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.
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.