A mechanistic description of the generation of whisker movements is essential for understanding the control of whisking and vibrissal active touch. We explore how facial-motoneuron spikes are translated, via an intrinsic muscle, to whisker movements. This is achieved by constructing, simulating, and analyzing a computational, biomechanical model of the motor plant, and by measuring spiking to movement transformations at small and large angles using high-precision whisker tracking in vivo. Our measurements revealed a supralinear summation of whisker protraction angles in response to consecutive motoneuron spikes with moderate interspike intervals (5 ms < Deltat < 30 ms). This behavior is explained by a nonlinear transformation from intracellular changes in Ca(2+) concentration to muscle force. Our model predicts the following spatial constraints: (1) Contraction of a single intrinsic muscle results in movement of its two attached whiskers with different amplitudes; the relative amplitudes depend on the resting angles and on the attachment location of the intrinsic muscle on the anterior whisker. Counterintuitively, for a certain range of resting angles, activation of a single intrinsic muscle can lead to a retraction of one of its two attached whiskers. (2) When a whisker is pulled by its two adjacent muscles with similar forces, the protraction amplitude depends only weakly on the resting angle. (3) Contractions of two adjacent muscles sums up linearly for small amplitudes and supralinearly for larger amplitudes. The model provides a direct translation from motoneuron spikes to whisker movements and can serve as a building block in closed-loop motor-sensory models of active touch.