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Higher Network Activity Induced by Tactile Compared to Electrical Stimulation of Leech Mechanoreceptors

The tiny ensemble of neurons in the leech ganglion can discriminate the locations of touch stimuli on the skin as precisely as a human fingertip. The leech uses this ability to locally bend the body-wall away from the stimulus. It is assumed that a three-layered feedforward network of pressure mecha...

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Autores principales: Fathiazar, Elham, Hilgen, Gerrit, Kretzberg, Jutta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5845893/
https://www.ncbi.nlm.nih.gov/pubmed/29563881
http://dx.doi.org/10.3389/fphys.2018.00173
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author Fathiazar, Elham
Hilgen, Gerrit
Kretzberg, Jutta
author_facet Fathiazar, Elham
Hilgen, Gerrit
Kretzberg, Jutta
author_sort Fathiazar, Elham
collection PubMed
description The tiny ensemble of neurons in the leech ganglion can discriminate the locations of touch stimuli on the skin as precisely as a human fingertip. The leech uses this ability to locally bend the body-wall away from the stimulus. It is assumed that a three-layered feedforward network of pressure mechanoreceptors, interneurons, and motor neurons controls this behavior. Most previous studies identified and characterized the local bend network based on electrical stimulation of a single pressure mechanoreceptor, which was sufficient to trigger the local bend response. Recent studies showed, however, that up to six mechanoreceptors of three types innervating the stimulated patch of skin carry information about both touch intensity and location simultaneously. Therefore, we hypothesized that interneurons involved in the local bend network might require the temporally concerted inputs from the population of mechanoreceptors representing tactile stimuli, to decode the tactile information and to provide appropriate synaptic inputs to the motor neurons. We examined the influence of current injection into a single mechanoreceptor on activity of postsynaptic interneurons in the network and compared it to responses of interneurons to skin stimulation with different pressure intensities. We used voltage-sensitive dye imaging to monitor the graded membrane potential changes of all visible cells on the ventral side of the ganglion. Our results showed that stimulation of a single mechanoreceptor activates several local bend interneurons, consistent with previous intracellular studies. Tactile skin stimulation, however, evoked a more pronounced, longer-lasting, stimulus intensity-dependent network dynamics involving more interneurons. We concluded that the underlying local bend network enables a non-linear processing of tactile information provided by population of mechanoreceptors. This task requires a more complex network structure than previously assumed, probably containing polysynaptic interneuron connections and feedback loops. This small, experimentally well-accessible neuronal system highlights the general importance of selecting adequate sensory stimulation to investigate the network dynamics in the context of natural behavior.
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spelling pubmed-58458932018-03-21 Higher Network Activity Induced by Tactile Compared to Electrical Stimulation of Leech Mechanoreceptors Fathiazar, Elham Hilgen, Gerrit Kretzberg, Jutta Front Physiol Physiology The tiny ensemble of neurons in the leech ganglion can discriminate the locations of touch stimuli on the skin as precisely as a human fingertip. The leech uses this ability to locally bend the body-wall away from the stimulus. It is assumed that a three-layered feedforward network of pressure mechanoreceptors, interneurons, and motor neurons controls this behavior. Most previous studies identified and characterized the local bend network based on electrical stimulation of a single pressure mechanoreceptor, which was sufficient to trigger the local bend response. Recent studies showed, however, that up to six mechanoreceptors of three types innervating the stimulated patch of skin carry information about both touch intensity and location simultaneously. Therefore, we hypothesized that interneurons involved in the local bend network might require the temporally concerted inputs from the population of mechanoreceptors representing tactile stimuli, to decode the tactile information and to provide appropriate synaptic inputs to the motor neurons. We examined the influence of current injection into a single mechanoreceptor on activity of postsynaptic interneurons in the network and compared it to responses of interneurons to skin stimulation with different pressure intensities. We used voltage-sensitive dye imaging to monitor the graded membrane potential changes of all visible cells on the ventral side of the ganglion. Our results showed that stimulation of a single mechanoreceptor activates several local bend interneurons, consistent with previous intracellular studies. Tactile skin stimulation, however, evoked a more pronounced, longer-lasting, stimulus intensity-dependent network dynamics involving more interneurons. We concluded that the underlying local bend network enables a non-linear processing of tactile information provided by population of mechanoreceptors. This task requires a more complex network structure than previously assumed, probably containing polysynaptic interneuron connections and feedback loops. This small, experimentally well-accessible neuronal system highlights the general importance of selecting adequate sensory stimulation to investigate the network dynamics in the context of natural behavior. Frontiers Media S.A. 2018-03-07 /pmc/articles/PMC5845893/ /pubmed/29563881 http://dx.doi.org/10.3389/fphys.2018.00173 Text en Copyright © 2018 Fathiazar, Hilgen and Kretzberg. http://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 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 Physiology
Fathiazar, Elham
Hilgen, Gerrit
Kretzberg, Jutta
Higher Network Activity Induced by Tactile Compared to Electrical Stimulation of Leech Mechanoreceptors
title Higher Network Activity Induced by Tactile Compared to Electrical Stimulation of Leech Mechanoreceptors
title_full Higher Network Activity Induced by Tactile Compared to Electrical Stimulation of Leech Mechanoreceptors
title_fullStr Higher Network Activity Induced by Tactile Compared to Electrical Stimulation of Leech Mechanoreceptors
title_full_unstemmed Higher Network Activity Induced by Tactile Compared to Electrical Stimulation of Leech Mechanoreceptors
title_short Higher Network Activity Induced by Tactile Compared to Electrical Stimulation of Leech Mechanoreceptors
title_sort higher network activity induced by tactile compared to electrical stimulation of leech mechanoreceptors
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5845893/
https://www.ncbi.nlm.nih.gov/pubmed/29563881
http://dx.doi.org/10.3389/fphys.2018.00173
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