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  Biological complexity facilitates tuning of the neuronal parameter space

Schneider, M., Bird, A. D., Gidon, A., Triesch, J., Jedlicka, P., & Cuntz, H. (2023). Biological complexity facilitates tuning of the neuronal parameter space. PLOS Computational Biology, 19(7): e1011212. doi:10.1371/journal.pcbi.1011212.

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Copyright: © 2023 Schneider et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Schneider, Marius1, 2, Author
Bird, Alexander D.1, 3, Author
Gidon, Albert, Author
Triesch, Jochen, Author
Jedlicka, Peter, Author
Cuntz, Hermann1, 3, Author                 
Jędrzejewska-Szmek, Joanna, Editor
Affiliations:
1Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Max Planck Society, ou_2074314              
2Vinck Lab, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Max Planck Society, Deutschordenstraße 46, 60528 Frankfurt, DE, ou_3381242              
3Cuntz Lab, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Max Planck Society, Deutschordenstraße 46, 60528 Frankfurt, DE, ou_3381227              

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Free keywords: Ion channels Action potentials Neurons Electrophysiology Potassium channels Behavior Neuronal tuning Random variables
 Abstract: The electrical and computational properties of neurons in our brains are determined by a rich repertoire of membrane-spanning ion channels and elaborate dendritic trees. However, the precise reason for this inherent complexity remains unknown, given that simpler models with fewer ion channels are also able to functionally reproduce the behaviour of some neurons. Here, we stochastically varied the ion channel densities of a biophysically detailed dentate gyrus granule cell model to produce a large population of putative granule cells, comparing those with all 15 original ion channels to their reduced but functional counterparts containing only 5 ion channels. Strikingly, valid parameter combinations in the full models were dramatically more frequent at ~6% vs. ~1% in the simpler model. The full models were also more stable in the face of perturbations to channel expression levels. Scaling up the numbers of ion channels artificially in the reduced models recovered these advantages confirming the key contribution of the actual number of ion channel types. We conclude that the diversity of ion channels gives a neuron greater flexibility and robustness to achieve a target excitability.

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Over the course of billions of years, evolution has led to a wide variety of biological systems. The emergence of the more complex among these seems surprising in the light of the high demands of searching for viable solutions in a correspondingly high-dimensional parameter space. In realistic neuron models with their inherently complex ion channel composition, we find a surprisingly large number of viable solutions when selecting parameters randomly. This effect is strongly reduced in models with fewer ion channel types but is recovered when inserting additional artificial ion channels. Because concepts from probability theory provide a plausible explanation for this improved distribution of valid model parameters, we propose that this effect may generalise to evolutionary selection in other complex biological systems.

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 Dates: 2023-07-03
 Publication Status: Published online
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 Rev. Type: Peer
 Identifiers: DOI: 10.1371/journal.pcbi.1011212
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Title: PLOS Computational Biology
Source Genre: Journal
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Pages: - Volume / Issue: 19 (7) Sequence Number: e1011212 Start / End Page: - Identifier: ISSN: 1553-7358