Abstract
While a topographic map of auditory space exists in the vertebrate midbrain, it is absent in the forebrain. Yet, both brain regions are implicated in sound localization. The heterogeneous spatial tuning of adjacent sites in the forebrain compared to the midbrain reflects different underlying circuitries, which is expected to affect the correlation structure, i.e., signal (similarity of tuning) and noise (trial-by-trial variability) correlations. Recent studies have drawn attention to the impact of response correlations on the information readout from a neural population. We thus analyzed the correlation structure in midbrain and forebrain regions of the barn owl’s auditory system. Tetrodes were used to record in the midbrain and two forebrain regions, Field L and the downstream auditory arcopallium (AAr), in anesthetized owls. Nearby neurons in the midbrain showed high signal and noise correlations, consistent with shared inputs. As previously reported, Field L was arranged in random clusters of similarly tuned neurons. Interestingly, AAr neurons displayed homogeneous monotonic azimuth tuning, while response variability of nearby neurons was significantly less correlated than the midbrain. Using a decoding approach, we demonstrate that low noise correlation in AAr restricts the potentially detrimental effect it can have on information, assuming a rate-code proposed for mammalian sound localization. This study harnesses the power of correlation structure analysis to investigate the coding of auditory space. Our findings demonstrate distinct correlation structures in the auditory midbrain and forebrain, which would be beneficial for a rate-code framework for sound localization in the non-topographic forebrain representation of auditory space.
Significance Statement Despite their established involvement in sound localization, our understanding of how the midbrain and forebrain encode sound location is limited. An outstanding difference between these regions is the lack of obvious topographic representations of auditory space in the forebrain. To shed light on the circuit function, we examined the tuning and correlation structure in responses of nearby neurons in the midbrain and forebrain. Interestingly, a different correlation structure emerged in the forebrain: uniform tuning shape and uncorrelated response variability. This finding highlights differences between the midbrain and forebrain representation of auditory space and provides evidence supporting a rate-code for sound location in the forebrain.
Footnotes
The authors declare no competing financial interests.
This work was supported by the National Institute of Health grant DC007690.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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