Nested Neuronal Dynamics Orchestrate a Behavioral Hierarchy across Timescales

Nested Neuronal Dynamics Orchestrate a Behavioral Hierarchy across Timescales
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DOI:
10.1016/j.neuron.2019.10.037
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发表时间:
2020-02-05
期刊:
影响因子:
16.2
通讯作者:
Zimmer, Manuel
Zimmer, Manuel
中科院分区:
医学1区
文献类型:
--
作者:
Kaplan, Harris S.;Thula, Oriana Salazar;Zimmer, Manuel

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经典和现代行为学研究表明,动物的行为是跨时间尺度分级组织的,因此较长时间尺度的行为由特定的较短时间尺度行为组成。尽管将神经元动力学与单时间尺度行为联系起来取得了进展,但不同的时间尺度动力学如何相互作用以产生这种更高级别的行为组织仍不清楚。在这里,我们展示了,在线虫秀丽线虫中,跨越三个时间尺度的行为层次是通过嵌套的神经元动力学实现的。在最高层级,横跨大脑和运动外周的缓慢神经元群体动力学控制着两个更快的运动神经元振荡,在不同的活动状态和功能角色之间切换。在较低的层级,这些更快的振荡进一步嵌套在一种方式上,使得能够在否则僵硬的层级框架中实现灵活的行为控制。我们的发现建立了嵌套的神经元活动模式,作为线虫神经系统的一个重复的动态基元,它们共同实现了可控的行为分层组织。
Classical and modern ethological studies suggest that animal behavior is organized hierarchically across timescales, such that longer-timescale behaviors are composed of specific shorter-timescale actions. Despite progress relating neuronal dynamics to single-timescale behavior, it remains unclear how different timescale dynamics interact to give rise to such higher-order behavioral organization. Here, we show, in the nematode Caenorhabditis elegans, that a behavioral hierarchy spanning three timescales is implemented by nested neuronal dynamics. At the uppermost hierarchical level, slow neuronal population dynamics spanning brain and motor periphery control two faster motor neuron oscillations, toggling them between different activity states and functional roles. At lower hierarchical levels, these faster oscillations are further nested in a manner that enables flexible behavioral control in an otherwise rigid hierarchical framework. Our findings establish nested neuronal activity patterns as a repeated dynamical motif of the C. elegans nervous system, which together implement a controllable hierarchical organization of behavior.