Mohammad Jarrah, Dana Tasabehji, Aviva Fraer, Mohamad Mokadem
{"title":"Spinal afferent neurons: emerging regulators of energy balance and metabolism.","authors":"Mohammad Jarrah, Dana Tasabehji, Aviva Fraer, Mohamad Mokadem","doi":"10.3389/fnmol.2024.1479876","DOIUrl":null,"url":null,"abstract":"<p><p>Recent advancements in neurophysiology have challenged the long-held paradigm that vagal afferents serve as the primary conduits for physiological signals governing food intake and energy expenditure. An expanding body of evidence now illuminates the critical role of spinal afferent neurons in these processes, necessitating a reevaluation of our understanding of energy homeostasis regulation. This comprehensive review synthesizes cutting-edge research elucidating the multifaceted functions of spinal afferent neurons in maintaining metabolic equilibrium. Once predominantly associated with nociception and pathological states, these neurons are now recognized as integral components in the intricate network regulating feeding behavior, nutrient sensing, and energy balance. We explore the role of spinal afferents in food intake and how these neurons contribute to satiation signaling and meal termination through complex gut-brain axis pathways. The review also delves into the developing evidence that spinal afferents play a crucial role in energy expenditure regulation. We explore the ability of these neuronal fibers to carry signals that can modulate feeding behavior as well as adaptive thermogenesis in adipose tissue influencing basal metabolic rate, and thereby contributing to overall energy balance. This comprehensive analysis not only challenges existing paradigms but also opens new avenues for therapeutic interventions suggesting potential targets for treating metabolic disorders. In conclusion, this review highlights the need for a shift in our understanding of energy homeostasis, positioning spinal afferent neurons as key players in the intricate web of metabolic regulation.</p>","PeriodicalId":12630,"journal":{"name":"Frontiers in Molecular Neuroscience","volume":"17 ","pages":"1479876"},"PeriodicalIF":3.5000,"publicationDate":"2024-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11583444/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Molecular Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3389/fnmol.2024.1479876","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Recent advancements in neurophysiology have challenged the long-held paradigm that vagal afferents serve as the primary conduits for physiological signals governing food intake and energy expenditure. An expanding body of evidence now illuminates the critical role of spinal afferent neurons in these processes, necessitating a reevaluation of our understanding of energy homeostasis regulation. This comprehensive review synthesizes cutting-edge research elucidating the multifaceted functions of spinal afferent neurons in maintaining metabolic equilibrium. Once predominantly associated with nociception and pathological states, these neurons are now recognized as integral components in the intricate network regulating feeding behavior, nutrient sensing, and energy balance. We explore the role of spinal afferents in food intake and how these neurons contribute to satiation signaling and meal termination through complex gut-brain axis pathways. The review also delves into the developing evidence that spinal afferents play a crucial role in energy expenditure regulation. We explore the ability of these neuronal fibers to carry signals that can modulate feeding behavior as well as adaptive thermogenesis in adipose tissue influencing basal metabolic rate, and thereby contributing to overall energy balance. This comprehensive analysis not only challenges existing paradigms but also opens new avenues for therapeutic interventions suggesting potential targets for treating metabolic disorders. In conclusion, this review highlights the need for a shift in our understanding of energy homeostasis, positioning spinal afferent neurons as key players in the intricate web of metabolic regulation.
期刊介绍:
Frontiers in Molecular Neuroscience is a first-tier electronic journal devoted to identifying key molecules, as well as their functions and interactions, that underlie the structure, design and function of the brain across all levels. The scope of our journal encompasses synaptic and cellular proteins, coding and non-coding RNA, and molecular mechanisms regulating cellular and dendritic RNA translation. In recent years, a plethora of new cellular and synaptic players have been identified from reduced systems, such as neuronal cultures, but the relevance of these molecules in terms of cellular and synaptic function and plasticity in the living brain and its circuits has not been validated. The effects of spine growth and density observed using gene products identified from in vitro work are frequently not reproduced in vivo. Our journal is particularly interested in studies on genetically engineered model organisms (C. elegans, Drosophila, mouse), in which alterations in key molecules underlying cellular and synaptic function and plasticity produce defined anatomical, physiological and behavioral changes. In the mouse, genetic alterations limited to particular neural circuits (olfactory bulb, motor cortex, cortical layers, hippocampal subfields, cerebellum), preferably regulated in time and on demand, are of special interest, as they sidestep potential compensatory developmental effects.