Acoustic factors govern developmental sharpening of spatial tuning in the auditory cortex

Abstract

Auditory localization relies on the detection and interpretation of acoustic cues that change in value as the head and external ears grow. Here we show that the maturation of these structures is an important determinant for the development of spatial selectivity in the ferret auditory cortex. Spatial response fields (SRFs) of high-frequency cortical neurons recorded at postnatal days (P) 33–39 were broader, and transmitted less information about stimulus direction, than in older ferrets. They also exhibited slightly broader frequency tuning than neurons recorded in adult animals. However, when infant neurons were stimulated through virtual ears of adults, SRFs sharpened significantly and the amount of transmitted information increased. This improvement was predicted by a model that generates SRF shape from the localization cue values and the neurons' binaural spectrotemporal response properties. The maturation of spatial response characteristics in auditory cortex therefore seems to be limited by peripheral rather than by central factors.

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Figure 1: Representative examples of near-threshold SRFs in ferret A1 at various developmental ages.
Figure 2: Sound-level dependence of SRF tuning parameters at different ages.
Figure 3: Summary of directional preferences of all recordings in infant (left) and adult (right) animals.
Figure 4: Infant spatial cues are less directional than in adult ferrets.
Figure 5: Pair-wise comparison of infant (P33–39) SRFs recorded with the animal's own acoustic cues (own ears) and with those from an adult ferret (adult ears) for five representative single units.
Figure 6: Listening through adult ears reduces the size of and increases the amount of information transmitted by infant near-threshold SRFs.
Figure 7: Switching between infant and adult acoustic cue values changes the size of the predicted SRFs of A1 units.
Figure 8: Temporal and spectral response properties of A1 neurons in infants and adults.

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Acknowledgements

We are grateful to I. Thompson for critique of an earlier draft, and to I. Nelken for advice on information theory. Our research was sponsored by the Wellcome Trust (Senior Research Fellowship to A.J.K., Research Studentship to T.D.M.F.) and Defeating Deafness (Dunhill Medical Research Trust Research Fellowship to J.W.H.S.).

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Correspondence to Andrew J King.

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Mrsic-Flogel, T., Schnupp, J. & King, A. Acoustic factors govern developmental sharpening of spatial tuning in the auditory cortex. Nat Neurosci 6, 981–988 (2003). https://doi.org/10.1038/nn1108

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