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)

Response properties of vertical (VC) and horizontal (HC) canal/otolith-convergent vestibular nuclei neurons were studied in decerebrate rats during stimulation with sinusoidal linear accelerations (0.2-1.4 Hz) along different directions in the head horizontal plane. A novel characteristic of the majority of tested neurons was the nonzero response often elicited during stimulation along the "null" direction (i.e., the direction perpendicular to the maximum sensitivity vector, Smax). The tuning ratio (Smin gain/Smax gain), a measure of the two-dimensional spatial sensitivity, depended on stimulus frequency. For most vestibular nuclei neurons, the tuning ratio was small at the lowest stimulus frequencies and progressively increased with frequency. Specifically, HC neurons were characterized by a flat Smax gain and an approximately 10-fold increase of Smin gain per frequency decade. Thus, these neurons encode linear acceleration when stimulated along their maximum sensitivity direction, and the rate of change of linear acceleration (jerk) when stimulated along their minimum sensitivity direction. While the Smax vectors were distributed throughout the horizontal plane, the Smin vectors were concentrated mainly ipsilaterally with respect to head acceleration and clustered around the naso-occipital head axis. The properties of VC neurons were distinctly different from those of HC cells. The majority of VC cells showed decreasing Smax gains and small, relatively flat, Smin gains as a function of frequency. The Smax vectors were distributed ipsilaterally relative to the induced (apparent) head tilt. In type I anterior or posterior VC neurons, Smax vectors were clustered around the projection of the respective ipsilateral canal plane onto the horizontal head plane. These distinct spatial and temporal properties of HC and VC neurons during linear acceleration are compatible with the spatiotemporal organization of the horizontal and the vertical/torsional ocular responses, respectively, elicited in the rat during linear translation in the horizontal head plane. In addition, the data suggest a spatially and temporally specific and selective otolith/canal convergence. We propose that the central otolith system is organized in canal coordinates such that there is a close alignment between the plane of angular acceleration (canal) sensitivity and the plane of linear acceleration (otolith) sensitivity in otolith/canal-convergent vestibular nuclei neurons.

Quantitative study of the static and dynamic response properties of some otolith-sensitive neurons has been difficult in the past partly because their responses to different linear acceleration vectors exhibited no "null" plane and a dependence of phase on stimulus orientation. The theoretical formulation of the response ellipse provides a quantitative way to estimate the spatio-temporal properties of such neurons. Its semi-major axis gives the direction of the polarization vector (i.e., direction of maximal sensitivity) and it estimates the neuronal response for stimulation along that direction. In addition, the semi-minor axis of the ellipse provides an estimate of the neuron's maximal sensitivity in the "null" plane. In this paper, extracellular recordings from otolith-sensitive vestibular nuclei neurons in decerebrate rats were used to demonstrate the practical application of the method. The experimentally observed gain and phase dependence on the orientation angle of the acceleration vector in a head-horizontal plane was described and satisfactorily fit by the response ellipse model. In addition, the model satisfactorily fits neuronal responses in three-dimensions and unequivocally demonstrates that the response ellipse formulation is the general approach to describe quantitatively the spatial properties of vestibular neurons.

The vertical eye movements induced by a brief period of free fall were recorded from three monkeys (Macaca mulatta) using the electromagnetic search coil technique. Free fall was initiated in total darkness immediately following binocular fixation of one of six target lights located at viewing distances ranging from 20 to 107 cm. Responses consisted of an initial transient downward eye movement (anticompensatory direction) with a latency of a few milliseconds at most followed by a sustained upward (compensatory) eye movement. The early transient was independent of viewing distance and attributed to an artifact, whereas the later component was a linear function of the inverse of the prior viewing distance and attributed to the translational vestibulo-ocular reflex (TVOR). Response latencies for the four nearer viewing distances were determined from the individual eye velocity traces using a computerized algorithm: after removing the initial transient by subtracting the mean response obtained with the most distant viewing, a regression line was fitted to the initial rising phase of the residual response and then extrapolated back to the baseline to determine the onset. When so determined, median latencies for the nearest viewing ranged from 16.4 to 18.5 ms, values appreciably shorter than any in the literature.

A change in otolith activity modifies the dynamic responses of both the and the vertical4 vestibuloocular reflexes (VOR). In response to rotations in vertical planes, dynamic otolith activity is necessary for compensatory eye movements in the rabbit5 and the cat.6 Therefore, significant convergence of otolith and canal information in the VOR pathway must occur.The activity of single vestibular nuclei neurons in the decerebrate rat were recorded extracellularly during sinusoidal linear translation in the horizontal head plane. Details of the experimental procedure are presented elsewhere.' Neurons from the four groups-(1) type I and (2) type I1 horizontal canal related, (3) vertical canal related, and (4) purely otolith-were systematically tested for their responses to translation at various horizontal head orientations. These responses were then used to describe a response ellipse*JO in which the semimajor axis (S1) defined the cell's direction of maximum sensitivity and its associated gain and phase and the semiminor axis (S2) defined the minimum sensitivity of the cell in the horizontal head plane. When the magnitude of the S2 vector was zero, the response was referred to as narrowly tuned and was characterized by gain values that were proportional to the cosine of the angle between S1 and the stimulus direction and phase values that were constant with respect to stimulus direction. Whereas, a response with a nonzero magnitude of the S2 vector was referred to as broadly tuned and was characterized by a response phase that varied as a function of stimulus angle. The accuracy with which the response ellipse quantitatively described the data was assessed by comparing the direction, gain, and phase values of the maximum response determined empirically with those calculated from the fitted curves (compare the data points with the curve in FIGURE 1). The calculated and experimentally measured responses had high linear regression coefficients (r = 0.93014.9976) and slopes close to unity.Broadly tuned neurons were observed in each of the four groups of neurons studied. The ratio of S2 and S, response magnitudes (tuning ratio) was calculated for all neurons.