Auditory Spatial Perception Dynamically Realigns with Changing Eye Position

Abstract

Audition and vision both form spatial maps of the environment in the brain, and their congruency requires alignment and calibration. Because audition is referenced to the head and vision is referenced to movable eyes, the brain must accurately account for eye position to maintain alignment between the two modalities as well as perceptual space constancy. Changes in eye position are known to variably, but inconsistently, shift sound localization, suggesting subtle shortcomings in the accuracy or use of eye position signals. We systematically and directly quantified sound localization across a broad spatial range and over time after changes in eye position. A sustained fixation task addressed the spatial (steady-state) attributes of eye position-dependent effects on sound localization. Subjects continuously fixated visual reference spots straight ahead (center), to the left (20°), or to the right (20°) of the midline in separate sessions while localizing auditory targets using a laser pointer guided by peripheral vision. An alternating fixation task focused on the temporal (dynamic) aspects of auditory spatial shifts after changes in eye position. Localization proceeded as in sustained fixation, except that eye position alternated between the three fixation references over multiple epochs, each lasting minutes. Auditory space shifted by ϳ40% toward the new eye position and dynamically over several minutes. We propose that this spatial shift reflects an adaptation mechanism for aligning the "straight-ahead" of perceived sensory-motor maps, particularly during early childhood when normal ocular alignment is achieved, but also resolving challenges to normal spatial perception throughout life.

Dependence of auditory spatial updating on vestibular, proprioceptive, and efference copy signals

“…Even if subjects maintained eccentric eye positions following active head movement, it would not be sufficient to explain our results because the effect of eye position on auditory localization is small (3°for 45°eye turn) compared with differences in auditory localization observed across conditions in the present study (8°difference between Active and Passive conditions for 30°head turn); the small effect of eye position is further reduced in complete darkness (Lewald and Ehrenstein 1996). Although larger effects of eye movements have been reported (Razavi et al 2007), these effects are typically observed only after an eccentric eye position is maintained for an extended period of time. Thus the effect of eye position signals on the current results is likely negligible.…”

Contextual plasticity, top-down, and non-auditory factors in sound localization with a distractor

“…Overall, the Keyboard response method was the most accurate, introducing only an approximate constant frontal bias. This bias is likely related to the fact that the subjects tended to look straight ahead before the stimulus was presented in each Keyboard-run trial, as previous studies reported that sound localization can be biased toward the gaze direction (Razavi et al, 2007). The pattern of results observed in the Open-Eyes-Pointer condition was similar, even though it was less consistent, possibly because the subjects did not use vision to guide their responses to the most lateral targets.…”

Influence of aging on human sound localization

“…This rapid adaptation of auditory space in the direction of eye position in the head applied equally to all experiments reported here and is unlikely to have biased the comparisons across conditions. Eye-position-dependent adaptation has been addressed at length previously by our group (Cui et al 2010a;Dobreva 2010;Razavi et al 2007) and by others (Bohlander 1984;Lewald 1998Lewald , 1997Lewald et al 2000;Ehrenstein 1998, 1996;Lewald and Getzmann 2006;Weerts and Thurlow 1971;Yao and Peck 1997).…”

“…The experimental environment has been described previously (Cui et al 2010a,b;Razavi et al 2007;Zwiers et al 2003). Subjects were seated in a fully enclosed and darkened room (3.0 x 3.7 ϫ 2.7 m) lined with 3-in.…”

“…Horizontal and vertical joystick position (i.e., subject response) was digitally encoded (at a resolution of Ͻ0.1°). It is important to note that subjects were free to move their eyes to aid pointing with foveal vision ("target fixation" paradigm; Razavi et al 2007) in all experiments in this study. Target fixation yields results distinctly different from those obtained with central ocular fixation in which peripheral vision guides pointing (Razavi et al 2007).…”