Roll-Dependent Modulation of the Subjective Visual Vertical: Contributions of Head- and Trunk-Based Signals

Abstract

Tarnutzer AA, Bockisch CJ, Straumann D. Roll-dependent modulation of the subjective visual vertical: contributions of head-and trunk-based signals. J Neurophysiol 103: 934 -941, 2010. First published December 16, 2009 doi:10.1152/jn.00407.2009. Precision and accuracy of the subjective visual vertical (SVV) modulate in the roll plane. At large roll angles, systematic SVV errors are biased toward the subject's body-longitudinal axis and SVV precision is decreased. To explain this, SVV models typically implement a bias signal, or a prior, in a head-fixed reference frame and assume the sensory input to be optimally tuned along the head-longitudinal axis. We tested the pattern of SVV adjustments both in terms of accuracy and precision in experiments in which the head and the trunk reference frames were not aligned. Twelve subjects were placed on a turntable with the head rolled about 28°counterclockwise relative to the trunk by lateral tilt of the neck to dissociate the orientation of head-and trunk-fixed sensors relative to gravity. Subjects were brought to various positions (roll of head-or trunk-longitudinal axis relative to gravity: 0°, Ϯ75°) and aligned an arrow with perceived vertical. Both accuracy and precision of the SVV were significantly (P Ͻ 0.05) better when the headlongitudinal axis was aligned with gravity. Comparing absolute SVV errors for clockwise and counterclockwise roll tilts, statistical analysis yielded no significant differences (P Ͼ 0.05) when referenced relative to head upright, but differed significantly (P Ͻ 0.001) when referenced relative to trunk upright. These findings indicate that the bias signal, which drives the SVV toward the subject's body-longitudinal axis, operates in a head-fixed reference frame. Further analysis of SVV precision supports the hypothesis that head-based graviceptive signals provide the predominant input for internal estimates of visual vertical.

Multisensory Processing in Spatial Orientation: An Inverse Probabilistic Approach

“…Previously, we have shown that to account for the typical nonlinear increase of the systematic SVV errors with tilt, the variability of the headtilt signal in the model must increase with tilt angle (De Vrijer et al, 2008). In line with this conclusion, decreasing effectiveness of the otoliths with increasing tilt has been suggested by various other reports (Schöne and Udo de Haes, 1968;Tarnutzer et al, 2009Tarnutzer et al, , 2010 and may reflect the geometry of otolith organs, the nonuniform distribution of otolith afferents in the roll-plane and nonlinear firing rates (Tarnutzer et al, 2010). This feature was incorporated by allowing the noise in the sensory headtilt signal, HS , to increase rectilinearly with tilt angle:…”

“…One reason to assume that otolith noise depends on tilt angle is based on the fact that the utricle contains considerably more hair cells than the saccule (Rosenhall, 1972(Rosenhall, , 1974. Because the utricle is most sensitive to tilts of ϳ0°, whereas the saccule is most sensitive at ϳ90°tilt (Jaeger et al, 2008), this may well cause the proposed increase of otolith noise with tilt angle (Tarnutzer et al, 2010). A tilt-dependent noise level of the otoliths would also help to explain why the perturbing effect of roll-optokinetic stimulation on the SVV (Dichgans et al, 1974;Fernández and Goldberg, 1976) and on the SBT (Young et al, 1975) is more pronounced at larger tilt angles and why the SVV is more strongly influenced by residual canal signals at larger tilt angles, after prolonged roll rotations (Lorincz and Hess, 2008).…”

A Pathway in the Brainstem for Roll-Tilt of the Subjective Visual Vertical: Evidence from a Lesion–Behavior Mapping Study

“…Thus, these structures seem to be directly involved in verticality perception within a multisensory system in which graviceptive pathways play a dominant role. In other words, since previous data showed strong evidence that graviceptive otolith signals subserve vestibular function (Halmagyi et al, 1979;Dieterich and Brandt, 1993;Tarnutzer et al, 2010), these structures are part of a vestibular graviceptive otolith brainstem pathway.…”

“…The roll-tilt of the subjective visual vertical (SVV) is considered to be the perceptual correlate of the OTR. Previous data showed that the perception of tilt of SVV depends not only on otolith information but also on somatosensory and visual signals (MacNeilage et al, 2007;Vingerhoets et al, 2009;Tarnutzer et al, 2010). It is well known that lesions of the eighth nerve as well as lesions of the vestibular nucleus cause an ipsiversive OTR (Halmagyi et al, 1979;Dieterich and Brandt, 1993), whereas lesions of the vestibular pathways in the pontomesencephalic brainstem such as the medial longitudinal fasciculus (MLF), its rostral interstitial nucleus (riMLF), and the interstitial nucleus of Cajal (INC) cause contraversive roll-tilts (Dieterich and Brandt, 1993;Brandt and Dieterich, 1994).…”

Does gravity influence the visual line bisection task?

“…While little is known about the influence of gravity on the LBT, its effect on visuospatial tasks such as the subjective visual vertical (SVV) has been extensively investigated (De Vrijer et al 2008;Kaptein and Van Gisbergen 2004;Tarnutzer et al 2009a;Tarnutzer et al 2010;Van Beuzekom and Van Gisbergen 2000). Awareness of head and trunk position, orientation in space, and perception of gravity are the result of a multimodal integration of sensory input from vestibular (utriculus, sacculus, and semicircular canals), somatosensory, and visual signals using internal models to generate an estimate of direction of gravity (Angelaki et al 2009;Barra et al 2010).…”