Neuronal thresholds and choice-related activity of otolith afferent fibers during heading perception

Abstract

How activity of sensory neurons leads to perceptual decisions remains a challenge to understand. Correlations between choices and single neuron firing rates have been found early in vestibular processing, in the brainstem and cerebellum. To investigate the origins of choice-related activity, we have recorded from otolith afferent fibers while animals performed a fine heading discrimination task. We find that afferent fibers have similar discrimination thresholds as central cells, and the most sensitive fibers have thresholds that are only twofold or threefold greater than perceptual thresholds. Unlike brainstem and cerebellar nuclei neurons, spike counts from afferent fibers do not exhibit trial-by-trial correlations with perceptual decisions. This finding may reflect the fact that otolith afferent responses are poorly suited for driving heading perception because they fail to discriminate self-motion from changes in orientation relative to gravity. Alternatively, if choice probabilities reflect top-down inference signals, they are not relayed to the vestibular periphery.

Keywords: choice probability; heading discrimination; neuronal threshold; otolith afferent; psychophysical threshold.

Fig. 1.

Behavioral task, neural analysis, and summary of neuronal and psychophysical performance. (A) Layout of the heading discrimination task and illustration of the Gaussian stimulus velocity (black) and biphasic linear acceleration (gray) profiles. (B) Peri-stimulus time histograms (PSTHs) of responses corresponding to seven distinct headings (top to bottom: −25°, −5°, −1°, 0°, −1°, −5°, and −25°) for an example neuron. Responses in a 400-ms window centered on peak acceleration (gray shading) were monotonically tuned (Fig. S1D). (C) Neurometric function (● and solid curve) for the same neuron showing the proportion of “rightward” decisions for an ideal observer as a function of heading. The corresponding psychometric function fit is also shown (□). (D) Individual (gray curves) and mean (black curve) psychometric functions are shown as cumulative Gaussian fits (n = 54 sessions). (E) Individual (gray curves) and mean (black curve) neurometric functions (cumulative Gaussian fits to ROC data from n = 62 otolith afferent fibers). With the exception of eight fibers, all primary otolith afferent data were recorded while trained animals performed the discrimination task.

Fig. 2.

Comparison of psychophysical and neuronal thresholds for otolith afferents. Symbol shapes denote different animals: monkey C (n = 30, ○), monkey Y (n = 20, □), monkey O (n = 2, ▽), and monkey H (n = 2, △). The diagonal histogram shows the distribution of neuronal-to-psychophysical (N/P) threshold ratios. In this comparison, psychophysical thresholds have been divided by the square root of 2 to be directly comparable to neuronal thresholds computed using the neuron/antineuron method. The arrowhead illustrates the mean N/P ratio. Dotted lines illustrate twofold and threefold ratios.

Fig. 3.

Dependence of neuronal sensitivity on discharge regularity. Scatter plots show the neuronal threshold (A), tuning curve slope (B), and median response variance (C) plotted against CV* (n = 62 afferents). Median response variance is computed across all headings tested in the discrimination task. Solid lines illustrate type II linear regression fits (shown only for significant correlations).

Fig. 4.

Comparison between otolith afferents and central VN/CN cells. Scatter plots of neuronal threshold vs. tuning curve slope (A) and median response variance (B) for otolith afferents (red symbols, n = 64) and VN/CN neurons (black symbols, n = 97; data from ref. 13). Solid lines show type II linear regression fits (plotted only for significant correlations). Marginal distributions of neuronal threshold (C), tuning curve slope (D), and median response variance (E) are shown. Arrowheads illustrate geometric means. spk, spike.

Fig. 5.

Comparison of CPs between otolith afferents and VN/CN neurons. (A) Grand CPs are plotted against neuronal thresholds for otolith afferents (red, n = 54) and VN/CN neurons (black, n = 97) (VN/CN data are from ref. 13). Solid black line indicates a type II regression fit to VN/CN data (the correlation was not significant for otolith afferents). Filled symbols represent CP values significantly different from 0.5 (permutation test: P < 0.05,). Marginal histograms show distributions of CPs for VN/CN neurons (black) and otolith afferents (red). Filled and open bars indicate neurons with significant and nonsignificant CPs, respectively. Arrowheads illustrate mean values. (B) Scatter plot of CPs against response variance. Filled and open symbols indicate neurons with significant and nonsignificant CPs, respectively. Horizontal dashed lines indicate the chance level (0.5) for CP.

Fig. 6.

Time dependence of neuronal thresholds (A) and CPs (B). Gray lines represent individual cells (threshold: n = 62, CP: n = 54). Open symbols (○) and the thick black line illustrate population means. Each point represents data computed in a 400-ms analysis window that is shifted by steps of 50 ms. The vertical dashed lines represent the time of peak stimulus acceleration (time point used for all other analyses). Filled symbols (●) indicate that the mean CP is significantly different from 0.5 (t test: P < 0.05).