中隔-海马系统的胆碱能动力学为空间新奇性提供相位复用信号,并与行为状态相关。

IF 4 2区 医学 Q1 NEUROSCIENCES
Fatemeh Farokhi Moghadam, Blanca E Gutiérrez-Guzmán, Xihui Zheng, Mina Parsa, Lojy M Hozyen, Holger Dannenberg
{"title":"中隔-海马系统的胆碱能动力学为空间新奇性提供相位复用信号,并与行为状态相关。","authors":"Fatemeh Farokhi Moghadam, Blanca E Gutiérrez-Guzmán, Xihui Zheng, Mina Parsa, Lojy M Hozyen, Holger Dannenberg","doi":"10.1523/JNEUROSCI.0133-25.2025","DOIUrl":null,"url":null,"abstract":"<p><p>In the hippocampal formation, cholinergic modulation from the medial septum/diagonal band of Broca is known to correlate with the speed of an animal's movements at subsecond timescales and also supports spatial memory formation. Yet, the extent to which subsecond cholinergic dynamics, if at all, align with transient behavioral and cognitive states supporting the encoding of novel spatial information remains unknown. In this study, we used fiber photometry to record the temporal dynamics in the population activity of septo-hippocampal cholinergic neurons at subsecond resolution during a hippocampus-dependent object location memory task using ChAT-Cre mice of both sexes. Using a linear mixed-effects model, we quantified the extent to which cholinergic dynamics were explained by changes in movement speed; behavioral states such as locomotion, grooming, and rearing; and hippocampus-dependent cognitive states such as recognizing a novel location of a familiar object. The data show that cholinergic dynamics contain a multiplexed code of fast and slow signals (1) coding for the logarithm of movement speed at subsecond timescales, (2) providing a phasic spatial novelty signal during the brief periods of exploring a novel object location, and (3) coding for recency of environmental change at a seconds-long timescale. Furthermore, behavioral event-related phasic cholinergic activity demonstrates that fast cholinergic transients correlate with a switch in cognitive and behavioral states. These findings enhance understanding of the mechanisms by which cholinergic modulation contributes to the coding of movement speed and encoding of novel spatial information.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0000,"publicationDate":"2025-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12509495/pdf/","citationCount":"0","resultStr":"{\"title\":\"Cholinergic Dynamics in the Septo-hippocampal System Provide Phasic Multiplexed Signals for Spatial Novelty and Correlate with Behavioral States.\",\"authors\":\"Fatemeh Farokhi Moghadam, Blanca E Gutiérrez-Guzmán, Xihui Zheng, Mina Parsa, Lojy M Hozyen, Holger Dannenberg\",\"doi\":\"10.1523/JNEUROSCI.0133-25.2025\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>In the hippocampal formation, cholinergic modulation from the medial septum/diagonal band of Broca is known to correlate with the speed of an animal's movements at subsecond timescales and also supports spatial memory formation. Yet, the extent to which subsecond cholinergic dynamics, if at all, align with transient behavioral and cognitive states supporting the encoding of novel spatial information remains unknown. In this study, we used fiber photometry to record the temporal dynamics in the population activity of septo-hippocampal cholinergic neurons at subsecond resolution during a hippocampus-dependent object location memory task using ChAT-Cre mice of both sexes. Using a linear mixed-effects model, we quantified the extent to which cholinergic dynamics were explained by changes in movement speed; behavioral states such as locomotion, grooming, and rearing; and hippocampus-dependent cognitive states such as recognizing a novel location of a familiar object. The data show that cholinergic dynamics contain a multiplexed code of fast and slow signals (1) coding for the logarithm of movement speed at subsecond timescales, (2) providing a phasic spatial novelty signal during the brief periods of exploring a novel object location, and (3) coding for recency of environmental change at a seconds-long timescale. Furthermore, behavioral event-related phasic cholinergic activity demonstrates that fast cholinergic transients correlate with a switch in cognitive and behavioral states. These findings enhance understanding of the mechanisms by which cholinergic modulation contributes to the coding of movement speed and encoding of novel spatial information.</p>\",\"PeriodicalId\":50114,\"journal\":{\"name\":\"Journal of Neuroscience\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":4.0000,\"publicationDate\":\"2025-10-08\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12509495/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of Neuroscience\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1523/JNEUROSCI.0133-25.2025\",\"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 Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.0133-25.2025","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

