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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Physiol. | doi: 10.3389/fphys.2019.01444

Non-synaptic plasticity in leech touch cells

  • 1Department of Neuroscience, School of Medicine and Health Sciences, Carl von Ossietzky University Oldenburg, Germany
  • 2Cluster of Excellence Hearing4all, Germany

The role of Na+/K+-pumps in activity-dependent synaptic plasticity has been described in both vertebrates and invertebrates. Here we provide evidence that the Na+/K+-pump is also involved in activity-dependent non-synaptic cellular plasticity in leech sensory neurons. We show that the resting membrane potential of T cells hyperpolarizes in response to repeated somatic current injection, while at the same time their spike count and the input resistance increase. Our Hodgkin-Huxley-type neuron model, adjusted to physiological T cell properties, suggests that repetitive action potential discharges lead to increased Na+/K+-pump activity, which then hyperpolarizes the resting membrane potential. In consequence, a slow, non-inactivating current decreases, which is presumably mediated by voltage-dependent, low-threshold potassium channels. Closing of these putative M-type channels due to hyperpolarization of the resting potential increases the input resistance of the cell, leading to a larger number of spikes. By this mechanism, the response behavior switches from rapidly to slowly adapting spiking. These changes in spiking behavior also effect other T cells on the same side of the ganglion, which are connected via a combination of electrical and chemical synapses. An increased spike count in the presynaptic T cell results in larger postsynaptic responses in the other T cells. However, when the number of elicited presynaptic spikes is kept constant, the postsynaptic response does not change. These results suggest that T cells change their responses in an activity-dependent manner through non-synaptic rather than synaptic plasticity. These changes might act as a gain-control mechanism. Depending on the previous activity, this gain could scale the relative impacts of synaptic inputs from other mechanoreceptors, versus the spike responses to tactile skin stimulation. This multi-tasking ability, and its flexible adaptation to previous activity, might make the T cell a key player in a preparatory network, enabling the leech to perform fast behavioral reactions to skin stimulation.

Keywords: invertebrate, mechanoreceptor, sodium potassium pump, M-type K+ current, Hodgkin Huxley model, Spike count, resting potential, input resistance

Received: 31 May 2019; Accepted: 08 Nov 2019.

Copyright: © 2019 Meiser, Ashida and Kretzberg. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Mrs. Sonja Meiser, Department of Neuroscience, School of Medicine and Health Sciences, Carl von Ossietzky University Oldenburg, Oldenburg, Germany, sonja.meiser@uni-oldenburg.de