Impact of cell-intrinsic plasticity on the neuronal control of behavior
Experimental and Theoretical Network Neuroscience
Final Report Abstract
The medicinal leech performs a strikingly precise avoidance behavior in response to touch. The sensitive tactile perception is based on mechanoreceptors that strongly resemble those of mammals. Like primate FA-I fibers, leech T (touch) cells signal changes in touch stimulation with precisely timed transient spike responses. In addition to these spikes elicited in the skin, synaptic inputs also trigger T cell spikes within the ganglion. This raises the question of how sensory and synaptic inputs interact in sensory coding. Our project built upon the previous finding that T cells respond to repeated somatic current injection with membrane potential hyperpolarization and increased spiking excitability. The preceding study proposed an activity-dependent mechanism of cell-intrinsic plasticity based on the interaction of Na+/K+-pump activity and slow K+ channels. To test this hypothesis, we conducted a control experiment, which demonstrated that the excitability of T cells also increases during recording periods in the absence of electrical stimulation. This finding suggests that the underlying mechanism is time-dependent rather than activity-dependent, and that experimental conditions may also contribute. However, even the initial excitability of T cells was found to be uniquely variable compared to other leech neurons. A combination of electrophysiology and anatomically detailed multi-compartment modeling revealed that three factors contribute to the observed highly variable excitability: (1) time-dependent changes in excitability, (2) synaptic input from the network, and (3) anatomical differences. However, none of these factors fully accounted for the systematic differences in excitability of T cells at two distinct sites in the ganglion, suggesting the interaction of multiple factors. Since we found considerable mutual interaction of T cells with the network via chemical and electrical synapses, we investigated the influence of synaptic network input on temporal encoding of sensory information. These experiments combined tactile stimulation, which triggered precisely timed spikes in the skin, with electrical stimulation of the soma, mimicking synaptic input. Hyperpolarization as well as spikes elicited by positive current pulses (resembling excitatory inputs) increased the propagation time of a subsequent spike from the skin to the T cell soma. Additionally, the propagation times and interaction of spikes from both initiation sites were influenced by temperature. This finding raises the question of how poikilothermic animals sense their environment based on a temporal code. In conclusion, this project shifted the perspective on the processing of behaviorally relevant sensory information. Our findings indicate that individual anatomical features and variable mutual network interactions play a more significant role in sensory coding than cell-intrinsic plasticity.
Publications
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Initial Variability and Time-Dependent Changes of Neuronal Response Features Are Cell-Type-Specific. Frontiers in Cellular Neuroscience, 16.
Scherer, Jens-Steffen; Riedesel, Oda E.; Arkhypchuk, Ihor; Meiser, Sonja & Kretzberg, Jutta
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Interaction of two spike initiation zones in a leech mechanoreceptor. Bernstein Conference 2022
Sandbote K., Scherer J., Ashida G. & Kretzberg J.
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Position dependent differences in response features of individual cells within the same type – intracellular double recordings of mechanosensory T cells of the leech. FENS Forum 2022
Sleeboom J.M., Meiser S. & Kretzberg J.
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The sound of silence – electrophysiological comparison of three cell types. FENS Forum 2022
Riedesel O., Scherer J.S., Meiser S. & Kretzberg J.
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Variability and diversity of sensory Touch cells and interneurons in the leech. Bernstein Conference 2022
Arkhypchuk I. & Kretzberg J.
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Anatomical variability explains neuronal response variability of leech T cells, but anatomical subtypes cannot explain systematically different responses. Bernstein Conference 2023
Sandbote K., Arkhypchuk I., Stalf K. & Kretzberg J.
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Cell anatomy and network input explain differences within but not between leech touch cells at two different locations. Frontiers in Cellular Neuroscience, 17.
Meiser, Sonja; Sleeboom, Jana Marie; Arkhypchuk, Ihor; Sandbote, Kevin & Kretzberg, Jutta
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Synaptic input and temperature influence sensory coding in a mechanoreceptor. Frontiers in Cellular Neuroscience, 17.
Scherer, Jens-Steffen; Sandbote, Kevin; Schultze, Bjarne L. & Kretzberg, Jutta
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Temperature effects on spike counts and spike timing in a mechanoreceptor of a poikilothermic animal. Bernstein Conference 2023
Schultze B.L., Sandbote K., Scherer J. & Kretzberg J.
