Head tilt–translation combinations distinguished at the level of neurons

Angular and linear accelerations of the head occur throughout everyday life, whether from external forces such as in a vehicle or from volitional head movements. The relative timing of the angular and linear components of motion differs depending on the movement. The inner ear detects the angular and linear components with its semicircular canals and otolith organs, respectively, and secondary neurons in the vestibular nuclei receive input from these vestibular organs. Many secondary neurons receive both angular and linear input. Linear information alone does not distinguish between translational linear acceleration and angular tilt, with its gravity-induced change in the linear acceleration vector. Instead, motions are thought to be distinguished by use of both angular and linear information. However, for combined motions, composed of angular tilt and linear translation, the infinite range of possible relative timing of the angular and linear components gives an infinite set of motions among which to distinguish the various types of movement. The present research focuses on motions consisting of angular tilt and horizontal translation, both sinusoidal, where the relative timing, i.e. phase, of the tilt and translation can take any value in the range −180° to 180°. The results show how hypothetical neurons receiving convergent input can distinguish tilt from translation, and that each of these neurons has a preferred combined motion, to which the neuron responds maximally. Also shown are the values of angular and linear response amplitudes and phases that can cause a neuron to be tilt-only or translation-only. Such neurons turn out to be sufficient for distinguishing between combined motions, with all of the possible relative angular–linear phases. Combinations of other neurons, as well, are shown to distinguish motions. Relative response phases and in-phase firing-rate modulation are the key to identifying specific motions from within this infinite set of combined motions.