Fahoum Savanna-Rae H, Blitz Dawn M
Department of Biology and Center for Neuroscience, Miami University, Oxford, Ohio, United States.
J Neurophysiol. 2024 Feb 1;131(2):417-434. doi: 10.1152/jn.00373.2023. Epub 2024 Jan 10.
Network flexibility is important for adaptable behaviors. This includes neuronal switching, where neurons alter their network participation, including changing from single- to dual-network activity. Understanding the implications of neuronal switching requires determining how a switching neuron interacts with each of its networks. Here, we tested ) whether "home" and second networks, operating via divergent rhythm generation mechanisms, regulate a switching neuron and ) if a switching neuron, recruited via modulation of intrinsic properties, contributes to rhythm or pattern generation in a new network. Small, well-characterized feeding-related networks (pyloric, ∼1 Hz; gastric mill, ∼0.1 Hz) and identified modulatory inputs make the isolated crab () stomatogastric nervous system (STNS) a useful model to study neuronal switching. In particular, the neuropeptide Gly-SIFamide switches the lateral posterior gastric (LPG) neuron (2 copies) from pyloric-only to dual-frequency pyloric/gastric mill (fast/slow) activity via modulation of LPG-intrinsic properties. Using current injections to manipulate neuronal activity, we found that gastric mill, but not pyloric, network neurons regulated the intrinsically generated LPG slow bursting. Conversely, selective elimination of LPG from both networks using photoinactivation revealed that LPG regulated gastric mill neuron-firing frequencies but was not necessary for gastric mill rhythm generation or coordination. However, LPG alone was sufficient to produce a distinct pattern of network coordination. Thus, modulated intrinsic properties underlying dual-network participation may constrain which networks can regulate switching neuron activity. Furthermore, recruitment via intrinsic properties may occur in modulatory states where it is important for the switching neuron to actively contribute to network output. We used small, well-characterized networks to investigate interactions between rhythmic networks and neurons that switch their network participation. For a neuron switching into dual-network activity, only the second network regulated its activity in that network. In addition, the switching neuron was sufficient but not necessary to coordinate second network neurons and regulated their activity levels. Thus, regulation of switching neurons may be selective, and a switching neuron is not necessarily simply a follower in additional networks.
网络灵活性对于适应性行为很重要。这包括神经元切换,即神经元改变其网络参与情况,包括从单网络活动转变为双网络活动。理解神经元切换的影响需要确定切换神经元如何与其每个网络相互作用。在这里,我们测试了:1)通过不同节律生成机制运行的“主”网络和第二网络是否调节切换神经元;2)通过内在特性调制招募的切换神经元是否有助于新网络中的节律或模式生成。小型的、特征明确的与进食相关的网络(幽门网络,约1赫兹;胃磨网络,约0.1赫兹)以及已确定的调制输入,使得分离的螃蟹口胃神经系统(STNS)成为研究神经元切换的有用模型。特别是,神经肽甘氨酸 - SIF酰胺通过调制LPG的内在特性,将外侧后胃(LPG)神经元(2个副本)从仅参与幽门网络的活动转变为双频幽门/胃磨(快/慢)活动。通过电流注入来操纵神经元活动,我们发现胃磨网络神经元而非幽门网络神经元调节了内在产生的LPG慢发放。相反,使用光灭活从两个网络中选择性消除LPG后发现,LPG调节胃磨神经元的放电频率,但对于胃磨节律的产生或协调并非必需。然而,仅LPG就足以产生一种独特的网络协调模式。因此,双网络参与背后的调制内在特性可能限制哪些网络能够调节切换神经元的活动。此外,通过内在特性进行招募可能发生在调制状态下,此时切换神经元对网络输出做出积极贡献很重要。我们使用小型的、特征明确的网络来研究节律网络与切换其网络参与的神经元之间的相互作用。对于切换到双网络活动的神经元,只有第二网络调节其在该网络中的活动。此外,切换神经元足以协调第二网络神经元,但并非必需,并且调节它们的活动水平。因此,对切换神经元的调节可能是选择性的,并且切换神经元在额外网络中不一定仅仅是追随者。