Encoding of head acceleration in vestibular neurons. I. Spatiotemporal response properties to linear acceleration

Abstract

1. Extracellular recordings were made in and around the medial vestibular nuclei in decerebrated rats. Neurons were functionally identified according to their semicircular canal input on the basis of their responses to angular head rotations around the yaw, pitch, and roll head axes. Those cells responding to angular acceleration were classified as either horizontal semicircular canal-related (HC) or vertical semicircular canal-related (VC) neurons. The HC neurons were further characterized as either type I or type II, depending on the direction of rotation producing excitation. Cells that lacked a response to angular head acceleration, but exhibited sensitivity to a change in head position, were classified as purely otolith organ-related (OTO) neurons. All vestibular neurons were then tested for their response to sinusoidal linear translation in the horizontal head plane. 2. Convergence of macular and canal inputs onto central vestibular nuclei neurons occurred in 73% of the type I HC, 79% of the type II HC, and 86% of the VC neurons. Out of the 223 neurons identified as receiving macular input, 94 neurons were further studied, and their spatiotemporal response properties to sinusoidal stimulation with pure linear acceleration were quantified. Data were obtained from 33 type I HC, 22 type II HC, 22 VC, and 17 OTO neurons. 3. For each neuron the angle of the translational stimulus vector was varied by 15, 30, or 45 degrees increments in the horizontal head plane. In all tested neurons, a direction of maximum sensitivity was identified. An interesting difference among neurons was their response to translation along the direction perpendicular to that that produced the maximum response ("null" direction). For the majority of neurons tested, it was possible to evoke a nonzero response during stimulation along the null direction always had response phases that varied as a function of stimulus direction. 4. These spatiotemporal response properties were quantified in two independent ways. First, the data were evaluated on the basis of the traditional one-dimensional principle governed by the "cosine gain rule" and constant response phase at different stimulus orientations. Second, the response gain and phase values that were empirically determined for each orientation of the applied linear stimulus vector were fitted on the basis of a newly developed formalism that treats neuronal responses as exhibiting two-dimensional spatial sensitivity. Thus two response vectors were determined for each neuron on the basis of its response gain and phase at different stimulus directions in the horizontal head plane.(ABSTRACT TRUNCATED AT 400 WORDS)

Maturation of canal‐related brainstem neurons in the detection of horizontal angular acceleration in rats

“…Combining the present data and the findings of Lai et al (2004), the distribution of horizontal canal-and utricle-related vestibular nuclear neurons exhibited considerable overlap, especially in the parvicellular portion of MV and the central part of SpV, where convergence of horizontal canal and utricular afferents is likely to occur Sato et al, 2002;Uchino 2001;Zhang et al, 2002). In fact, many neurons in the MV responded to both canal and otolith inputs (Reisine and Raphan 1992;Bush et al, 1993;Schor et al, 1998;Dickman and Angelaki, 2002). Taken together, our findings indicate that spatial orientations registered in the vestibular nucleus during horizontal translational and rotational head movements are not represented in a topographic pattern.…”

Degradation of Head Direction Cell Activity during Inverted Locomotion

“…Although we know of no evidence that the functioning of the canals would be affected by the orientation of the head relative to gravity, the otolith signal has been shown to be distorted at nonupright orientations (Walsh, 1960;Plotnik et al, 1999), and the stabilization of head and eye position in space is likely a function of vestibular information converging from both of these sources. Indeed, many neurons of the medial vestibular nuclei, the proposed source of vestibular information reaching the HD system, seem to integrate both canal and otolith signals (Bush et al, 1993).…”

Vestibular Signals in Primate Thalamus: Properties and Origins

“…We have used a spatiotemporal analysis to describe each cell's tuning as a set of two orthogonal response vectors (Angelaki, 1991;Angelaki and Dickman, 2000). This analysis represents a generalization of cosine tuning that allows a nonzero minimum response gain and phase that can change as a function of motion direction (Angelaki, 1991;Bush et al, 1993;Angelaki and Dickman, 2000). In the present study, it was used to compute a maximum response gain and phase, as well as the corresponding preferred direction for each cell and each stimulus frequency.…”