Roll rotation cues influence roll tilt perception assayed using a somatosensory technique

Abstract

We investigated how the nervous system processes ambiguous cues from the otolith organs by measuring roll tilt perception elicited by two motion paradigms. In one paradigm (tilt), eight subjects were sinusoidally tilted in roll with the axis of rotation near ear level. Stimulus frequencies ranged from 0.005 to 0.7 Hz, and the peak amplitude of tilt was 20 degrees . During this paradigm, subjects experienced a sinusoidal variation of interaural gravitational force with a peak of 0.34 g. The second motion paradigm (translation) was designed to yield the same sinusoidal variation in interaural force but did not include a roll canal cue. This was achieved by sinusoidally translating the subjects along their interaural axis. For the 0.7-Hz translation trial, the subjects were simply translated from side to side. A centrifuge was used for the 0.005- to 0.5-Hz translation trials; the subjects were rotated in yaw at 250 degrees /s for 5 min before initiating sinusoidal translations yielding an interaural otolith stimulus composed of both centrifugal and radial acceleration. Using a somatosensory task to measure roll tilt perception, we found substantial differences in tilt perception during the two motion paradigms. Because the primary difference between the two motion paradigms was the presence of roll canal cues during roll tilt trials, these perceptual differences suggest that canal cues influence tilt perception. Specifically, rotational cues provided by the semicircular canals help the CNS resolve ambiguous otolith cues during head tilt, yielding more accurate tilt perception.

FIG. 1

Examples of discrete somatosensory bar tilt settings provided by a single subject during the 0.005-Hz tilt paradigm (A), 0.005-Hz translation paradigm (B), 0.05-Hz tilt paradigm (C), and 0.05-Hz translation paradigm (D). Large light gray vertical lines show the subject offsetting the bar to the left and right, as instructed, before providing a discrete tilt indication (black dots). Discrete tilt indications are only shown for the steady-state part of the motion stimulus. Cycle-by-cycle fits are shown in gray. Motion stimuli (tilt angle for the tilt paradigm and interaural acceleration for the translation paradigm) are shown on the bottom row of each graph. Note that for these 2 stimulus frequencies, the tilt responses provided during the tilt paradigm (A and C) were nearly equal in amplitude to those provided during the translation paradigm (B and D).

FIG. 2

Examples of continuous somatosensory bar tilt settings provided by a single subject during 0.05-Hz tilt paradigm (A), 0.05- Hz translation paradigm (B), 0.7-Hz tilt paradigm (C), and 0.7-Hz translation paradigm (D). Cycle-by-cycle fits of tilt responses at steady-state are shown in gray. Motion stimulus is shown on the bottom row of each graph. Note that there is almost no indication of perceived tilt during the 0.7-Hz translation stimulus (D), whereas a substantial indication of perceived tilt is present during the 0.7-Hz tilt stimulus (C).

FIG. 3

Average somatosensory tilt responses (amplitude and phase) as a function of frequency during the translation (○, n = 6 subjects) and tilt (×, n = 8 subjects) paradigms. Error bars represent SE. A: mean tilt amplitude was calculated by computing the vector average across subjects. B: mean phase was calculated by normalizing the data from each subject to have gain of 1 before performing a vector average, from which phase was calculated φ = tan⁻¹(A_s/A_c). A_s and A_c are the mean sine and cosine components, respectively. The normalization process was performed so that the phase of responses from subjects with smaller tilt indications (e.g., 10–15°) would have the same influence on the average phase data as the phase from subjects with larger tilt indications (e.g., 30–40°). C: because previous studies have shown that continuous tilt measures underestimate tilt (Merfeld et al. 2001), we rescaled the continuous data (—) to match the amplitude of the discrete task data (···) at overlapping frequencies (0.05 and 0.1 Hz). To accomplish this, we calculated the average ratio of the mean discrete tilt indications divided by the mean continuous tilt indications at overlapping frequencies and used this ratio of 1.09 and 1.29 for each translation and tilt trial, respectively, as a scaling factor to multiply all continuous tilt settings. A first order low-pass filter (blue) was fit to the amplitude of the tilt data during the translation paradigm. A cut-off frequency of 0.07 Hz provided the best fit to the amplitude data. Internal model predictions of the phase (B) and amplitude (C) of the tilt response during tilt (green) and translation (red) paradigms are also shown. To provide a direct comparison between the tilt data and model predictions, the modeled nondimensional tilt gain (the ratio of peak estimated interaural gravitational force divided by the peak interaural gravito-inertial force) was scaled to best match the data with the scaling factor of 30.7 and 24.0° for translation and tilt paradigms, respectively.