A Population Rate Code of Auditory Space in the Human Cortex

Abstract

BackgroundPrevious work on the human auditory cortex has revealed areas specialized in spatial processing but how the neurons in these areas represent the location of a sound source remains unknown.Methodology/Principal FindingsHere, we performed a magnetoencephalography (MEG) experiment with the aim of revealing the neural code of auditory space implemented by the human cortex. In a stimulus-specific adaptation paradigm, realistic spatial sound stimuli were presented in pairs of adaptor and probe locations. We found that the attenuation of the N1m response depended strongly on the spatial arrangement of the two sound sources. These location-specific effects showed that sounds originating from locations within the same hemifield activated the same neuronal population regardless of the spatial separation between the sound sources. In contrast, sounds originating from opposite hemifields activated separate groups of neurons.Conclusions/SignificanceThese results are highly consistent with a rate code of spatial location formed by two opponent populations, one tuned to locations in the left and the other to those in the right. This indicates that the neuronal code of sound source location implemented by the human auditory cortex is similar to that previously found in other primates.

Lateralization and Binaural Interaction of Middle-Latency and Late-Brainstem Components of the Auditory Evoked Response

“…It is also consistent with human fMRI data, which has shown that primary auditory cortex is highly sensitive to both ear of stimulation (Woods et al 2010;Stecker et al 2015;Gutschalk and Steinmann 2015) and interaural level differences (ILDs) Stecker et al 2015), but not ITD (von Kriegstein et al 2008;McLaughlin et al 2015). Although ITD sensitivity has been found in human auditory cortex, it is generally located in more posterolateral areas (von Kriegstein et al 2008;McLaughlin et al 2015) and in long-as opposed to middle-latency components of the AER (McEvoy et al 1993;Salminen et al 2009;Salminen et al 2010;Magezi and Krumbholz 2010;Gutschalk et al 2012) (for reviews, see Salminen et al 2012;Gutschalk 2014). In any case, the population-level representation of ITD at the level of the midbrain might be fundamentally different from that found in primary AC (Thompson et al 2006;von Kriegstein et al 2008;Belliveau et al 2014;Vonderschen and Wagner 2014;Yao et al 2015), though this is in need of further clarification.…”

Relative sound localisation abilities in human listeners

“…Previous neuroimaging studies have measured the change in neural activity elicited by a change in sound source location following a brief adapting stimulus in order to compare two-channel and topographic models of sound localisation and have demonstrated that predictions generated from a two-channel model best match the observed data (Salminen et al, 2009;Salminen et al, 2010;Magezi and Krumbholz, 2010;Briley et al, 2013). In order to compare our observed behavioural performance to that predicted by FIG.…”

“…Three simple models were developed where auditory space was represented as a two-channel model, a topographic model, or a modified topographic model, based on recent nonbehavioural imaging studies that tested brain responses to shifts in sound source locations (Salminen et al, 2009;Salminen et al, 2010;Magezi and Krumbholz, 2010), and predictions were generated for psychophysical performance in this task. Specifically, the two-channel and modified topographic model predicted that performance should be better around the midline than in the periphery, while only the modified topographic model, predicted that performance should differ (specifically should be superior) for inward-as compared to outward-moving sounds.…”

“…This model was first proposed for the encoding of ITD in small mammals (McAlpine et al, 2001) and was adapted to the auditory cortex following the observation that neural tuning in auditory cortex was typically broad and contralateral (Stecker et al, 2005). While such a model is likely an over-simplification, recent human imaging studies have suggested that both sound localisation cues and auditory space might be represented in human auditory cortex by this kind of "hemifield code" (Salminen et al, 2009;Salminen et al, 2010;Magezi and Krumbholz, 2010;Briley et al, 2013).…”

Neuronal representations of distance in human auditory cortex

“…However, given that only one simulated direction was studied, the present data cannot offer conclusive evidence that the distance of sounds originating on one side of the head is always represented by the contralateral hemisphere or that soundsource distance (or direction) is represented in a topographical fashion analogous to other sensory modalities (note also evidence supporting an alternative two-channel model, refs. [40][41][42].…”