Interactions between CNS regulation and serotonergic modulation of crayfish hindgut motility

Motility is a critical function of the gastrointestinal (GI) system governed by neurogenic and myogenic processes. Due to its major role in maintaining homeostasis, overlapping mechanisms have evolved for its adaptive operation including modulation by the central nervous system (CNS), enteric nervou...

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Main Authors: Spandan Pathak, Norma Peña-Flores, Phillip Alvarez, Jenna Feeley, Reza Ghodssi, Wolfgang Losert, Jens Herberholz
Format: Article
Language:English
Published: The Royal Society 2025-06-01
Series:Royal Society Open Science
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Online Access:https://royalsocietypublishing.org/doi/10.1098/rsos.250094
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author Spandan Pathak
Norma Peña-Flores
Phillip Alvarez
Jenna Feeley
Reza Ghodssi
Wolfgang Losert
Jens Herberholz
author_facet Spandan Pathak
Norma Peña-Flores
Phillip Alvarez
Jenna Feeley
Reza Ghodssi
Wolfgang Losert
Jens Herberholz
author_sort Spandan Pathak
collection DOAJ
description Motility is a critical function of the gastrointestinal (GI) system governed by neurogenic and myogenic processes. Due to its major role in maintaining homeostasis, overlapping mechanisms have evolved for its adaptive operation including modulation by the central nervous system (CNS), enteric nervous system (ENS) and intrinsic pacemaker cells. Our understanding of the modulatory mechanisms that underlie intestinal motility remains incomplete. Crayfish provide a tractable ex vivo model to study the interplay between CNS and neurochemical regulation of GI motor patterns. Our study investigated the effects of CNS denervation and exogenously applied serotonin (5-HT) on crayfish hindgut motility. Multiscale spatial measurements showed stable motility parameters throughout 90 min of control conditions. Denervation, i.e. separating the gut from the CNS, resulted in a significant decrease in the magnitude and synchrony of hindgut contractions, while preserving the underlying frequency and directional bias of the waves. Subsequent application of 5-HT to the denervated preparation enhanced motility but disrupted spatiotemporal coordination. Treatment with TTX (a sodium channel blocker) had minor impacts on motility metrics, indicating a prominent role of myogenic mechanisms. Our model provides a multiscale analysis framework to dissect CNS and interrelated neurochemistry contributions to GI motor dynamics.
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spelling doaj-art-0750843fb5bd4e4bb8774827826459b62025-08-20T02:40:26ZengThe Royal SocietyRoyal Society Open Science2054-57032025-06-0112610.1098/rsos.250094Interactions between CNS regulation and serotonergic modulation of crayfish hindgut motilitySpandan Pathak0Norma Peña-Flores1Phillip Alvarez2Jenna Feeley3Reza Ghodssi4Wolfgang Losert5Jens Herberholz6Institute for Physical Science and Technology, University of Maryland at College Park, College Park, MD, USANeuroscience and Cognitive Science Program, University of Maryland at College Park, College Park, MD, USAInstitute for Physical Science and Technology, University of Maryland at College Park, College Park, MD, USAInstitute for Physical Science and Technology, University of Maryland at College Park, College Park, MD, USADepartment of Electrical and Computer Engineering, University of Maryland at College Park, College Park, MD, USAInstitute for Physical Science and Technology, University of Maryland at College Park, College Park, MD, USANeuroscience and Cognitive Science Program, University of Maryland at College Park, College Park, MD, USAMotility is a critical function of the gastrointestinal (GI) system governed by neurogenic and myogenic processes. Due to its major role in maintaining homeostasis, overlapping mechanisms have evolved for its adaptive operation including modulation by the central nervous system (CNS), enteric nervous system (ENS) and intrinsic pacemaker cells. Our understanding of the modulatory mechanisms that underlie intestinal motility remains incomplete. Crayfish provide a tractable ex vivo model to study the interplay between CNS and neurochemical regulation of GI motor patterns. Our study investigated the effects of CNS denervation and exogenously applied serotonin (5-HT) on crayfish hindgut motility. Multiscale spatial measurements showed stable motility parameters throughout 90 min of control conditions. Denervation, i.e. separating the gut from the CNS, resulted in a significant decrease in the magnitude and synchrony of hindgut contractions, while preserving the underlying frequency and directional bias of the waves. Subsequent application of 5-HT to the denervated preparation enhanced motility but disrupted spatiotemporal coordination. Treatment with TTX (a sodium channel blocker) had minor impacts on motility metrics, indicating a prominent role of myogenic mechanisms. Our model provides a multiscale analysis framework to dissect CNS and interrelated neurochemistry contributions to GI motor dynamics.https://royalsocietypublishing.org/doi/10.1098/rsos.250094optical flowintestinal motilityinvertebrateserotoningut–brain axis
spellingShingle Spandan Pathak
Norma Peña-Flores
Phillip Alvarez
Jenna Feeley
Reza Ghodssi
Wolfgang Losert
Jens Herberholz
Interactions between CNS regulation and serotonergic modulation of crayfish hindgut motility
Royal Society Open Science
optical flow
intestinal motility
invertebrate
serotonin
gut–brain axis
title Interactions between CNS regulation and serotonergic modulation of crayfish hindgut motility
title_full Interactions between CNS regulation and serotonergic modulation of crayfish hindgut motility
title_fullStr Interactions between CNS regulation and serotonergic modulation of crayfish hindgut motility
title_full_unstemmed Interactions between CNS regulation and serotonergic modulation of crayfish hindgut motility
title_short Interactions between CNS regulation and serotonergic modulation of crayfish hindgut motility
title_sort interactions between cns regulation and serotonergic modulation of crayfish hindgut motility
topic optical flow
intestinal motility
invertebrate
serotonin
gut–brain axis
url https://royalsocietypublishing.org/doi/10.1098/rsos.250094
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