Sodium pumps adapt spike bursting to stimulus statistics

Abstract

Pump activity is a homeostatic mechanism that maintains ionic gradients. Here we examined whether the slow reduction in excitability induced by sodium-pump activity that has been seen in many neuronal types is also involved in neuronal coding. We took intracellular recordings from a spike-bursting sensory neuron in the leech Hirudo medicinalis in response to naturalistic tactile stimuli with different statistical distributions. We show that regulation of excitability by sodium pumps is necessary for the neuron to make different responses depending on the statistical context of the stimuli. In particular, sodium-pump activity allowed spike-burst sizes and rates to code not for stimulus values per se, but for their ratio with the standard deviation of the stimulus distribution. Modeling further showed that sodium pumps can be a general mechanism of adaptation to statistics on the time scale of 1 min. These results implicate the ubiquitous pump activity in the adaptation of neural codes to statistics.

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Figure 1: Reduction in membrane excitability with stimulus variance.
Figure 2: Burst size and rate code for mechanical velocity.
Figure 3: Adaptive rescaling in burst size.
Figure 4: Adaptive rescaling in burst rates.
Figure 5: Blocking sodium pumps disrupts adaptive scaling.
Figure 6: Sodium pumps responsible for adaptive rescaling in a neuron model.

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Acknowledgements

W. Kristan is gratefully acknowledged for support in the initial stages and M. Juusola for lending the mechanical stimulators and the MatLab-based BIOSYST program for data acquisition. F. Gabbiani is acknowledged for critical comments. Discussions with B. Burton, M. Fuenlazida, R. Harris, S. Laughlin, P. Lombardo and R. Scuri were also appreciated. We thank Ministerio de Educación y Ciencia, Spain (R.G., G.G.d.P.), Comunidad de Madrid-Universidad Autonoma de Madrid (G.G.d.P.), Comunidad de Madrid (BIOCIENCIA program) (G.G.d.P.), and a Comunidad de Madrid fellowship (S.A.) for financial support.

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S.A. conducted experiments and performed significance tests, R.G. analyzed data, performed modeling and was responsible for writing parts of the supplementary information and G.G.d.P. conceived and directed the project, procured funding and wrote the paper.

Corresponding author

Correspondence to Gonzalo G de Polavieja.

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Arganda, S., Guantes, R. & de Polavieja, G. Sodium pumps adapt spike bursting to stimulus statistics. Nat Neurosci 10, 1467–1473 (2007). https://doi.org/10.1038/nn1982

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