The ciliary cycle during hyperpolarization-induced activity: an analysis of axonemal functional parameters

Motor responses of the frontal cirri of the ciliate Stylonychia were recorded at the axial view of the ciliary base with high-speed cinematography. Voltage-clamp applying sustained hyperpolarizing voltage steps was used to explore the properties of the ciliary cycle modulated by the membrane potential. Upon hyperpolarization between -1 and -13 mV, a previously inactive frontal cirrus reoriented from a neutral posture and started beating so that the axis of the beating cone of a proximal cirral segment assumed an orientation near 100 degrees (proceeding counterclockwise from posterior = 0 degrees) and inclination near 60 degrees (0 degrees = perpendicular to the cell surface). The major beating amplitude was limited to about 150 degrees. Increasing hyperpolarization increased the spatial polarity of the cycle (ratio of major over minor amplitude, from 2 to 2.4). Rates of the power stroke increased with hyperpolarizations up to -4 mV but were consistently smaller than those of the return stroke during the ciliary cycle (ratio: 0.4 to 0.6; = temporal polarity). Comparison of different hypothetical beat forms (0-shape, D-shape, and egg-shape) showed that the orientation-time data are the major determinants of the angular velocity and rate of reorientation of the cilium during the cycle. Geometric transformation of these data led to descriptions of the cycle of a proximal ciliary segment in terms of active sliding velocities and rates of unidirectional sliding translocation between identified doublets. Three voltage-sensitive functional parameters of the cilium--the inclination (which is noncyclic) and the rates of active sliding and sliding translocation (both of which are cyclic in nature)--are discussed as generating the spatial and temporal properties of the ciliary beat.