Responses of vestibular-only translation sensitive (VOTS) neurons in vestibular nuclei of two squirrel monkeys were studied at multiple frequencies to three-dimensional translations and rotations. A novel frequency-dependent spatiotemporal analysis examined in each neuron whether complex models, with unrestricted response dynamics in three-dimensional (3D) space, provided significantly better fits than restricted models following simple, cosine rule. Subsequently, the statistically selected optimal model was used to predict the maximum translation direction, expressed as a unitary vector, Vtmax, and its associated sensitivity and phase across frequencies. Simple models were sufficient to quantify the 3D translational responses of 66% of neurons. Most VOTS neurons, complex or simple, exhibited flat-gain or low-pass response dynamics. The Vtmax of simple neurons was fixed, whereas that of complex neurons changed with frequency. The spatial distribution of Vt max in simple neurons, which fell within 30° of either the horizontal plane or/and the sagittal plane, was closely aligned with Vt max of vestibular afferents. In contrast, the frequency-dependent Vtmax of most complex neurons migrated from the dorsoventral axis at higher frequency toward the horizontal plane, especially the interaural axis, at lower frequency. When the maximum rotation direction was estimated from responses of the same VOTS neurons to 1.2 Hz yaw, pitch, and roll rotations, complex neurons were more likely to respond to rotations activating vertical canals. Responses to 0.15-0.3 Hz linear accelerations produced by inertial or gravitational forces were indistinguishable in most complex neurons but significantly different in most simple neurons. These observations suggest that simple and complex VOTS neurons constitute distinctive vestibular pathways where complex neurons, exhibiting a novel spatiotemporal filtering mechanism in processing otolith-related signals, are well suited to drive tilt-related responses, whereas simple neurons probably mediate pure translation related responses.
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