The Dynamics of Context-Dependent Space Representations in Auditory Cortex

Auditory space is not mapped onto the receptor surface in the inner ear but results from complex neuronal computations by our brain. However, there is no consensus about the resulting neuronal representation of space in auditory cortex (AC) owing to contradicting reports: While many studies found a tuning preference for sound source positions in the contralateral hemisphere, others have observed an additional population of cells tuned to midline positions or even context-dependent dynamic changes in the tuning of individual cells. A fundamental difference across studies was the animals brain state, which might affect AC processing and thus the apparent nature of its spatial code. Yet no study to date investigated spatial tuning of identified AC neurons across brain states. Here, we employed longitudinal two-photon calcium imaging in the AC of mice under distinct states of wakefulness: anesthetized, idle awake, and during involvement in a go/no-go localization task. We find that previously reported differences in coding regimes are directly linked to wakefulness: A strong contralateral tuning bias is present under anesthesia, while pronounced and stable mid-line tuning appeared in awake but idle animals. Intriguingly, in localizing mice, tuning was different again with a large proportion of AC neurons responding to the position of the currently relevant sound-source. These population regimes remained stable across imaging sessions despite the spatial tuning of individual neurons being highly variable. Our findings resolve apparent contradictions in the literature and thus give a dynamical explanation for the multiple space representations in the AC.