Saltiel Philippe, d'Avella Andrea, Wyler-Duda Kuno, Bizzi Emilio
Department of Brain and Cognitive Sciences, McGovern Institute for Brain Research, Massachusetts Institute of Technology, 77 Massachusetts Ave. 46-6189, Cambridge, MA, 02139, USA.
Department of Biomedical Sciences and Morphological and Functional Images, University of Messina, Messina, Italy.
Brain Struct Funct. 2016 Nov;221(8):3869-3890. doi: 10.1007/s00429-015-1133-5. Epub 2015 Oct 26.
Locomotion is produced by a central pattern generator. Its spinal cord organization is generally considered to be distributed, with more rhythmogenic rostral lumbar segments. While this produces a rostrocaudally traveling wave in undulating species, this is not thought to occur in limbed vertebrates, with the exception of the interneuronal traveling wave demonstrated in fictive cat scratching (Cuellar et al. J Neurosci 29:798-810, 2009). Here, we reexamine this hypothesis in the frog, using the seven muscle synergies A to G previously identified with intraspinal NMDA (Saltiel et al. J Neurophysiol 85:605-619, 2001). We find that locomotion consists of a sequence of synergy activations (A-B-G-A-F-E-G). The same sequence is observed when focal NMDA iontophoresis in the spinal cord elicits a caudal extension-lateral force-flexion cycle (flexion onset without the C synergy). Examining the early NMDA-evoked motor output at 110 sites reveals a rostrocaudal topographic organization of synergy encoding by the lumbar cord. Each synergy is preferentially activated from distinct regions, which may be multiple, and partially overlap between different synergies. Comparing the sequence of synergy activation in locomotion with their spinal cord topography suggests that the locomotor output is achieved by a rostrocaudally traveling wave of activation in the swing-stance cycle. A two-layer circuitry model, based on this topography and a traveling wave reproduces this output and explores its possible modifications under different afferent inputs. Our results and simulations suggest that a rostrocaudally traveling wave of excitation takes advantage of the topography of interneuronal regions encoding synergies, to activate them in the proper sequence for locomotion.
运动是由中枢模式发生器产生的。其脊髓组织通常被认为是分布式的，在腰段脊髓头侧部分具有更多的节律产生能力。虽然这在波动类物种中会产生头尾向传播的波，但除了在虚拟猫抓挠行为中显示的中间神经元传播波外（Cuellar等人，《神经科学杂志》29:798 - 810，2009年），人们认为在有肢脊椎动物中不会发生这种情况。在这里，我们使用先前通过脊髓内NMDA鉴定出的七种肌肉协同作用A至G（Saltiel等人，《神经生理学杂志》85:605 - 619，2001年），在青蛙中重新审视这一假设。我们发现运动由一系列协同作用激活组成（A - B - G - A - F - E - G）。当脊髓内局部NMDA离子电渗引发尾侧伸展 - 侧向力 - 屈曲循环（无C协同作用的屈曲起始）时，观察到相同的序列。在110个位点检查早期NMDA诱发的运动输出，揭示了腰段脊髓协同作用编码的头尾向拓扑组织。每种协同作用从不同的区域优先被激活，这些区域可能有多个，并且在不同协同作用之间部分重叠。将运动中协同作用激活的序列与其脊髓拓扑结构进行比较表明，运动输出是通过摆动 - 站立周期中头尾向传播的激活波实现的。基于这种拓扑结构和传播波的两层电路模型再现了这种输出，并探索了在不同传入输入下其可能的变化。我们的结果和模拟表明，头尾向传播的兴奋波利用编码协同作用的中间神经元区域的拓扑结构，以适当的运动序列激活它们。