在海马结构中,来自内侧隔/布洛卡斜带(MSDB)的胆碱能调节与动物在亚秒时间尺度上的运动速度有关,也支持空间记忆的形成。然而,亚秒胆碱能动态在多大程度上与支持新空间信息编码的瞬时行为和认知状态相一致,仍然是未知的。在这项研究中,我们使用纤维光度法记录了在海马依赖的物体位置记忆任务中,在亚秒分辨率下隔海海马胆碱能神经元群体活动的时间动态。使用线性混合效应模型,我们量化了胆碱能动力学在多大程度上可以通过运动速度、行为状态(如运动、梳理和饲养)以及海马体依赖的认知状态(如识别熟悉物体的新位置)的变化来解释。数据表明,胆碱能动力学包含快慢信号的多路编码:1)在亚秒级时间尺度上对运动速度的对数进行编码;2)在探索新目标位置的短暂时间内提供相位空间新颖性信号;3)在秒级时间尺度上对环境变化的近时性进行编码。此外,行为事件相关的阶段性胆碱能活动表明,快速胆碱能瞬变与认知和行为状态的转换有关。这些发现加强了对胆碱能调节对运动速度编码和新空间信息编码的机制的理解。众所周知,乙酰胆碱是一种认知功能和行为的神经调节剂,计算模型表明它在新记忆的编码中起着重要作用。然而,胆碱能动力学是否足够快以作为空间新颖性信号尚不清楚。在这里,我们证明了小鼠中隔-海马体回路中的胆碱能信号表现出多个时间尺度的活动,其中快速信号反映了对新物体位置的检测,编码了运动速度的对数,并与行为状态转换相关。在更长的时间尺度上,胆碱能瞬态编码环境变化的近时性。这些发现为探究乙酰胆碱在探索行为和记忆引导导航过程中对空间记忆的编码和检索动力学以及获取的作用机制提供了重要的见解。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Cholinergic Dynamics in the Septo-hippocampal System Provide Phasic Multiplexed Signals for Spatial Novelty and Correlate with Behavioral States.

In the hippocampal formation, cholinergic modulation from the medial septum/diagonal band of Broca is known to correlate with the speed of an animal's movements at subsecond timescales and also supports spatial memory formation. Yet, the extent to which subsecond cholinergic dynamics, if at all, align with transient behavioral and cognitive states supporting the encoding of novel spatial information remains unknown. In this study, we used fiber photometry to record the temporal dynamics in the population activity of septo-hippocampal cholinergic neurons at subsecond resolution during a hippocampus-dependent object location memory task using ChAT-Cre mice of both sexes. Using a linear mixed-effects model, we quantified the extent to which cholinergic dynamics were explained by changes in movement speed; behavioral states such as locomotion, grooming, and rearing; and hippocampus-dependent cognitive states such as recognizing a novel location of a familiar object. The data show that cholinergic dynamics contain a multiplexed code of fast and slow signals (1) coding for the logarithm of movement speed at subsecond timescales, (2) providing a phasic spatial novelty signal during the brief periods of exploring a novel object location, and (3) coding for recency of environmental change at a seconds-long timescale. Furthermore, behavioral event-related phasic cholinergic activity demonstrates that fast cholinergic transients correlate with a switch in cognitive and behavioral states. These findings enhance understanding of the mechanisms by which cholinergic modulation contributes to the coding of movement speed and encoding of novel spatial information.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
Journal of Neuroscience
Journal of Neuroscience 医学-神经科学
CiteScore
9.30
自引率
3.80%
发文量
1164
审稿时长
12 months
期刊介绍: JNeurosci (ISSN 0270-6474) is an official journal of the Society for Neuroscience. It is published weekly by the Society, fifty weeks a year, one volume a year. JNeurosci publishes papers on a broad range of topics of general interest to those working on the nervous system. Authors now have an Open Choice option for their published articles
×
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