Audrey N Nash, Morgan Shakeshaft, Cecilia G Bouaichi, Katherine E Odegaard, Tom Needham, Martin Bauer, Richard Bertram, Roberto Vincis
{"title":"活跃舔食小鼠的味觉和热信号的皮质编码。","authors":"Audrey N Nash, Morgan Shakeshaft, Cecilia G Bouaichi, Katherine E Odegaard, Tom Needham, Martin Bauer, Richard Bertram, Roberto Vincis","doi":"10.1113/JP287499","DOIUrl":null,"url":null,"abstract":"<p><p>Eating behaviours are influenced by the integration of gustatory, olfactory and somatosensory signals, which all contribute to the perception of flavour. Although extensive research has explored the neural correlates of taste in the gustatory cortex (GC), less is known about its role in encoding thermal information. This study investigates the encoding of oral thermal and chemosensory signals by GC neurons compared to the oral somatosensory cortex. In this study we recorded the spiking activity of more than 900 GC neurons and 500 neurons from the oral somatosensory cortex in mice allowed to freely lick small drops of gustatory stimuli or deionized water at varying non-nociceptive temperatures. We then developed and used a Bayesian-based analysis technique to assess neural classification scores based on spike rate and phase timing within the lick cycle. Our results indicate that GC neurons rely predominantly on rate information, although phase information is needed to achieve maximum accuracy, to effectively encode both chemosensory and thermosensory signals. GC neurons can effectively differentiate between thermal stimuli, excelling in distinguishing both large contrasts (14 vs. 36°C) and, although less effectively, more subtle temperature differences. Finally a direct comparison of the decoding accuracy of thermosensory signals between the two cortices reveals that whereas the somatosensory cortex exhibited higher overall accuracy, the GC still encodes significant thermosensory information. These findings highlight the GC's dual role in processing taste and temperature, emphasizing the importance of considering temperature in future studies of taste processing. KEY POINTS: Flavour perception relies on gustatory, olfactory and somatosensory integration, with the gustatory cortex (GC) central to taste processing. GC neurons also respond to temperature, but the specifics of how the GC processes taste and oral thermal stimuli remain unclear. The focus of this study is on the role of GC neurons in the encoding of oral thermal information, particularly compared to the coding functions of the oral somatosensory cortex. We found that whereas the somatosensory cortex shows a higher classification accuracy for distinguishing water temperature, the GC still encodes a substantial amount of thermosensory information. These results emphasize the importance of including temperature as a key factor in future studies of cortical taste coding.</p>","PeriodicalId":50088,"journal":{"name":"Journal of Physiology-London","volume":" ","pages":""},"PeriodicalIF":4.7000,"publicationDate":"2025-01-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Cortical coding of gustatory and thermal signals in active licking mice.\",\"authors\":\"Audrey N Nash, Morgan Shakeshaft, Cecilia G Bouaichi, Katherine E Odegaard, Tom Needham, Martin Bauer, Richard Bertram, Roberto Vincis\",\"doi\":\"10.1113/JP287499\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Eating behaviours are influenced by the integration of gustatory, olfactory and somatosensory signals, which all contribute to the perception of flavour. Although extensive research has explored the neural correlates of taste in the gustatory cortex (GC), less is known about its role in encoding thermal information. This study investigates the encoding of oral thermal and chemosensory signals by GC neurons compared to the oral somatosensory cortex. In this study we recorded the spiking activity of more than 900 GC neurons and 500 neurons from the oral somatosensory cortex in mice allowed to freely lick small drops of gustatory stimuli or deionized water at varying non-nociceptive temperatures. We then developed and used a Bayesian-based analysis technique to assess neural classification scores based on spike rate and phase timing within the lick cycle. Our results indicate that GC neurons rely predominantly on rate information, although phase information is needed to achieve maximum accuracy, to effectively encode both chemosensory and thermosensory signals. GC neurons can effectively differentiate between thermal stimuli, excelling in distinguishing both large contrasts (14 vs. 36°C) and, although less effectively, more subtle temperature differences. Finally a direct comparison of the decoding accuracy of thermosensory signals between the two cortices reveals that whereas the somatosensory cortex exhibited higher overall accuracy, the GC still encodes significant thermosensory information. These findings highlight the GC's dual role in processing taste and temperature, emphasizing the importance of considering temperature in future studies of taste processing. KEY POINTS: Flavour perception relies on gustatory, olfactory and somatosensory integration, with the gustatory cortex (GC) central to taste processing. GC neurons also respond to temperature, but the specifics of how the GC processes taste and oral thermal stimuli remain unclear. The focus of this study is on the role of GC neurons in the encoding of oral thermal information, particularly compared to the coding functions of the oral somatosensory cortex. We found that whereas the somatosensory cortex shows a higher classification accuracy for distinguishing water temperature, the GC still encodes a substantial amount of thermosensory information. These results emphasize the importance of including temperature as a key factor in future studies of cortical taste coding.