The central hypothesis of this investigation is that a shortening myoc
yte generates a time-varying transmural pressure, or intracellular pre
ssure. A mathematical model was formulated for a single myocyte, consi
sting of a fluid-filled cylindrical shell with axially arranged contra
ctile filaments, to quantitate the fiberfluid interaction. In this mod
el, the intracellular pressure mediates the interaction between myofil
ament force, cell shortening, and the mechanical properties of the sar
colemma. Shortening of myofibrils, which are embedded in the fluid-fil
led myocytes, deforms the myocyte, thereby altering its transmural flu
id pressure. This increase in transmural pressure counteracts fiber sh
ortening, hence constituting an. internal load to shortening. The shor
tening of the myocyte is accompanied by thickening, due to the incompr
essible nature of its contents. Consequently, the overall contractile
performance of the cell is integrally linked to the generation of intr
acellular pressure. The model manifests a positive transmural pressure
during shortening, but not without shortening. The pressure in the my
ocyte, therefore, is not a direct function of the force generated, but
rather of shortening. Intracellular pressure was measured through a f
luid-filled glass micropipette (5mu ID) employing a servo-nulling pres
sure transducer in a standard micropuncture technique. Measured intrac
ellular pressure in a contracting isolated skeletal myocyte of the gia
nt barnacle is observed to be dynamically related to shortening, but n
ot to tension without shortening. The relation between the force of co
ntraction, cell shortening, and intracellular pressure was assessed du
ring both isotonic and isometric contractions. The results support the
prediction that isometric, or nondeforming, contractions will not dev
elop intracellular pressure and identify a reason for relengthening of
the myocytes during relaxation.