Adaptive coding is constrained to midline locations in a spatial listening task

Abstract

Although such adaptation is thought to improve coding of relevant stimulus features, the relationship between adaptation at the neural and behavioral levels remains to be established. Here we describe improved discrimination performance for an auditory spatial cue (interaural time differences, ITDs) following adaptation to stimulus statistics. Physiological recordings in the midbrain of anesthetized guinea pigs and measurement of discrimination performance in humans both demonstrate improved coding of the most prevalent ITDs in a distribution, but with highest accuracy maintained for ITDs corresponding to frontal locations, suggesting the existence of a fovea for auditory space. A biologically plausible model accounting for the physiological data suggests that neural tuning is stabilized by inhibition to maintain high discriminability for frontal locations. The data support the notion that adaptive coding in the midbrain is a key element of behaviorally efficient sound localization in dynamic acoustic environments.adaptation; interaural time difference; midbrain; neural model; psychophysics MOST SPECIES EVOLVE in complex environments containing diverse sources of sensory information over a very wide range of intensities, frequencies, and locations. Sensory systems must efficiently encode over this wide range of possible stimulus values, given a limited availability of coding resources. One means by which neural systems can overcome this challenge is to adapt on a behavioral timescale in order to represent with particular efficiency the subset of natural stimuli in the current environment. Such adaptive coding is observed across a wide range of species and stimulus modalities and is apparent in the responses of single neurons (Dean et al. 2005;Fairhall et al. 2001;Ohzawa et al. 1982) and across populations of neurons (Dean et al. 2005(Dean et al. , 2008Watkins and Barbour 2008). Fisher information (FI) represents one possible measure of coding quality that can be used to evaluate adaptive coding (Dean et al. 2005).Nevertheless, despite the apparent advantage adaptive coding would confer on sensory processing, the link between adaptive coding at the neural level and performance in sensory tasks is difficult to establish. Psychophysical assessment of adapted neural systems is often considered with respect to perceptual illusions such as afterimages (McCollough 1965) At the cognitive level, the term "cuing" is employed to describe the influence of prior stimulation on sensory performance, for example, in reducing reaction times required to localize a sound source in a given spatial hemifield (Spence and Driver 1994).However, none of these concepts-aftereffects, mislocalization, or cuing-is easily reconciled with the concept of adaptive coding at the neural level. This normally describes the rapid adjustment of neural tuning properties to better represent the prevailing stimulus environment (Garcia-Lazaro et al. 2007;Maravall et al. 2007; Nagel and Doupe 2006) rather than neural fatigue or higher, perhaps attentiona...

Cortical modulation of auditory processing in the midbrain

“…One mechanism for adapting to the presence of an earplug in one ear would be to adjust the sensitivity of auditory neurons to binaural localization cues. Recent studies have shown that the sensitivity of IC neurons to interaural level differences (ILDs; Dahmen et al, 2010) and interaural time differences (ITDs; Maier et al, 2012) can change following short-term adaptation to stimulus statistics, and, as previously illustrated (Figure 8), cortical cooling can produce pronounced alterations in collicular firing-rate-ILD functions. Behavioral evidence, however, suggests that adaptation to a conductive hearing loss in one ear takes place by learning to reweight different localization cues in favor of the monaural spectral localization cues provided by the non-occluded ear rather than by remapping the altered binaural cues (Kacelnik et al, 2006; Kumpik et al, 2010).…”

Directing Eye Gaze Enhances Auditory Spatial Cue Discrimination

“…The best coding resolution, i.e., the most information, is found in this steeper region [30]. Intensity and ITD response functions have been shown to shift as result of adapting to stimulus statistics [31, 32]. Such shifts of nonlinear response functions change the operating point, resulting in larger differences in neural firing rates.…”

Visual task enhances spatial selectivity in the human auditory cortex

“…These coincide normally with locations directly in front (Stecker et al, 2005). In the subcortical neurons described in these previous studies, the slope of the tuning curve tended to approach the location from which the majority of sounds originated (Dahmen et al, 2010; Maier et al, 2012). Thereby, these neurons shift their best discrimination ability toward the direction in which most of the sound sources reside.…”

“…However, recent animal studies have described an alternative mechanisms through which the population rate code might be able to target better selectivity to specific spatial locations. This has been described in subcortical auditory neurons as an adaptation mechanism to stimulation statistics (Dahmen et al, 2010; Maier et al, 2012). In the wide spatial tuning curves, the best discrimination power between sound source locations is provided by the steepest parts of the slopes.…”