Increased Na+/K+ pump activity induces non-synaptic plasticity in leech sensory neurons

Sonja Meiser¹, Go Ashida², Kevin Sandbote¹, Jens-Steffen Scherer¹, Jutta Kretzberg²

¹ Computational Neuroscience, Department of Neuroscience, Faculty VI, Carl von Ossietzky University of Oldenburg, Oldenburg, Germany
² Computational Neuroscience, Department of Neuroscience, Faculty VI, Carl von Ossietzky University of Oldenburg, Oldenburg, Germany & Cluster of Excellence Hearing4all, Carl von Ossietzky University of Oldenburg, Oldenburg, Germany

Touch mechanoreceptors (T cells) of the leech respond transiently to tactile skin stimulation and employ several mechanisms of plasticity. Recently, we demonstrated that repeated somatic current stimulation leads to a resting membrane potential (RMP) hyperpolarization of T cells while their spike count (SC) and input resistance (IR) increase. Our results suggest that augmented Na⁺/K⁺-pump activity due to repeated discharges of somatic action potential initiates this activity-dependent, non-synaptic plasticity (Meiser et al. 2019). Our model also predicted that the observed SC increase is caused by a slow, non-inactivating outward current that decreases with RMP hyperpolarization. This current is presumably mediated by voltage-dependent, low-threshold M-type K⁺ channels. Here, we tested these predictions. Blocking Na⁺/K⁺-pump with Ouabain leads to a slow depolarization of the membrane potential. In agreement with the model predictions, depolarization induced by blocking the Na⁺/K⁺-pump decreases SC and IR, as would be expected for a higher percentage of open M-type K⁺ channels. Further evidence that supports this is that M-type K+ channels are blocked with XE-991 Moreover, according to Kretzberg et al. (2007) and Burgin & Szczupak (2003), T cells have at least two distinct spike initiation zones. In the skin, spikes are elicited by tactile stimuli, and in the central ganglion by synaptic inputs. Our preliminary results demonstrate that the SC decreases with repeated tactile stimulation. This is in contrast to the increased activity observed in repeated somatic current stimulation. This system allows us to analyse the interaction of opponent effects of non-synaptic plasticity at two spike initiation sites.