Neuronal representations of distance in human auditory cortex

Abstract

Neuronal mechanisms of auditory distance perception are poorly understood, largely because contributions of intensity and distance processing are difficult to differentiate. Typically, the received intensity increases when sound sources approach us. However, we can also distinguish between soft-but-nearby and loud-but-distant sounds, indicating that distance processing can also be based on intensity-independent cues. Here, we combined behavioral experiments, fMRI measurements, and computational analyses to identify the neural representation of distance independent of intensity. In a virtual reverberant environment, we simulated sound sources at varying distances (15-100 cm) along the right-side interaural axis. Our acoustic analysis suggested that, of the individual intensity-independent depth cues available for these stimuli, direct-to-reverberant ratio (D/R) is more reliable and robust than interaural level difference (ILD). However, on the basis of our behavioral results, subjects' discrimination performance was more consistent with complex intensity-independent distance representations, combining both available cues, than with representations on the basis of either D/R or ILD individually. fMRI activations to sounds varying in distance (containing all cues, including intensity), compared with activations to sounds varying in intensity only, were significantly increased in the planum temporale and posterior superior temporal gyrus contralateral to the direction of stimulation. This fMRI result suggests that neurons in posterior nonprimary auditory cortices, in or near the areas processing other auditory spatial features, are sensitive to intensity-independent sound properties relevant for auditory distance perception.

Asymmetries in behavioral and neural responses to spectral cues demonstrate the generality of auditory looming bias

“…Previous studies addressed this issue by comparing sounds of different spectral structure: complex tones elicited stronger behavioral looming bias (2, 11) and larger neural differences (14-16) than did noise with equal intensity increase, indicating that intensity changes did not directly cause looming bias. However, studies with a different spatial task (17) or species (10) found the opposite effect (i.e., stronger looming bias for noise than tonal sounds), calling into question these results.An early fMRI study that contrasted static sounds with sounds increasing or decreasing in intensity found activity in the right planum temporale (4), which is associated with processing of auditory motion in any spatial direction (18,19), consistent with the idea that sound intensity changes can be perceived as motion in distance. The contrast between sounds increasing vs. decreasing in intensity, however, revealed a different network, including superior temporal sulcus and amygdala, which may reflect a warning process for approaching objects (4,9,20).…”

“…An early fMRI study that contrasted static sounds with sounds increasing or decreasing in intensity found activity in the right planum temporale (4), which is associated with processing of auditory motion in any spatial direction (18,19), consistent with the idea that sound intensity changes can be perceived as motion in distance. The contrast between sounds increasing vs. decreasing in intensity, however, revealed a different network, including superior temporal sulcus and amygdala, which may reflect a warning process for approaching objects (4,9,20).…”

“…Interaural level differences (ILDs) are also known to act as cues for distance perception (18,29). Relative changes in frequencyspecific ILDs can be easily extracted from loudness predictions (Fig.…”

“…of ILDs (35), which is arguably a prominent auditory distance cue (18,29,36). Further experiments and/or modeling analyses will be required to clarify the perceptual weighting of these potential distance cues.…”

Psychophysics and neuronal bases of sound localization in humans

“…In humans, the putative posterior auditory “ where ” pathway, encompassing the planum temporale (PT) and posterior superior temporal gyrus (STG), is strongly activated by horizontal sound direction changes (Ahveninen et al, 2006; Brunetti et al, 2005; Deouell et al, 2007; Tata et al, 2005), movement (Baumgart et al, 1999; Formisano et al, 2003; Krumbholz et al, 2005; Warren et al, 2002), intensity-independent distance cues (Kopco et al, 2012), and under conditions where separation of multiple sound sources is required (Zündorf et al, 2013). However, it is still unclear how the human AC encodes the acoustic space: Is there an orderly topographic organization of neurons representing different spatial origins of sounds, or are sound locations, even at the level of non-primary cortices, computed by neurons that are broadly tuned to more basic cues such as ITD and ILD, using a “two-channel” rate code (McAlpine, 2005; Middlebrooks et al, 1994; Middlebrooks et al, 1998; Stecker et al, 2003; Werner-Reiss et al, 2008)?…”