Neural Processing of Gravito-Inertial Cues in Humans. IV. Influence of Visual Rotational Cues During Roll Optokinetic Stimuli

Abstract

Sensory systems often provide ambiguous information. For example, otolith organs measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. However, according to Einstein's equivalence principle, a change in gravitational force due to tilt is indistinguishable from a change in inertial force due to translation. Therefore the central nervous system (CNS) must use other sensory cues to distinguish tilt from translation. For example, the CNS might use dynamic visual cues indicating rotation to help determine the orientation of gravity (tilt). This, in turn, might influence the neural processes that estimate linear acceleration, since the CNS might estimate gravity and linear acceleration such that the difference between these estimates matches the measured GIF. Depending on specific sensory information inflow, inaccurate estimates of gravity and linear acceleration can occur. Specifically, we predict that illusory tilt caused by roll optokinetic cues should lead to a horizontal vestibuloocular reflex compensatory for an interaural estimate of linear acceleration, even in the absence of actual linear acceleration. To investigate these predictions, we measured eye movements binocularly using infrared video methods in 17 subjects during and after optokinetic stimulation about the subject's nasooccipital (roll) axis (60°/s, clockwise or counterclockwise). The optokinetic stimulation was applied for 60 s followed by 30 s in darkness. We simultaneously measured subjective roll tilt using a somatosensory bar. Each subject was tested in three different orientations: upright, pitched forward 10°, and pitched backward 10°. Five subjects reported significant subjective roll tilt (>10°) in directions consistent with the direction of the optokinetic stimulation. In addition to torsional optokinetic nystagmus and afternystagmus, we measured a horizontal nystagmus to the right during and following clockwise (CW) stimulation and to the left during and following counterclockwise (CCW) stimulation. These measurements match predictions that subjective tilt in the absence of real tilt should induce a nonzero estimate of interaural linear acceleration and, therefore, a horizontal eye response. Furthermore, as predicted, the horizontal response in the dark was larger for Tilters ( n = 5) than for Non-Tilters ( n= 12).

Roll Tilt Psychophysics in Rhesus Monkeys During Vestibular and Visual Stimulation

“…Percepts of roll tilt during sinusoidal variable-radius centrifugation, in particular, appear to support contributions from frequency-segregation. Similar to prior reports in human subjects (Glasauer 1995;Merfeld et al 2005a;Zupan and Merfeld 2005), illusions of roll tilt were greatest at the lowest frequency and became smaller as the frequency of translation increased. While these findings suggest that high and low-pass filters may disambiguate the shifts in GIF produced by head translation Paige and Tomko 1991), the frequency independence of the phase is not consistent with a simple filtering mechanism (Glausauer 1995).…”

“…While we did not measure torsional eye position, prior studies have shown only small torsional deviations of the eyes during roll optokinetic stimulation (Ibbotson et al 2005;Zupan and Merfeld 2003). Therefore it is unlikely that the shift in SVV responses resulted solely from changes in torsional eye position.…”

“…1) percepts of head tilt cannot be deduced from eye movement responses (Zupan and Merfeld 2005). Torsional eye movements, for example, include an angular vestibuloocular reflex (VOR) component that is independent of gravity as well as utricular contributions that do not reflect roll tilt of the GIF (Angelaki 1998;Merfeld et al 1996;Paige and Tomko 1991).…”

Evaluation of Driver Distraction with Changes in Gaze Direction Based on a Vestibulo-Ocular Reflex Model

“…According to the results obtained by Zupan and Merfeld [16] and by Angelaki and co-workers [17] [which measure linear accelerations of the head (α) and gravity (g)] sense the proprioceptive information from the environment; this is the first step in calculating sensory information from the measurements (α oto , α scc ). In the next step, the measurements are compared with the sensory information predicted by the internal model.…”

Discrepancy between the Directions of Body Sway and Gaze during Simultaneous Optokinetic and Posterior Neck Muscle Vibration Stimulation

“…The former can be attributed to an illusory traveling perception driven by retinal slip 2) 3) , whereas the presence of a cross-coupling effect on the postural response may indicate that the latter is driven by the velocity storage integrator (VSI) 1) . On the other hand, Ivanenko et al reported that neck vibration induces body sway in the direction of gaze, which they attributed to rotation of the viewer-centered reference frame 4) .…”