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Synaptic input and temperature influence sensory coding in a mechanoreceptor

Many neurons possess more than one spike initiation zone (SIZ), which adds to their computational power and functional flexibility. Integrating inputs from different origins is especially relevant for sensory neurons that rely on relative spike timing for encoding sensory information. Yet, it is poo...

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Autores principales: Scherer, Jens-Steffen, Sandbote, Kevin, Schultze, Bjarne L., Kretzberg, Jutta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10522859/
https://www.ncbi.nlm.nih.gov/pubmed/37771930
http://dx.doi.org/10.3389/fncel.2023.1233730
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author Scherer, Jens-Steffen
Sandbote, Kevin
Schultze, Bjarne L.
Kretzberg, Jutta
author_facet Scherer, Jens-Steffen
Sandbote, Kevin
Schultze, Bjarne L.
Kretzberg, Jutta
author_sort Scherer, Jens-Steffen
collection PubMed
description Many neurons possess more than one spike initiation zone (SIZ), which adds to their computational power and functional flexibility. Integrating inputs from different origins is especially relevant for sensory neurons that rely on relative spike timing for encoding sensory information. Yet, it is poorly understood if and how the propagation of spikes generated at one SIZ in response to sensory stimulation is affected by synaptic inputs triggering activity of other SIZ, and by environmental factors like temperature. The mechanosensory Touch (T) cell in the medicinal leech is an ideal model system to study these potential interactions because it allows intracellular recording and stimulation of its soma while simultaneously touching the skin in a body-wall preparation. The T cell reliably elicits spikes in response to somatic depolarization, as well as to tactile skin stimulation. Latencies of spikes elicited in the skin vary across cells, depending on the touch location relative to the cell’s receptive field. However, repetitive stimulation reveals that tactilely elicited spikes are more precisely timed than spikes triggered by somatic current injection. When the soma is hyperpolarized to mimic inhibitory synaptic input, first spike latencies of tactilely induced spikes increase. If spikes from both SIZ follow shortly after each other, the arrival time of the second spike at the soma can be delayed. Although the latency of spikes increases by the same factor when the temperature decreases, the effect is considerably stronger for the longer absolute latencies of spikes propagating from the skin to the soma. We therefore conclude that the propagation time of spikes from the skin is modulated by internal factors like synaptic inputs, and by external factors like temperature. Moreover, fewer spikes are detected when spikes from both origins are expected to arrive at the soma in temporal proximity. Hence, the leech T cell might be a key for understanding how the interaction of multiple SIZ impacts temporal and rate coding of sensory information, and how cold-blooded animals can produce adequate behavioral responses to sensory stimuli based on temperature-dependent relative spike timing.
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spelling pubmed-105228592023-09-28 Synaptic input and temperature influence sensory coding in a mechanoreceptor Scherer, Jens-Steffen Sandbote, Kevin Schultze, Bjarne L. Kretzberg, Jutta Front Cell Neurosci Cellular Neuroscience Many neurons possess more than one spike initiation zone (SIZ), which adds to their computational power and functional flexibility. Integrating inputs from different origins is especially relevant for sensory neurons that rely on relative spike timing for encoding sensory information. Yet, it is poorly understood if and how the propagation of spikes generated at one SIZ in response to sensory stimulation is affected by synaptic inputs triggering activity of other SIZ, and by environmental factors like temperature. The mechanosensory Touch (T) cell in the medicinal leech is an ideal model system to study these potential interactions because it allows intracellular recording and stimulation of its soma while simultaneously touching the skin in a body-wall preparation. The T cell reliably elicits spikes in response to somatic depolarization, as well as to tactile skin stimulation. Latencies of spikes elicited in the skin vary across cells, depending on the touch location relative to the cell’s receptive field. However, repetitive stimulation reveals that tactilely elicited spikes are more precisely timed than spikes triggered by somatic current injection. When the soma is hyperpolarized to mimic inhibitory synaptic input, first spike latencies of tactilely induced spikes increase. If spikes from both SIZ follow shortly after each other, the arrival time of the second spike at the soma can be delayed. Although the latency of spikes increases by the same factor when the temperature decreases, the effect is considerably stronger for the longer absolute latencies of spikes propagating from the skin to the soma. We therefore conclude that the propagation time of spikes from the skin is modulated by internal factors like synaptic inputs, and by external factors like temperature. Moreover, fewer spikes are detected when spikes from both origins are expected to arrive at the soma in temporal proximity. Hence, the leech T cell might be a key for understanding how the interaction of multiple SIZ impacts temporal and rate coding of sensory information, and how cold-blooded animals can produce adequate behavioral responses to sensory stimuli based on temperature-dependent relative spike timing. Frontiers Media S.A. 2023-09-12 /pmc/articles/PMC10522859/ /pubmed/37771930 http://dx.doi.org/10.3389/fncel.2023.1233730 Text en Copyright © 2023 Scherer, Sandbote, Schultze and Kretzberg. https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Cellular Neuroscience
Scherer, Jens-Steffen
Sandbote, Kevin
Schultze, Bjarne L.
Kretzberg, Jutta
Synaptic input and temperature influence sensory coding in a mechanoreceptor
title Synaptic input and temperature influence sensory coding in a mechanoreceptor
title_full Synaptic input and temperature influence sensory coding in a mechanoreceptor
title_fullStr Synaptic input and temperature influence sensory coding in a mechanoreceptor
title_full_unstemmed Synaptic input and temperature influence sensory coding in a mechanoreceptor
title_short Synaptic input and temperature influence sensory coding in a mechanoreceptor
title_sort synaptic input and temperature influence sensory coding in a mechanoreceptor
topic Cellular Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10522859/
https://www.ncbi.nlm.nih.gov/pubmed/37771930
http://dx.doi.org/10.3389/fncel.2023.1233730
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