Identified neurons B4/B5 function as sensory neurons, motor neurons, and interneurons in Aplysia.

IF 2.1 3区 医学 Q3 NEUROSCIENCES
Journal of neurophysiology Pub Date : 2025-05-01 Epub Date: 2025-03-26 DOI:10.1152/jn.00630.2024
Yu Huan, Eileen E Faulk, Jeffrey P Gill, Hillel J Chiel
{"title":"Identified neurons B4/B5 function as sensory neurons, motor neurons, and interneurons in <i>Aplysia</i>.","authors":"Yu Huan, Eileen E Faulk, Jeffrey P Gill, Hillel J Chiel","doi":"10.1152/jn.00630.2024","DOIUrl":null,"url":null,"abstract":"<p><p>Adaptive behavior is critical for animals' survival. A multifunctional nervous system is crucial to generate behaviors that respond effectively to the changing environment. Multiple mechanisms behind a multifunctional neural circuit have been found in vertebrate and invertebrate systems: the change in the nervous system can occur at the cellular level, the synaptic level and at the circuitry level. <i>Aplysia</i>'s feeding circuit is a multifunctional system capable of producing different modes of behavior. In <i>Aplysia</i>, B4/B5 are two electrically coupled multiaction neurons that have wide inhibitory synaptic outputs to multiple key motor neurons, mediating an important component of rejection behavior. However, B4/B5 also fire at a lower frequency during ingestion, generating a limited inhibitory effect on their synaptic followers. To further understand the role of B4/B5 in different behaviors, we investigated the functions of B4/B5 and their firing patterns in freely feeding animals. As previous studies suggested that B4/B5 have sensory and motor functions, we further characterized the sensory response and the motor effect of B4/B5 and related these functions to different behaviors. We found that B4/B5 receive direct sensory inputs from different receptive fields within the feeding apparatus, and they innervate and alter forces in the retractor muscles and reduce forces induced by a motor neuron (B3) for the retractor muscles. Their sensory signaling may be related to contact with food during ingestion. Studies on the B4/B5 neurons demonstrated how a neural circuit can be influenced by multifunctional neurons, suggesting another way that adaptive behaviors can be generated.<b>NEW & NOTEWORTHY</b> The B4/B5 neurons in <i>Aplysia californica</i> have multiple functions. In this study, we further characterized B4/B5's sensory responses to mechanical stimuli at different locations in the feeding apparatus and identified their direct motor effect on the muscles. The bidirectional signaling of B4/B5, which was also observed in freely feeding animals, suggests that these neurons may play a role in detecting nociceptive or proprioceptive information and regulating the movements that facilitate particular feeding behaviors.</p>","PeriodicalId":16563,"journal":{"name":"Journal of neurophysiology","volume":" ","pages":"1435-1455"},"PeriodicalIF":2.1000,"publicationDate":"2025-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of neurophysiology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1152/jn.00630.2024","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/3/26 0:00:00","PubModel":"Epub","JCR":"Q3","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Adaptive behavior is critical for animals' survival. A multifunctional nervous system is crucial to generate behaviors that respond effectively to the changing environment. Multiple mechanisms behind a multifunctional neural circuit have been found in vertebrate and invertebrate systems: the change in the nervous system can occur at the cellular level, the synaptic level and at the circuitry level. Aplysia's feeding circuit is a multifunctional system capable of producing different modes of behavior. In Aplysia, B4/B5 are two electrically coupled multiaction neurons that have wide inhibitory synaptic outputs to multiple key motor neurons, mediating an important component of rejection behavior. However, B4/B5 also fire at a lower frequency during ingestion, generating a limited inhibitory effect on their synaptic followers. To further understand the role of B4/B5 in different behaviors, we investigated the functions of B4/B5 and their firing patterns in freely feeding animals. As previous studies suggested that B4/B5 have sensory and motor functions, we further characterized the sensory response and the motor effect of B4/B5 and related these functions to different behaviors. We found that B4/B5 receive direct sensory inputs from different receptive fields within the feeding apparatus, and they innervate and alter forces in the retractor muscles and reduce forces induced by a motor neuron (B3) for the retractor muscles. Their sensory signaling may be related to contact with food during ingestion. Studies on the B4/B5 neurons demonstrated how a neural circuit can be influenced by multifunctional neurons, suggesting another way that adaptive behaviors can be generated.NEW & NOTEWORTHY The B4/B5 neurons in Aplysia californica have multiple functions. In this study, we further characterized B4/B5's sensory responses to mechanical stimuli at different locations in the feeding apparatus and identified their direct motor effect on the muscles. The bidirectional signaling of B4/B5, which was also observed in freely feeding animals, suggests that these neurons may play a role in detecting nociceptive or proprioceptive information and regulating the movements that facilitate particular feeding behaviors.

已鉴定的神经元B4/B5分别具有感觉神经元、运动神经元和中间神经元的功能。
适应性行为对动物的生存至关重要。一个多功能的神经系统对于产生对不断变化的环境做出有效反应的行为至关重要。在脊椎动物和无脊椎动物系统中,多功能神经回路背后的多种机制已经被发现:神经系统的变化可以发生在细胞水平、突触水平以及回路水平。海鬣蜥的进食回路是一个多功能系统,能够产生不同的行为模式。在澳大利亚,B4/B5是两个电偶联的多作用神经元,它们对多个关键运动神经元有广泛的抑制性突触输出,介导排斥行为的一个重要组成部分。然而,B4/B5在摄入过程中也以较低的频率放电,对其突触跟随者产生有限的抑制作用。为了进一步了解B4/B5在不同行为中的作用,我们研究了自由饲养动物B4/B5的功能及其放电模式。鉴于已有研究表明B4/B5具有感觉和运动功能,我们进一步研究了B4/B5的感觉反应和运动效应,并将这些功能与不同行为联系起来。我们发现B4/B5接收来自进食装置内不同感受野的直接感觉输入,它们支配和改变牵牵肌的力,并减少牵牵肌运动神经元(B3)诱导的力。它们的感觉信号可能与进食过程中与食物接触有关。对B4/B5神经元的研究表明,神经回路可以受到多功能神经元的影响,这表明适应性行为可以产生的另一种方式。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Journal of neurophysiology
Journal of neurophysiology 医学-神经科学
CiteScore
4.80
自引率
8.00%
发文量
255
审稿时长
2-3 weeks
期刊介绍: The Journal of Neurophysiology publishes original articles on the function of the nervous system. All levels of function are included, from the membrane and cell to systems and behavior. Experimental approaches include molecular neurobiology, cell culture and slice preparations, membrane physiology, developmental neurobiology, functional neuroanatomy, neurochemistry, neuropharmacology, systems electrophysiology, imaging and mapping techniques, and behavioral analysis. Experimental preparations may be invertebrate or vertebrate species, including humans. Theoretical studies are acceptable if they are tied closely to the interpretation of experimental data and elucidate principles of broad interest.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信