Direction discrimination thresholds of vestibular and cerebellar nuclei neurons

Abstract

To understand the roles of the vestibular system in perceptual detection and discrimination of self-motion, it is critical to account for response variability in computing the sensitivity of vestibular neurons. Here we study responses of neurons with no eye movement sensitivity in the vestibular (VN) and rostral fastigial nuclei (FN) using high-frequency (2 Hz) oscillatory translational motion stimuli. The axis of translation (i.e., heading) varied slowly (1 degrees /s) in the horizontal plane as the animal was translated back and forth. Signal detection theory was used to compute the threshold sensitivity of VN/FN neurons for discriminating small variations in heading around all possible directions of translation. Across the population, minimum heading discrimination thresholds averaged 16.6 degrees +/- 1 degrees SE for FN neurons and 15.3 degrees +/- 2.2 degrees SE for VN neurons, severalfold larger than perceptual thresholds for heading discrimination. In line with previous studies and theoretical predictions, maximum discriminability was observed for directions where firing rate changed steeply as a function of heading, which occurs at headings approximately perpendicular to the maximum response direction. Forward/backward heading thresholds tended to be lower than lateral motion thresholds, and the ratio of lateral over forward heading thresholds averaged 2.2 +/- 6.1 (geometric mean +/- SD) for FN neurons and 1.1 +/- 4.4 for VN neurons. Our findings suggest that substantial pooling and/or selective decoding of vestibular signals from the vestibular and deep cerebellar nuclei may be important components of further processing. Such a characterization of neural sensitivity is critical for understanding how early stages of vestibular processing limit behavioral performance.

Figure 1.

Experimental protocol and neuronal responses. A, Schematic of the continuous linear acceleration stimulus around the head horizontal plane. B, IFR of a FN cell during combined sinusoidal translation (2 Hz; ±0.3G) and constant velocity rotation (1°/s). C, Enlarged time scale near the minimum and maximum response modulation, respectively.

Figure 2.

Quantification of response tuning, including response amplitude and phase as a function of heading direction. A, Response amplitude is plotted as a function of heading direction for each cycle of translation (filled symbols). The best fit of a spatiotemporal model is shown as the gray curve. B, Response phase values (obtained from sinusoidal fits to each cycle response) are plotted as a function of heading direction (filled symbols), along with the model fit (gray curve). The tuning ratio for this cell was 0.12. Data shown are superimposed from five runs (yaw revolutions) for the same FN cell as illustrated in Figure 1.

Figure 3.

Firing rate as a function of heading direction for an example FN neuron. A, Data from the two half-cycles are shown by black and gray symbols, respectively (data pooled across 5 runs). B, Firing rate from the second half of each response cycle is shifted by 180° to overlap with data from the first half-cycle. C, Computed neuronal threshold plotted against reference heading direction. Data shown are from the same cell as in Figures 1 and 2. A vertical dashed line illustrates that the minimum discrimination threshold is observed away from the preferred direction, where tuning changes rapidly.

Figure 4.

Quantification of neuronal threshold for a single reference direction. A, Tuning curve, plotting firing rate (mean ± SE) as a function of heading direction in the range of ±20° around the reference heading. Positive angles indicate rightward directions; negative angles indicate leftward directions (relative to the reference). B, Firing rate distributions for four pairs of comparison headings, ±20° ±12°, ±2°, and ±1° relative to the reference. C, Example neurometric function showing proportion rightward decisions of an ideal observer as a function of heading direction. Each data point corresponds to an ROC value computed from a pair of firing rate distributions like those shown in B. Solid line shows a cumulative Gaussian fit to the neurometric function.

Figure 5.

Summary of neuronal thresholds. A, Distribution of minimum neuronal thresholds for 41 FN and 20 VN cells. B, Distribution of reference heading directions for which minimum neuronal thresholds were obtained. C, Distribution of the difference between minimum threshold direction and the maximum response direction. Open bars, FN cells; striped bars, VN cells.

Figure 6.

Relationship between minimum discrimination threshold and tuning ratio. A, Distribution of tuning ratio in VN (n = 20, striped bars) and FN (n = 41, open bars). B, Scatter plot of tuning ratio versus minimum discrimination threshold. C, Scatter plot of tuning ratio versus the absolute difference between minimum threshold direction and maximum response direction. Filled symbols, FN cells (n = 41); open symbols, VN cells (n = 20).

Figure 7.

A, Comparison of neuronal thresholds for forward versus lateral reference headings. B, Analogous comparison for backward versus lateral reference headings. The histograms on top and right illustrate the corresponding distributions (capped at a threshold value of 900). Arrows illustrate geometric means (Table 1). Filled symbols, FN cells (n = 41); open symbols, VN cells (n = 20). Note that each cell is plotted twice, showing data for both rightward and leftward motion.

Figure 8.

A, Dependence of neuronal thresholds on the length of the time window (centered on the middle of each response half-cycle) in which firing rates were computed. B, Dependence of thresholds on the range of comparison headings used to construct the neurometric function using ROC analysis. This dependence is illustrated for the reference heading that produced the minimum threshold for each neuron using a time interval of 250 ms and a 40° heading range. Filled symbols, FN cells (n = 41); open symbols, VN cells (n = 20). Data illustrate mean ± SE.