Egocentric and allocentric alignment tasks are affected by otolith input

Abstract

Gravicentric visual alignments become less precise when the head is roll-tilted relative to gravity, which is most likely due to decreasing otolith sensitivity. To align a luminous line with the perceived gravity vector (gravicentric task) or the perceived body-longitudinal axis (egocentric task), the roll orientation of the line on the retina and the torsional position of the eyes relative to the head must be integrated to obtain the line orientation relative to the head. Whether otolith input contributes to egocentric tasks and whether the modulation of variability is restricted to vision-dependent paradigms is unknown. In nine subjects we compared precision and accuracy of gravicentric and egocentric alignments in various roll positions (upright, 45°, and 75° right-ear down) using a luminous line (visual paradigm) in darkness. Trial-to-trial variability doubled for both egocentric and gravicentric alignments when roll-tilted. Two mechanisms might explain the roll-angle-dependent modulation in egocentric tasks: 1) Modulating variability in estimated ocular torsion, which reflects the roll-dependent precision of otolith signals, affects the precision of estimating the line orientation relative to the head; this hypothesis predicts that variability modulation is restricted to vision-dependent alignments. 2) Estimated body-longitudinal reflects the roll-dependent variability of perceived earth-vertical. Gravicentric cues are thereby integrated regardless of the task's reference frame. To test the two hypotheses the visual paradigm was repeated using a rod instead (haptic paradigm). As with the visual paradigm, precision significantly decreased with increasing head roll for both tasks. These findings propose that the CNS integrates input coded in a gravicentric frame to solve egocentric tasks. In analogy to gravicentric tasks, where trial-to-trial variability is mainly influenced by the properties of the otolith afferents, egocentric tasks may also integrate otolith input. Such a shared mechanism for both paradigms and frames of reference is supported by the significantly correlated trial-to-trial variabilities.

Visually guided adjustments of body posture in the roll plane

“…In fact, we found significantly higher variability for desired 75° RED whole-body roll compared to desired upright position in the earth-fixed paradigm, supporting the "all sensors' integrated hypothesis". This phenomenon was recently also reported for visual line adjustments along the body-longitudinal axis in whole-body roll-tilted positions (Tarnutzer et al 2012). Such a behavior is compatible with the previously observed whole-body roll-angle dependent increase of SVV variability, which most likely reflects head-roll dependent variability of otolith signals (Tarnutzer et al 2009a).…”

“…However, trial-to-trial variability of alignment tasks increases independently from the presence / absence of retinal input when the subject is roll-tilted (Tarnutzer et al 2012), so increased variability in our tasks cannot be explained solely on the basis of variability of torsional eye position. At the same time, the oblique effect diminishes when the head is rolltilted (Luyat et al 2001;McIntyre et al 2001), mostly due to increased discrimination thresholds along the principal axes.…”

“…The hypothesis of the "purely visual strategy" predicts that, for selfadjustments along an earth-fixed visual cue, the trial-to-trial variability remains unaffected by the body-roll position as the signal-to-noise ratio of the retina's ability to determine stimulus position modulates little with the torsional orientation of a visual cue. In a recent study, however, we proposed that for both the SVV and the SHV sensed direction of gravity influences a task, that -in theory -could be done solely by retinal input (Tarnutzer et al 2012). We call this strategy, which includes otolith input independently of the task, the "all sensors' integration strategy".…”

“…However, we previously found that an estimate of head orientation relative to gravity is also integrated when solving visual alignment tasks in egocentric frames of reference (Tarnutzer et al 2012). This would increase the level of variability in the earth-fixed task and makes different levels in task complexity between the body-fixed and the earth-fixed task a less likely explanation for the observed difference in trial-to-trial variability.…”

Does gravity influence the visual line bisection task?

“…Manipulations of the environment, such as obtaining the SVV while roll-tilted under water, have shown that the influence of proprioception on the SVV is minor compared with that of otolith input in healthy human subjects (Graybiel et al 1968;Jarchow and Mast 1999;Wade 1973). For visual as well as haptic line adjustments along an Earth-vertical (gravicentric) axis or a body-longitudinal (egocentric) axis, Tarnutzer and colleagues observed roll angle-dependent modulations of alignment precision in all conditions (Tarnutzer et al 2012). The comparable results in the egocentric and gravicentric (i.e., a special case of an allocentric frame) task suggest that the same mechanism is responsible for the increased trial-to-trial variability in roll-tilted positions.…”