Nature of motions between sarcomeres in asynchronously contracting cardiac muscle cells

We observed the asynchronized motions that occur between the sarcomeres during spontaneous contractions to study the mechanical nature of the intact cardiac muscle cell (guinea pig, rat). The cell's striated image is detected by a photodiode array, and sarcomere length is measured very precisely 526/s in two separate, selected fixed regions of the image from the localized frequency of the array's video signal (Krueger and Denton, 1992, Biophys. J., 61:129-144, second of two companion manuscripts). An extension of this approach is described here in which the spatial variation of sarcomere length is visualized by scanned sampling, i.e., displacing the first window along the length of the cell, and nonuniform strain is deduced from the histograms of sarcomere length. The nature of asynchronous motion that was obtained from both fixed sampling of the sarcomere's dynamics and by scanned sampling of sarcomere length was consistent. In spontaneously active cells, sarcomeres lengthen approximately 0.1 micron beyond their rest length before the arrival of the propagated wave of contraction. Such prelengthening extends in a nonuniform fashion for approximately 10 to 15 microns in the unattached cell. Shortening and lengthening motions, being in proportion for both large and small displacements, are well coupled. Lifting the cell from the substrate showed that the force that sustains prelengthening arises within the cell. Differences in the sarcomere's dynamics in synchronous and asynchronous contractions corroborate that asynchrony imposes an additional internal restoring force. The extra force estimated to account for prelengthening (0.5-0.7 mN/mm2) has little effect on the velocity of shortening, and so the true intracellular restoring force must be correspondingly larger. The intracellular restoring force may contribute significantly to the rapid 'diastolic' recoil of the heart muscle at short sarcomere lengths.