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Only negligible deviations from electroneutrality are expected in dendritic spines

Nature Reviews Neuroscience volume 21, page 53 (2020)Cite this article

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The central aim of the Opinion article by Holcman and Yuste (The new nanophysiology: regulation of ionic flow in neuronal subcompartments. Nat. Rev. Neurosci. 16, 685–692 (2015))1 is to suggest that revolutionary ionic and electrical behaviour will be identified and understood if we no longer apply the classical constraint of electroneutrality when modelling electrodiffusion in small neuronal structures such as dendritic spines. However, as I have argued online2, the authors misunderstand the origin of the electroneutrality approximation and present inconsistent calculations that are irrelevant in a biological context. The result is a misleading and deeply confusing Perspective.

The authors calculate distributions of charges in a dieletric ball, which is intended to approximate a spine head. The relative permittivity of the dielectric is that of water, but its conductivity is zero. The authors only consider a single species of ion. In so doing, they ignore completely the large and nearly balanced concentrations of positive and negative ions (and small molecules) that are present inside and outside mammalian neurons. These ions transform the physiological solutions into conductors and cause shielding of charges over an extremely short distance — the Debye length, which is less than a nanometre at physiological ionic strength3. No direct electrostatic interactions can operate much beyond this length. However, by ignoring the background ions, the authors enable direct repulsion over microns, 1000-fold greater distances. These considerations of a single charged species are therefore without apparent relevance to the biological situation.

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References

  1. Holcman, D. & Yuste, R. The new nanophysiology: regulation of ionic flow in neuronal subcompartments. Nat. Rev. Neurosci. 16, 685–692 (2015).

    Article  CAS  Google Scholar 

  2. Barbour, B. The electroneutrality liberation front. https://referee3.org/2018/08/14/the-electroneutrality-liberation-front/ (2018).

  3. Hille, B. Ion channels of excitable membranes (Sinauer, 2001).

  4. Holcman, D. & Yuste, R. Answer to B. Barbour fiction-blog about a perspective article: “The new nanophysiology: regulation of ionic flow in neuronal subcompartments”. https://www.ibens.ens.fr/IMG/pdf/response-barbour4_tl_rydh.pdf (2018).

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Acknowledgements

The author thanks J. Ranft, V. Hakim and P. Serna for helpful discussion.

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  1. Institut de biologie de l’École normale supérieure (IBENS), École normale supérieure, CNRS, INSERM, PSL University, Paris, France

    Boris Barbour

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Correspondence to Boris Barbour.

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Barbour, B. Only negligible deviations from electroneutrality are expected in dendritic spines. Nat Rev Neurosci 21, 53 (2020). https://doi.org/10.1038/s41583-019-0238-x

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