Motor Neurons Tune Premotor Activity in a Vertebrate Central Pattern Generator

Motor Neurons Tune Premotor Activity in a Vertebrate Central Pattern Generator
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DOI:
10.1523/jneurosci.2755-16.2017
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发表时间:
2017-03-22
影响因子:
5.3
通讯作者:
Zornik, Erik
Zornik, Erik
中科院分区:
医学1区
文献类型:
--
作者:
Lawton, Kristy J.;Perry, Wick M.;Zornik, Erik

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中枢模式发生器(CPGs)是一种在没有感官反馈的情况下驱动有节奏运动输出的神经回路。脊椎动物CPGs通常被认为以自上而下的方式运作,其中前运动中间神经元激活运动神经元,运动神经元反过来驱动肌肉。相比之下,非洲爪蟾(Xenopus laevis)的声音CPG包含一个从运动核到运动前核的功能未知的神经元投影,表明一个可能有助于节奏产生的循环途径。在这项研究中,我们描述了这种自下而上的连接的功能。X. laevis的声音CPG产生50-60赫兹的“快颤音”歌曲,雄性在求偶期间使用。我们记录了来自喉神经的体外CPG的“有效发声”,同时记录了群体和单细胞水平的运动前活动。我们发现,横切运动到前运动的投射消除了前运动神经元的特征放电率。用胞内钠通道阻滞剂QX-314沉默运动神经元也会破坏运动前节律,就像阻断运动核中的尼古丁突触一样(运动神经元与神经元间连接的假定位置)。电刺激喉神经主要在运动前神经元中激发ipsp,这可以被烟碱受体拮抗剂阻断。我们的研究结果表明,运动神经元激活的抑制信号是CPG正常功能所必需的。据我们所知,这些发现代表了CPG中精确的运动前节律由运动神经元活动调节的第一个例子。
Central patterns generators (CPGs) are neural circuits that drive rhythmic motor output without sensory feedback. Vertebrate CPGs are generally believed to operate in a top-down manner in which premotor interneurons activate motor neurons that in turn drive muscles. In contrast, the frog (Xenopus laevis) vocal CPG contains a functionally unexplored neuronal projection from the motor nucleus to the premotor nucleus, indicating a recurrent pathway that may contribute to rhythm generation. In this study, we characterized the function of this bottom-up connection. The X. laevis vocal CPG produces a 50-60 Hz "fast trill" song used by males during courtship. We recorded "fictive vocalizations" in the in vitro CPG from the laryngeal nerve while simultaneously recording premotor activity at the population and single-cell level. We show that transecting the motor-to-premotor projection eliminated the characteristic firing rate of premotor neurons. Silencing motor neurons with the intracellular sodium channel blocker QX-314 also disrupted premotor rhythms, as did blockade of nicotinic synapses in the motor nucleus (the putative location of motor neuron-to-interneuron connections). Electrically stimulating the laryngeal nerve elicited primarily IPSPs in premotor neurons that could be blocked by a nicotinic receptor antagonist. Our results indicate that an inhibitory signal, activated by motor neurons, is required for proper CPG function. To our knowledge, these findings represent the first example of a CPG in which precise premotor rhythms are tuned by motor neuron activity.