microns) were observed to progressively constrict (by 8 +/- 1 and 17 +/- 2 microns, respectively) with muscle lengthening, reducing blood flow by > 50%; reciprocal changes occurred with passive shortening. Sodium nitroprusside (10 mumol/L) dilated vessels (to 47 +/- 2 and 98 +/- 4 microns, respectively) and abolished vasomotor responses to changing muscle length. The coordination of vasomotor responses between arterioles and feed arteries maintained wall shear rate (control, 1764 +/- 200 s-1) and perfusion pressure (60 +/- 5 mm Hg) into the arteriolar network. Tetrodotoxin (TTX, 1 mumol/L), phentolamine (1 mumol/L), prazosin (0.1 mumol/L), or 6-hydroxydopamine (1 mmol/L) inhibited vasoconstrictor responses, indicating that action potentials initiated by muscle lengthening give rise to norepinephrine release from sympathetic nerves. As shown with glyoxylic acid staining, sympathetic nerves formed a plexus encompassing arterioles and feed arteries. To test for a reflexive response initiated by intramuscular mechanoreceptors, TTX was applied with micropipettes to proximal segments of feed arteries, thereby neurally "isolating" the muscle from the hamster. Whereas lengthening-induced vasoconstriction persisted in arterioles and in feed artery segments distal to TTX, there was no vasomotor response central to the block. We conclude that passive lengthening stimulates the activity of periarteriolar sympathetic nerves; this activity propagates antidromically along nerve fibers into the feed arteries. These findings identify a mechanotransduction sequence by which the length of skeletal muscle actively governs vasomotor tone and the supply of oxygen to muscle fibers.