Egocentric and allocentric representations in auditory cortex

Abstract

A key function of the brain is to provide a stable representation of an object’s location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which neurons represent sound space remains undefined: classical spatial receptive fields in head-fixed subjects can be explained either by sensitivity to sound source location relative to the head (egocentric) or relative to the world (allocentric encoding). This coordinate frame ambiguity can be resolved by studying freely moving subjects; here we recorded spatial receptive fields in the auditory cortex of freely moving ferrets. We found that most spatially tuned neurons represented sound source location relative to the head across changes in head position and direction. In addition, we also recorded a small number of neurons in which sound location was represented in a world-centered coordinate frame. We used measurements of spatial tuning across changes in head position and direction to explore the influence of sound source distance and speed of head movement on auditory cortical activity and spatial tuning. Modulation depth of spatial tuning increased with distance for egocentric but not allocentric units, whereas, for both populations, modulation was stronger at faster movement speeds. Our findings suggest that early auditory cortex primarily represents sound source location relative to ourselves but that a minority of cells can represent sound location in the world independent of our own position.

Author summary

When we hear a sound, we can describe its location relative to ourselves (e.g., “the phone is on my right”) or relative to the world (e.g., “the phone is in the corner”). These descriptions of space are known as egocentric and allocentric, respectively, and illustrate the representation of sound location in reference frames defined either by the observer or the world. We know that neurons in the brain can represent the location of a sound source. However, previous experiments have been performed in static subjects, in which it’s not possible to tell whether spatial tuning reflects sensitivity to the position of the sound relative to the head or in the world. Here, we recorded neurons in the auditory cortex of freely moving ferrets and showed that most cells represent the position of a sound relative to the head, i.e., in an egocentric reference frame. We also recorded a smaller number of allocentric cells that were tuned to the position of a sound in the world, across the movement of the subject. By recording in freely moving animals, we were also able to investigate the neural encoding of sound source distance and the modulation of auditory processing by head movement speed.