Visual Object Localization through Vestibular and Neck Inputs. 1: Localization with Respect to Space and Relative to the Head and Trunk Mid-Sagittal Planes

Abstract

Object localization in space signals in the absence of an external reference (visual, auditory, haptic) involves a signal of the head in space (vestibular). The present study asks whether signals of body position relative to the support surface (proprioceptive) are involved as well, by investigating the role of vestibular-neck interaction (dissociating head and trunk position). Normal human subjects saw a light spot (object) and continuously nulled displacement steps of the spot. They did so before and after vestibular and/or neck rotational stimulation in the horizontal plane, reproducing a predesignated object localization in space (i), relative to the head mid-sagittal (ii), and relative to the trunk mid-sagittal (iii). The predominant frequency contained in the stimuli was varied (0.05, 0.1, and 0.4 Hz). (I) Object localization in space upon whole-body rotation (vestibular stimulus) at high frequency was veridical, whereas that at low frequency fell short. Almost identical results were obtained for trunk rotation about the stationary head (neck stimulus). In contrast, when combining the stimuli in the form of head rotation on the stationary trunk, the results were veridical, independent of stimulus frequency. Additional findings obtained with a large variety of vestibular-neck stimulus combinations suggest a linear summation of vestibular and neck signals. (II) Object localization with respect to the head was approximately veridical, being independent of vestibular and neck stimulation. However, this only applied if subjects were not biased by a head-in-space motion illusion of neck origin. (III) Object localization with respect to the trunk was veridical in all conditions tested. The findings support a recently developed concept, according to which humans evaluate the kinematic state of a visual object in space by (a) relating it to that of the body support by means of an essentially ideal proprioceptive coordinate transformation, and (b) relating, in turn, the kinematic state of the support to a vestibularly derived notion of space, using a proprioceptive coordinate transformation that “knows” the vestibular transfer characteristics. One important aspect is that object localization in space always is veridical during head and trunk rotation relative to a stationary support (for example, the ground) despite non-ideal vestibular transfer characteristics. Additional findings in patients with chronic loss of vestibular function confirm this concept.