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Somatovisceral Convergence in Sleep-Wake Cycle: Transmitting Different Types of Information via the Same Pathway
Convergence of somatic and visceral inputs occurs at the levels of nervous system ranging from spinal cord to cerebral cortex. This anatomical organization gave explanation to a referred pain phenomenon. However, it also presents a problem: How does the brain know what information is coming for proc...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10013007/ https://www.ncbi.nlm.nih.gov/pubmed/36926092 http://dx.doi.org/10.3389/fnetp.2022.840565 |
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author | Levichkina, Ekaterina Pigareva, Marina L. Limanskaya, Alexandra Pigarev, Ivan N. |
author_facet | Levichkina, Ekaterina Pigareva, Marina L. Limanskaya, Alexandra Pigarev, Ivan N. |
author_sort | Levichkina, Ekaterina |
collection | PubMed |
description | Convergence of somatic and visceral inputs occurs at the levels of nervous system ranging from spinal cord to cerebral cortex. This anatomical organization gave explanation to a referred pain phenomenon. However, it also presents a problem: How does the brain know what information is coming for processing—somatic or visceral - if both are transferred by the same spinal cord fibers by means of the standard neuronal spikes? Recent studies provided evidence for cortical processing of interoceptive information largely occurring in sleep, when somatosensation is suppressed, and for the corresponding functional brain networks rearrangement. We suggest that convergent units of the spinal cord would be able to collectively provide mainly somatosensory information in wakefulness and mainly visceral in sleep, solving the puzzle of somatovisceral convergence. We recorded spiking activity from the spinal cord lemniscus pathway during multiple sleep-wake cycles in freely behaving rabbits. In wakefulness high increased spiking corresponded to movements. When animals stopped moving this activity ceased, the fibers remained silent during passive wakefulness. However, upon transition to sleep fibers began firing again. Analysis of spiking patterns of individual fibers revealed that in the majority of them spiking rates recovered in slow wave sleep. Thus, despite cessation of motion and a corresponding decrease of somatic component of the convergent signal, considerable ascending signaling occurs during sleep, that is likely to be visceral. We also recorded evoked responses of the lemniscus pathway to innocuous electrostimulation of the abdominal viscera, and uncovered the existence of two groups of responses depending upon the state of vigilance. Response from an individual fiber could be detected either during wakefulness or in sleep, but not in both states. Wakefulness-responsive group had lower spiking rates in wakefulness and almost stopped spiking in sleep. Sleep-responsive retained substantial spiking during sleep. These groups also differed in spike amplitudes, indicative of fiber diameter differences; however, both had somatic responses during wakefulness. We suggest a mechanism that utilizes differences in somatic and visceral activities to extract both types of information by varying transmission thresholds, and discuss the implications of this mechanism on functional networks under normal and pathological conditions. |
format | Online Article Text |
id | pubmed-10013007 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-100130072023-03-15 Somatovisceral Convergence in Sleep-Wake Cycle: Transmitting Different Types of Information via the Same Pathway Levichkina, Ekaterina Pigareva, Marina L. Limanskaya, Alexandra Pigarev, Ivan N. Front Netw Physiol Network Physiology Convergence of somatic and visceral inputs occurs at the levels of nervous system ranging from spinal cord to cerebral cortex. This anatomical organization gave explanation to a referred pain phenomenon. However, it also presents a problem: How does the brain know what information is coming for processing—somatic or visceral - if both are transferred by the same spinal cord fibers by means of the standard neuronal spikes? Recent studies provided evidence for cortical processing of interoceptive information largely occurring in sleep, when somatosensation is suppressed, and for the corresponding functional brain networks rearrangement. We suggest that convergent units of the spinal cord would be able to collectively provide mainly somatosensory information in wakefulness and mainly visceral in sleep, solving the puzzle of somatovisceral convergence. We recorded spiking activity from the spinal cord lemniscus pathway during multiple sleep-wake cycles in freely behaving rabbits. In wakefulness high increased spiking corresponded to movements. When animals stopped moving this activity ceased, the fibers remained silent during passive wakefulness. However, upon transition to sleep fibers began firing again. Analysis of spiking patterns of individual fibers revealed that in the majority of them spiking rates recovered in slow wave sleep. Thus, despite cessation of motion and a corresponding decrease of somatic component of the convergent signal, considerable ascending signaling occurs during sleep, that is likely to be visceral. We also recorded evoked responses of the lemniscus pathway to innocuous electrostimulation of the abdominal viscera, and uncovered the existence of two groups of responses depending upon the state of vigilance. Response from an individual fiber could be detected either during wakefulness or in sleep, but not in both states. Wakefulness-responsive group had lower spiking rates in wakefulness and almost stopped spiking in sleep. Sleep-responsive retained substantial spiking during sleep. These groups also differed in spike amplitudes, indicative of fiber diameter differences; however, both had somatic responses during wakefulness. We suggest a mechanism that utilizes differences in somatic and visceral activities to extract both types of information by varying transmission thresholds, and discuss the implications of this mechanism on functional networks under normal and pathological conditions. Frontiers Media S.A. 2022-03-02 /pmc/articles/PMC10013007/ /pubmed/36926092 http://dx.doi.org/10.3389/fnetp.2022.840565 Text en Copyright © 2022 Levichkina, Pigareva, Limanskaya and Pigarev. 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 | Network Physiology Levichkina, Ekaterina Pigareva, Marina L. Limanskaya, Alexandra Pigarev, Ivan N. Somatovisceral Convergence in Sleep-Wake Cycle: Transmitting Different Types of Information via the Same Pathway |
title | Somatovisceral Convergence in Sleep-Wake Cycle: Transmitting Different Types of Information via the Same Pathway |
title_full | Somatovisceral Convergence in Sleep-Wake Cycle: Transmitting Different Types of Information via the Same Pathway |
title_fullStr | Somatovisceral Convergence in Sleep-Wake Cycle: Transmitting Different Types of Information via the Same Pathway |
title_full_unstemmed | Somatovisceral Convergence in Sleep-Wake Cycle: Transmitting Different Types of Information via the Same Pathway |
title_short | Somatovisceral Convergence in Sleep-Wake Cycle: Transmitting Different Types of Information via the Same Pathway |
title_sort | somatovisceral convergence in sleep-wake cycle: transmitting different types of information via the same pathway |
topic | Network Physiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10013007/ https://www.ncbi.nlm.nih.gov/pubmed/36926092 http://dx.doi.org/10.3389/fnetp.2022.840565 |
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