Advancing age alters the influence of eye position on sound localization

Abstract

Vision and audition provide spatial information about the environment to guide natural behavior. Because the eyes move in the head while the ears remain head-fixed, input conveying eye position in the head is required to maintain audiovisual congruence. Human perception of auditory space was previously shown to shift with changes in eye position, regardless of the target's frequency content and spatial cues underlying horizontal and vertical localization. In this study, we examined whether this interaction is altered by advancing age. Head-restrained young (18-44 yo), middle-aged (45-64 yo), and elderly (65-81 yo) human subjects localized noise bursts under conditions of transient and sustained ocular deflection. All three age groups demonstrated a time-dependent shift of auditory space in the direction of eye position. Moreover, this adaptation showed a clear decline with advancing age, but only for peripheral auditory space (beyond ±10° from midline). Alternatively, adaptation in the periphery may occur, but is more sluggish than in the central field and therefore not fully observed in this experiment. The age-dependent effect cannot be readily explained by senescent peripheral hearing loss, suggesting a change in central processing of auditory space in relation to the control of gaze.

Fig. 1

Experimental setup. a Subject position and laboratory configuration. b Target array of 61 locations within ± 50° Az by ±25° El, including 13 multi-sampled locations at 10° intervals (5 trials per session). This appears in similar fashion in a; filled symbols signify multi-sampled targets. Fixation spots appear as larger open symbols in both a and b. (Reproduced with permission from the Journal of Neuroscience, © Society for Neuroscience)

Fig. 2

Localization accuracy (signed error between response and target location) in Az for multi-sampled targets in the horizontal plane (0° El) for Young (a), Middle-aged (b), and Elderly (c) subjects for the target fixation paradigm, and the Ctr, L20° and R20° sustained fixation paradigm. Data points are offset slightly in Az for graphic clarity. The slope of accuracy vs. target location is related to spatial gain (SG = slope ? 1.0, where 1.0 represents perfect performance). All age groups demonstrated comparable overshoot (Az SG > 1.0, or a positive slope as shown here) during target fixation. However, the overshoot is reduced significantly with Ctr fixation in the Young and the Middle-aged, but not in the Elderly. Eccentric fixation (L and R 20°) predominantly shifts perceived target Az in the direction of gaze across space

Fig. 3

a Localization accuracy in Az during eccentric fixation (L and R) pooled within age groups and adjusted with respect to eye position such that foveal fixation is at −20° and positive auditory space is contralateral to fixation for all eccentric fixation conditions. Shift magnitude (error) is significantly lower in peripheral auditory space in the Elderly than in the other age groups. b During sustained eccentric (L and R) fixation, Az shift magnitude declines more with increasing age for peripheral targets (beyond ±10° of zero and excluding the fixation point at −20°) than for central targets (midline ±10°). The age-related decline in the shift magnitude of peripheral, but not central, auditory targets occurs in a progressive fashion; within age group averages (open rectangle) serve to emphasize the tread; values are offset for clarity; error bars indicate SD across subjects