Farmer David G S, Patros Mikaela, Ottaviani Matteo M, Dawood Tye, Kumric Marko, Bozic Josko, Badour Matt I, Bain Anthony R, Barak Otto F, Dujic Zeljko, Macefield Vaughan G
Department of Neuroscience, Monash University, Melbourne, Victoria, Australia.
Department of Neurosurgery, Università Politecnica delle Marche, Ancona, Italy.
J Physiol. 2025 Mar;603(7):1941-1958. doi: 10.1113/JP286423. Epub 2024 Sep 25.
Microneurographic recordings of the human cervical vagus nerve have revealed the presence of multi-unit neural activity with measurable cardiac rhythmicity. This suggests that the physiology of vagal neurones with cardiovascular regulatory function can be studied using this method. Here, the activity of cardiac rhythmic single units was discriminated from human cervical vagus nerve recordings using template-based waveform matching. The activity of 44 cardiac rhythmic neurones (22 with myelinated axons and 22 with unmyelinated axons) was isolated. By consideration of each unit's firing pattern with respect to the cardiac and respiratory cycles, the functional identification of each unit was attempted. Of note is the observation of seven cardiac rhythmic neurones with myelinated axons whose activity was recruited or enhanced by slow, deep breathing, was maximal during the nadir of respiratory sinus arrhythmia, and showed an expiratory peak. This is characteristic of cardioinhibitory efferent neurones, which are responsible for respiratory sinus arrhythmia. The remaining 15 cardiac rhythmic neurones with myelinated axons were categorised as cardiopulmonary receptors or arterial baroreceptors based on the position of their peak in firing with respect to the R-wave of the cardiac cycle. This latter method is not viable for neurones with unmyelinated axons due to their slow and unknown conduction velocities. With the exception of three neurones whose expiratory modulation implicates them as cardiac-projecting efferent neurones, this population is likely dominated by arterial baroreceptors. In conclusion, the activity of single units with cardiovascular function has been discriminated within the human cervical vagus, enabling their systematic study. KEY POINTS: Recordings of the electrical activity of the vagus nerve have recently been made at the level of the neck in humans. Examination of the gross activity of this nerve reveals subpopulations of neurones whose activity fluctuates in time with the heart's beat, suggesting that the neurones that monitor or modify cardiac function can be studied using this method. Here, the activity of individual cardiac rhythmic neurones was isolated from human vagus nerve recordings using template-based spike sorting. The relationship between this activity and the cardiac and respiratory cycles was used as a means of classifying each neurone. Neuronal firing patterns that are consistent with that of neurones that modify cardiac function, including heart-slowing 'cardioinhibitory' neurones, as well as neurones that inform the brain of cardiovascular status were observed. This approach enables, for the first time, the systematic study of the function of these neurones in humans in both health and disease.
对人类颈迷走神经的微神经图记录显示,存在具有可测量心脏节律性的多单位神经活动。这表明可以使用这种方法研究具有心血管调节功能的迷走神经元的生理学。在此,使用基于模板的波形匹配从人类颈迷走神经记录中区分出心脏节律性单个单位的活动。分离出44个心脏节律性神经元(22个有髓鞘轴突和22个无髓鞘轴突)的活动。通过考虑每个单位相对于心脏和呼吸周期的放电模式,尝试对每个单位进行功能识别。值得注意的是,观察到7个有髓鞘轴突的心脏节律性神经元,其活动在缓慢深呼吸时被募集或增强,在呼吸性窦性心律不齐的最低点时最大,并显示呼气峰值。这是负责呼吸性窦性心律不齐的心脏抑制性传出神经元的特征。其余15个有髓鞘轴突的心脏节律性神经元根据其放电峰值相对于心动周期R波的位置被分类为心肺感受器或动脉压力感受器。由于无髓鞘轴突神经元的传导速度缓慢且未知,后一种方法对它们不可行。除了三个呼气调制表明它们是投射到心脏的传出神经元外,这群神经元可能主要是动脉压力感受器。总之,已在人类颈迷走神经中区分出具有心血管功能的单个单位的活动,从而能够对其进行系统研究。要点:最近在人类颈部水平对迷走神经的电活动进行了记录。对该神经总体活动的检查揭示了神经元亚群,其活动随心跳时间波动,这表明可以使用这种方法研究监测或改变心脏功能的神经元。在此,使用基于模板的尖峰分类从人类迷走神经记录中分离出单个心脏节律性神经元的活动。这种活动与心脏和呼吸周期之间的关系被用作对每个神经元进行分类的一种手段。观察到与改变心脏功能的神经元一致的神经元放电模式,包括使心脏减慢的“心脏抑制性”神经元,以及向大脑传递心血管状态信息的神经元。这种方法首次能够在健康和疾病状态下对人类这些神经元的功能进行系统研究。