The Complement of Projection Neurons Activated Determines the Type of Feeding Motor Program in Aplysia

Multiple projection neurons are often activated to initiate behavior. A question that then arises is, what is the unique functional role of each neuron activated? We address this issue in the feeding system of Aplysia. Previous experiments identified a projection neuron [cerebral buccal interneuron...

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Main Authors: Colin G. Evans, Michael A. Barry, Jian Jing, Matthew H. Perkins, Klaudiusz R. Weiss, Elizabeth C. Cropper
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncir.2021.685222/full
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author Colin G. Evans
Michael A. Barry
Jian Jing
Jian Jing
Matthew H. Perkins
Klaudiusz R. Weiss
Elizabeth C. Cropper
author_facet Colin G. Evans
Michael A. Barry
Jian Jing
Jian Jing
Matthew H. Perkins
Klaudiusz R. Weiss
Elizabeth C. Cropper
author_sort Colin G. Evans
collection DOAJ
description Multiple projection neurons are often activated to initiate behavior. A question that then arises is, what is the unique functional role of each neuron activated? We address this issue in the feeding system of Aplysia. Previous experiments identified a projection neuron [cerebral buccal interneuron 2 (CBI-2)] that can trigger ingestive motor programs but only after it is repeatedly stimulated, i.e., initial programs are poorly defined. As CBI-2 stimulation continues, programs become progressively more ingestive (repetition priming occurs). This priming results, at least in part, from persistent actions of peptide cotransmitters released from CBI-2. We now show that in some preparations repetition priming does not occur. There is no clear seasonal effect; priming and non-priming preparations are encountered throughout the year. CBI-2 is electrically coupled to a second projection neuron, cerebral buccal interneuron 3 (CBI-3). In preparations in which priming does not occur, we show that ingestive activity is generated when CBI-2 and CBI-3 are coactivated. Programs are immediately ingestive, i.e., priming is not necessary, and a persistent state is not induced. Our data suggest that dynamic changes in the configuration of activity can vary and be determined by the complement of projection neurons that trigger activity.
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spelling doaj.art-798ac011388b4f538c4219413f29c45e2022-12-21T22:01:50ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102021-06-011510.3389/fncir.2021.685222685222The Complement of Projection Neurons Activated Determines the Type of Feeding Motor Program in AplysiaColin G. Evans0Michael A. Barry1Jian Jing2Jian Jing3Matthew H. Perkins4Klaudiusz R. Weiss5Elizabeth C. Cropper6Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesState Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Collaborative Innovation Center of Chemistry for Life Sciences, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, School of Life Sciences, Nanjing University, Nanjing, ChinaDepartment of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesMultiple projection neurons are often activated to initiate behavior. A question that then arises is, what is the unique functional role of each neuron activated? We address this issue in the feeding system of Aplysia. Previous experiments identified a projection neuron [cerebral buccal interneuron 2 (CBI-2)] that can trigger ingestive motor programs but only after it is repeatedly stimulated, i.e., initial programs are poorly defined. As CBI-2 stimulation continues, programs become progressively more ingestive (repetition priming occurs). This priming results, at least in part, from persistent actions of peptide cotransmitters released from CBI-2. We now show that in some preparations repetition priming does not occur. There is no clear seasonal effect; priming and non-priming preparations are encountered throughout the year. CBI-2 is electrically coupled to a second projection neuron, cerebral buccal interneuron 3 (CBI-3). In preparations in which priming does not occur, we show that ingestive activity is generated when CBI-2 and CBI-3 are coactivated. Programs are immediately ingestive, i.e., priming is not necessary, and a persistent state is not induced. Our data suggest that dynamic changes in the configuration of activity can vary and be determined by the complement of projection neurons that trigger activity.https://www.frontiersin.org/articles/10.3389/fncir.2021.685222/fullmolluscfeedingAplysiacentral pattern generatorscommand neuron
spellingShingle Colin G. Evans
Michael A. Barry
Jian Jing
Jian Jing
Matthew H. Perkins
Klaudiusz R. Weiss
Elizabeth C. Cropper
The Complement of Projection Neurons Activated Determines the Type of Feeding Motor Program in Aplysia
Frontiers in Neural Circuits
mollusc
feeding
Aplysia
central pattern generators
command neuron
title The Complement of Projection Neurons Activated Determines the Type of Feeding Motor Program in Aplysia
title_full The Complement of Projection Neurons Activated Determines the Type of Feeding Motor Program in Aplysia
title_fullStr The Complement of Projection Neurons Activated Determines the Type of Feeding Motor Program in Aplysia
title_full_unstemmed The Complement of Projection Neurons Activated Determines the Type of Feeding Motor Program in Aplysia
title_short The Complement of Projection Neurons Activated Determines the Type of Feeding Motor Program in Aplysia
title_sort complement of projection neurons activated determines the type of feeding motor program in aplysia
topic mollusc
feeding
Aplysia
central pattern generators
command neuron
url https://www.frontiersin.org/articles/10.3389/fncir.2021.685222/full
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