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Lumbar V3 interneurons provide direct excitatory synaptic input onto thoracic sympathetic preganglionic neurons, linking locomotor, and autonomic spinal systems
Frontiers in Neural Circuits ( IF 3.5 ) Pub Date : 2023-08-28 , DOI: 10.3389/fncir.2023.1235181
Camila Chacon 1 , Chioma V Nwachukwu 1 , Narjes Shahsavani 1 , Kristine C Cowley 1 , Jeremy W Chopek 1
Affiliation  

Although sympathetic autonomic systems are activated in parallel with locomotion, the neural mechanisms mediating this coordination are incompletely understood. Sympathetic preganglionic neurons (SPNs), primarily located in the intermediate laminae of thoracic and upper lumbar segments (T1-L2), increase activation of tissues and organs that provide homeostatic and metabolic support during movement and exercise. Recent evidence suggests integration between locomotor and autonomic nuclei occurs within the brainstem, initiating both descending locomotor and sympathetic activation commands. However, both locomotor and sympathetic autonomic spinal systems can be activated independent of supraspinal input, in part due to a distributed network involving propriospinal neurons. Whether an intraspinal mechanism exists to coordinate activation of these systems is unknown. We hypothesized that ascending spinal neurons located in the lumbar region provide synaptic input to thoracic SPNs. Here, we demonstrate that synaptic contacts from locomotor-related V3 interneurons (INs) are present in all thoracic laminae. Injection of an anterograde tracer into lumbar segments demonstrated that 8–20% of glutamatergic input onto SPNs originated from lumbar V3 INs and displayed a somatotopographical organization of synaptic input. Whole cell patch clamp recording in SPNs demonstrated prolonged depolarizations or action potentials in response to optical activation of either lumbar V3 INs in spinal cord preparations or in response to optical activation of V3 terminals in thoracic slice preparations. This work demonstrates a direct intraspinal connection between lumbar locomotor and thoracic sympathetic networks and suggests communication between motor and autonomic systems may be a general function of the spinal cord.

中文翻译:

腰椎 V3 中间神经元向胸交感神经节前神经元提供直接兴奋性突触输入,连接运动和自主脊柱系统

尽管交感神经自主系统在运动的同时被激活,但介导这种协调的神经机制尚不完全清楚。交感节前神经元 (SPN) 主要位于胸段和上腰段 (T1-L2) 的中间层,可增加组织和器官的激活,从而在运动和锻炼期间提供稳态和代谢支持。最近的证据表明,运动核和自主神经核之间的整合发生在脑干内,启动下行运动和交感神经激活命令。然而,运动和交感自主脊髓系统都可以独立于脊髓上输入而被激活,部分原因是涉及本体脊髓神经元的分布式网络。是否存在协调这些系统激活的脊柱内机制尚不清楚。我们假设位于腰部区域的上升脊髓神经元为胸部 SPN 提供突触输入。在这里,我们证明来自运动相关的 V3 中间神经元 (IN) 的突触接触存在于所有胸椎板中。向腰节注射顺行示踪剂表明,SPN 上 8-20% 的谷氨酸输入源自腰椎 V3 IN,并显示了突触输入的体形组织。SPN 中的全细胞膜片钳记录表明,响应于脊髓制备物中腰椎 V3 IN 的光学激活或响应于胸部切片制备物中 V3 末端的光学激活,存在延长的去极化或动作电位。这项工作证明了腰椎运动网络和胸交感神经网络之间的直接脊柱内联系,并表明运动系统和自主系统之间的通信可能是脊髓的一般功能。
更新日期:2023-08-28
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