</p>\",\"PeriodicalId\":50088,\"journal\":{\"name\":\"Journal of Physiology-London\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":4.7000,\"publicationDate\":\"2025-01-19\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of Physiology-London\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1113/JP287499\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Physiology-London","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1113/JP287499","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
摘要
饮食行为受到味觉、嗅觉和体感信号的综合影响,这些信号都有助于对味道的感知。尽管广泛的研究已经探索了味觉皮层(GC)中味觉的神经相关性,但对其编码热信息的作用知之甚少。本研究比较了GC神经元和口腔体感皮层对口腔热感觉和化学感觉信号的编码。在这项研究中,我们记录了900多个GC神经元和500多个来自口腔体感皮层的神经元的尖峰活动,这些神经元被允许在不同的非伤害性温度下自由舔小滴的味觉刺激或去离子水。然后,我们开发并使用了基于贝叶斯的分析技术来评估基于舔循环内的峰值率和相位定时的神经分类分数。我们的研究结果表明,GC神经元主要依赖于速率信息,尽管相位信息需要达到最大的准确性,以有效地编码化学感觉和热感觉信号。GC神经元可以有效地区分热刺激,擅长区分大反差(14°C vs. 36°C)和更细微的温差(尽管效率较低)。最后,直接比较两种皮层对热感觉信号的解码精度表明,尽管体感皮层表现出更高的整体精度,但GC仍然编码了重要的热感觉信息。这些发现强调了GC在味觉加工和温度加工中的双重作用,强调了在未来味觉加工研究中考虑温度的重要性。重点:味觉感知依赖于味觉、嗅觉和体感的整合,而味觉皮层(GC)是味觉处理的中心。GC神经元也对温度有反应,但GC如何处理味觉和口腔热刺激的细节尚不清楚。本研究的重点是GC神经元在口腔热信息编码中的作用,特别是与口腔体感皮层的编码功能进行比较。我们发现,尽管体感皮层在区分水温方面表现出更高的分类精度,但GC仍然编码了大量的热感觉信息。这些结果强调了将温度作为未来皮层味觉编码研究的关键因素的重要性。
Cortical coding of gustatory and thermal signals in active licking mice.
Eating behaviours are influenced by the integration of gustatory, olfactory and somatosensory signals, which all contribute to the perception of flavour. Although extensive research has explored the neural correlates of taste in the gustatory cortex (GC), less is known about its role in encoding thermal information. This study investigates the encoding of oral thermal and chemosensory signals by GC neurons compared to the oral somatosensory cortex. In this study we recorded the spiking activity of more than 900 GC neurons and 500 neurons from the oral somatosensory cortex in mice allowed to freely lick small drops of gustatory stimuli or deionized water at varying non-nociceptive temperatures. We then developed and used a Bayesian-based analysis technique to assess neural classification scores based on spike rate and phase timing within the lick cycle. Our results indicate that GC neurons rely predominantly on rate information, although phase information is needed to achieve maximum accuracy, to effectively encode both chemosensory and thermosensory signals. GC neurons can effectively differentiate between thermal stimuli, excelling in distinguishing both large contrasts (14 vs. 36°C) and, although less effectively, more subtle temperature differences. Finally a direct comparison of the decoding accuracy of thermosensory signals between the two cortices reveals that whereas the somatosensory cortex exhibited higher overall accuracy, the GC still encodes significant thermosensory information. These findings highlight the GC's dual role in processing taste and temperature, emphasizing the importance of considering temperature in future studies of taste processing. KEY POINTS: Flavour perception relies on gustatory, olfactory and somatosensory integration, with the gustatory cortex (GC) central to taste processing. GC neurons also respond to temperature, but the specifics of how the GC processes taste and oral thermal stimuli remain unclear. The focus of this study is on the role of GC neurons in the encoding of oral thermal information, particularly compared to the coding functions of the oral somatosensory cortex. We found that whereas the somatosensory cortex shows a higher classification accuracy for distinguishing water temperature, the GC still encodes a substantial amount of thermosensory information. These results emphasize the importance of including temperature as a key factor in future studies of cortical taste coding.
期刊介绍:
The Journal of Physiology publishes full-length original Research Papers and Techniques for Physiology, which are short papers aimed at disseminating new techniques for physiological research. Articles solicited by the Editorial Board include Perspectives, Symposium Reports and Topical Reviews, which highlight areas of special physiological interest. CrossTalk articles are short editorial-style invited articles framing a debate between experts in the field on controversial topics. Letters to the Editor and Journal Club articles are also published. All categories of papers are subjected to peer reivew.
The Journal of Physiology welcomes submitted research papers in all areas of physiology. Authors should present original work that illustrates new physiological principles or mechanisms. Papers on work at the molecular level, at the level of the cell membrane, single cells, tissues or organs and on systems physiology are all acceptable. Theoretical papers and papers that use computational models to further our understanding of physiological processes will be considered if based on experimentally derived data and if the hypothesis advanced is directly amenable to experimental testing. While emphasis is on human and mammalian physiology, work on lower vertebrate or invertebrate preparations may be suitable if it furthers the understanding of the functioning of other organisms including mammals.