Non-synaptic Plasticity in Leech Touch Cells.

Sonja Meiser,Go Ashida,Jutta Kretzberg

doi:10.3389/fphys.2019.01444

Sonja Meiser, Go Ashida + Show 1 more

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https://doi.org/10.3389/fphys.2019.01444

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Abstract

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 (RMP) of T cells hyperpolarizes in response to repeated somatic current injection, while at the same time their spike count (SC) and the input resistance (IR) 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 RMP. 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 IR 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 SC in the presynaptic T cell results in larger postsynaptic responses (PRs) in the other T cells. However, when the number of elicited presynaptic spikes is kept constant, the PR 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.

Highlights

Understanding the mechanisms of how sensory information elicits behavioral reactions is a major goal in neuroscience
Responses were analyzed for changes in the physiological properties spike count (SC), resting membrane potential (RMP), and cell input resistance (IR)
As can be seen in the representative intracellular response traces (Figures 2A,B), repeated current injection caused an increase in SC and in IR, while the RMP hyperpolarized

Summary

Introduction

Understanding the mechanisms of how sensory information elicits behavioral reactions is a major goal in neuroscience. The sensory input layer consists of three different types of leech mechanosensory cells [touch (T), pressure (P), and nociceptive (N) cells], which share several fundamental properties with the human tactile receptors (Baca et al, 2005; Smith and Lewin, 2009; Pirschel and Kretzberg, 2016). Studies focused mostly on P cells, because stimulation of a single P cell is sufficient to elicit muscle movements for several behavioral responses, like swimming or local bending (Kristan, 1982; Kristan et al, 1982). Pirschel and Kretzberg (2016) suggested that T cells might play a substantial role in the local bend response, making in-depth investigations on these sensory neurons necessary

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