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Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content

Abstract

Although examples of variation and diversity exist throughout the nervous system, their importance remains a source of debate. Even neurons of the same molecular type have notable intrinsic differences. Largely unknown, however, is the degree to which these differences impair or assist neural coding. We examined the outputs from a single type of neuron, the mitral cells of the mouse olfactory bulb, to identical stimuli and found that each cell's spiking response was dictated by its unique biophysical fingerprint. Using this intrinsic heterogeneity, diverse populations were able to code for twofold more information than their homogeneous counterparts. In addition, biophysical variability alone reduced pair-wise output spike correlations to low levels. Our results indicate that intrinsic neuronal diversity is important for neural coding and is not simply the result of biological imprecision.

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Figure 1: Intrinsic diversity of mitral cell populations.
Figure 2: Uniqueness of mitral cell output to identical input.
Figure 3: Intrinsic diversity affects pair-wise spike train correlations.
Figure 4: Mitral cell STA diversity.
Figure 5: Heterogeneous populations of mitral cells carry more information than their homogeneous counterparts.
Figure 6: Biophysical diversity correlates to information transfer.
Figure 7: Heterogeneous populations improve the coding of physiologically relevant stimuli.

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Acknowledgements

We wish to thank G.M. LaRocca for assistance with the immunohistochemistry and B. Benedetti, A. Barth, J. Castro and members of the Urban laboratory for helpful comments on this manuscript. Funding was provided by the National Institute on Deafness and Other Communication Disorders (R01DC0005798).

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K.P. conducted the experiments and the analysis. K.P. and N.N.U. wrote the manuscript.

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Correspondence to Nathaniel N Urban.

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The authors declare no competing financial interests.

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Padmanabhan, K., Urban, N. Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat Neurosci 13, 1276–1282 (2010). https://doi.org/10.1038/nn.2630

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