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Efficient coding of natural scenes improves neural system identification

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  • Yongrong Qiu
  • David A Klindt
  • Klaudia P Szatko
  • Dominic Gonschorek
  • Larissa Hoefling
  • Timm Schubert
  • Laura Busse
  • Matthias Bethge
  • Thomas Euler

Abstract

Neural system identification aims at learning the response function of neurons to arbitrary stimuli using experimentally recorded data, but typically does not leverage normative principles such as efficient coding of natural environments. Visual systems, however, have evolved to efficiently process input from the natural environment. Here, we present a normative network regularization for system identification models by incorporating, as a regularizer, the efficient coding hypothesis, which states that neural response properties of sensory representations are strongly shaped by the need to preserve most of the stimulus information with limited resources. Using this approach, we explored if a system identification model can be improved by sharing its convolutional filters with those of an autoencoder which aims to efficiently encode natural stimuli. To this end, we built a hybrid model to predict the responses of retinal neurons to noise stimuli. This approach did not only yield a higher performance than the “stand-alone” system identification model, it also produced more biologically plausible filters, meaning that they more closely resembled neural representation in early visual systems. We found these results applied to retinal responses to different artificial stimuli and across model architectures. Moreover, our normatively regularized model performed particularly well in predicting responses of direction-of-motion sensitive retinal neurons. The benefit of natural scene statistics became marginal, however, for predicting the responses to natural movies. In summary, our results indicate that efficiently encoding environmental inputs can improve system identification models, at least for noise stimuli, and point to the benefit of probing the visual system with naturalistic stimuli.Author summary: Computational models use experimental data to learn stimulus-response functions of neurons, but they are rarely informed by normative coding principles, such as the idea that sensory neural systems have evolved to efficiently process natural stimuli. We here introduce a novel method to incorporate natural scene statistics to predict responses of retinal neurons to visual stimuli. We show that considering efficient representations of natural scenes improves the model’s predictive performance and produces biologically-plausible receptive fields, at least for responses to noise stimuli. Generally, our approach provides a promising framework to test various (normative) coding principles using experimental data for understanding the computations of biological neural networks.

Suggested Citation

  • Yongrong Qiu & David A Klindt & Klaudia P Szatko & Dominic Gonschorek & Larissa Hoefling & Timm Schubert & Laura Busse & Matthias Bethge & Thomas Euler, 2023. "Efficient coding of natural scenes improves neural system identification," PLOS Computational Biology, Public Library of Science, vol. 19(4), pages 1-29, April.
  • Handle: RePEc:plo:pcbi00:1011037
    DOI: 10.1371/journal.pcbi.1011037
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    References listed on IDEAS

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    1. Jonathan W. Pillow & Jonathon Shlens & Liam Paninski & Alexander Sher & Alan M. Litke & E. J. Chichilnisky & Eero P. Simoncelli, 2008. "Spatio-temporal correlations and visual signalling in a complete neuronal population," Nature, Nature, vol. 454(7207), pages 995-999, August.
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    Cited by:

    1. Nan Wu & Isabel Valera & Fabian Sinz & Alexander Ecker & Thomas Euler & Yongrong Qiu, 2024. "Probabilistic neural transfer function estimation with Bayesian system identification," PLOS Computational Biology, Public Library of Science, vol. 20(7), pages 1-21, July.

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