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The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits

Abstract

The primary auditory cortex (A1) is organized tonotopically, with neurons sensitive to high and low frequencies arranged in a rostro-caudal gradient. We used laser scanning photostimulation in acute slices to study the organization of local excitatory connections onto layers 2 and 3 (L2/3) of the mouse A1. Consistent with the organization of other cortical regions, synaptic inputs along the isofrequency axis (orthogonal to the tonotopic axis) arose predominantly within a column. By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column. In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3. Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

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Figure 1: Auditory cortex LSPS experimental preparation.
Figure 2: Synaptic input organization along the isofrequency axis.
Figure 3: Synaptic input organization along the tonotopic axis.
Figure 4: Along tonotopic but not isofrequency axis, inputs to L3 arise asymmetrically out-of-column.
Figure 5: Synaptic input correlation between pairs of auditory cortical neurons.
Figure 6: L3 neurons are less responsive to simple auditory stimuli than L2 neurons.

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Acknowledgements

We thank B. Burbach for invaluable technical help, S. Joshi for invaluable input on juxtacellular labeling, N. Gray, G. Otazu and T. Hackett for discussions, and W. Bair (Department of Physiology, Anatomy and Genetics, University of Oxford) for spike detection software. This work was supported by grants from the US National Institutes of Health, the Patterson Foundation (H.V.O.) the Swartz Foundation and Autism Speaks.

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H.V.O. and A.M.Z. conceived the experiments, analyzed the data and wrote the paper. H.V.O. performed all the experiments. I.B. and K.S. provided expert advice and LSPS experimental set-up.

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Correspondence to Anthony M Zador.

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Oviedo, H., Bureau, I., Svoboda, K. et al. The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits. Nat Neurosci 13, 1413–1420 (2010). https://doi.org/10.1038/nn.2659

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