Canal–Otolith Interactions and Detection Thresholds of Linear and Angular Components During Curved-Path Self-Motion

Abstract

MacNeilage PR, Turner AH, Angelaki DE. Canal-otolith interactions and detection thresholds of linear and angular components during curved-path self-motion. J Neurophysiol 104: 765-773, 2010. First published June 16, 2010 doi:10.1152/jn.01067.2009. Gravitational signals arising from the otolith organs and vertical plane rotational signals arising from the semicircular canals interact extensively for accurate estimation of tilt and inertial acceleration. Here we used a classical signal detection paradigm to examine perceptual interactions between otolith and horizontal semicircular canal signals during simultaneous rotation and translation on a curved path. In a rotation detection experiment, blindfolded subjects were asked to detect the presence of angular motion in blocks where half of the trials were pure nasooccipital translation and half were simultaneous translation and yaw rotation (curved-path motion). In separate, translation detection experiments, subjects were also asked to detect either the presence or the absence of nasooccipital linear motion in blocks, in which half of the trials were pure yaw rotation and half were curved path. Rotation thresholds increased slightly, but not significantly, with concurrent linear velocity magnitude. Yaw rotation detection threshold, averaged across all conditions, was 1.45 Ϯ 0.81°/s (3.49 Ϯ 1.95°/s 2 ). Translation thresholds, on the other hand, increased significantly with increasing magnitude of concurrent angular velocity. Absolute nasooccipital translation detection threshold, averaged across all conditions, was 2.93 Ϯ 2.10 cm/s (7.07 Ϯ 5.05 cm/s 2 ). These findings suggest that conscious perception might not have independent access to separate estimates of linear and angular movement parameters during curved-path motion. Estimates of linear (and perhaps angular) components might instead rely on integrated information from canals and otoliths. Such interaction may underlie previously reported perceptual errors during curved-path motion and may originate from mechanisms that are specialized for tilt-translation processing during vertical plane rotation.

Strong Correlations between Sensitivity and Variability Give Rise to Constant Discrimination Thresholds across the Otolith Afferent Population

“…threshold values equal to those reported by MacNeilage et al (2010b) and Valko et al (2012), respectively. In contrast, when the firing rate was estimated using the inverse ISI, the population sizes were significantly larger (ϳ70 and ϳ1100, respectively).…”

“…Based on previous studies (Sadeghi et al, 2007;Massot et al, 2011), we hypothesized that threshold values should strongly depend on both sensitivity and resting discharge regularity. To test this, we determined the detection threshold of each individual afferent by plotting its time-dependent firing rate as a function of linear acceleration (Fig.…”

“…This is expected (Seung and Sompolinsky, 1993) given that there is no correlation between the variabilities of different otolith afferents as discussed below. Using this fit, we extrapolated the population size for which the neural discrimination threshold value is equal to perceptual values reported by MacNeilage et al (2010b) and Valko et al (2012). We only compared our neural threshold values to perceptual threshold values from these studies because they used experimental paradigms that were most similar to our own as discussed below.…”

“…At the earliest stages of vestibular processing, otolith afferents detect linear acceleration. Studies performed in other systems show that central pathways must integrate information transmitted by peripheral sensory neuron populations to explain perceptual thresholds as peripheral sensory neurons display much higher values (visual: Pelli, 1985;Amano et al, 2006; Shadlen et al, 1996; auditory: Pfingst and Xu, 2004;Bizley et al, 2010; cross modal: McDonald et al, 2000; Shams et al, 2000 Shams et al, , 2002 vestibular (rotation): Sadeghi et al, 2007;Massot et al, 2011). Surprisingly, however, Yu et al (2012) recently extrapolated threshold values for single macaque otolith afferents that were comparable with perceptual ones, which suggests that the vestibular system uses a unique strategy for coding linear acceleration.…”

Clinical Testing of Otolith Function: Perceptual Thresholds and Myogenic Potentials

“…The block began with the largest displacement (15 cm). While we did not measure the acceleration at the head for each subject on each trial, we have previously used an accelerometer mounted on the platform to verify that the platform reproduces the desired trajectories very accurately (MacNeilage et al 2010b).…”