Evoked Responses to Localized Sounds Suggest Linear Representation of Elevation in Human Auditory Cortex

Abstract

The auditory system computes the position of a sound along each of the three spatial axes, azimuth, elevation and distance, from very different acoustical cues. The extraction of sound azimuth from binaural cues (differences in arrival time and intensity between the ears) is well understood, as is the representation of these binaural cues in the auditory cortex of different species. Sound elevation is computed from monaural spectral cues arising from direction-dependent filtering of the pinnae, head, and upper body. The cortical representation of these cues in humans is still debated. We have shown that the fMRI blood-oxigen level-dependent activity in small parts of auditory cortex relates monotonically to perceived sound elevation and tracks listeners internal adaptation to new spectral cues. Here we confirm the previously suggested cortical code with a different method that reflects neural activity rather than blood oxigenation (electroencephalography), show that elevation is represented relatively late in the cortex, with related activity peaking at about 400 ms after sound onset, and show that differences in sound elevation can be decoded from the electroencephalogram of listeners, particularely from those who can distinguish elevations well. We used an adaptation design to isolate elevation-specific brain responses from those to other features of the stimuli. These responses gradually increased with decreasing sound elevation, consistent with our previous fMRI findings and population rate code for sound elevation. The long latency as well as the topographical distribution of the elevation-specific brain response indicates the involvement of higher-level cognitive processes not present for binaural cue representation. The differences between brain responses to sounds at different elevations predicted the listeners sound localization accuracy, suggesting that these responses reflect perceived elevation. This is, to our knowledge, the first study that demonstrates the cortical encoding of sound elevation in humans with high-temporal resolution. Our results agree with previous findings from functional magnetic resonance imaging, providing strong support for the hypothesis that elevation is represented in a population-rate code. This represents a critical advance in our understanding of spatial auditory processing along a dimension that is still poorly understood.