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Existence of a Long-Range Caudo-Rostral Sensory Influence in Terrestrial Locomotion
Journal of Neuroscience ( IF 4.4 ) Pub Date : 2022-06-15 , DOI: 10.1523/jneurosci.2290-20.2022
Martyna Grabowska , Tibor I. Toth , Ansgar Büschges , Silvia Daun

In multisegmented locomotion, coordination of all appendages is crucial for the generation of a proper motor output. In running for example, leg coordination is mainly based on the central interaction of rhythm generating networks, called central pattern generators (CPGs). In slower forms of locomotion, however, sensory feedback, which originates from sensory organs that detect changes in position, velocity and load of the legs' segments, has been shown to play a more crucial role. How exactly sensory feedback influences the activity of the CPGs to establish functional neuronal connectivity is not yet fully understood. Using the female stick insect Carausius morosus, we show for the first time that a long-range caudo-rostral sensory connection exists and highlight that load as sensory signal is sufficient to entrain rhythmic motoneuron (MN) activity in the most rostral segment. So far, mainly rostro-caudal influencing pathways have been investigated where the strength of activation, expressed by the MN activity in the thoracic ganglia, decreases with the distance from the stepping leg to these ganglia. Here, we activated CPGs, producing rhythmic neuronal activity in the thoracic ganglia by using the muscarinic agonist pilocarpine and enforced the stepping of a single, remaining leg. This enabled us to study sensory influences on the CPGs' oscillatory activity. Using this approach, we show that, in contrast to the distance-dependent activation of the protractor-retractor CPGs in different thoracic ganglia, there is no such dependence for the entrainment of the rhythmic activity of active protractor-retractor CPG networks by individual stepping legs.

SIGNIFICANCE STATEMENT We show for the first time that sensory information is transferred not only to the immediate adjacent segmental ganglia but also to those farther away, indicating the existence of a long-range caudo-rostral sensory influence. This influence is dependent on stepping direction but independent of whether the leg is actively or passively moved. We suggest that the sensory information comes from unspecific load signals sensed by cuticle mechanoreceptors (campaniform sensilla) of a leg. Our results provide a neuronal basis for the long-established behavioral rules of insect leg coordination. We thus provide a breakthrough in understanding the neuronal networks underlying multilegged locomotion and open new vistas into the neuronal functional connectivity of multisegmented locomotion systems across the animal kingdom.



中文翻译:

陆地运动中远距离尾嘴感觉影响的存在

在多节运动中,所有附件的协调对于产生适当的运动输出至关重要。例如,在跑步中,腿部协调主要基于节奏生成网络的中央交互,称为中央模式生成器 (CPG)。然而,在较慢的运动形式中,源自检测腿部位置、速度和负荷变化的感觉器官的感觉反馈已被证明发挥着更关键的作用。感觉反馈究竟如何影响 CPG 的活动以建立功能性神经元连接性尚不完全清楚。使用雌性竹节虫Carausius morosus,我们首次证明存在长程的尾端感觉连接,并强调作为感觉信号的负载足以在最头端部分夹带节律性运动神经元 (MN) 活动。到目前为止,主要研究了rostro-caudal影响途径,其中激活强度(由胸神经节中的MN活动表示)随着从踏腿到这些神经节的距离而降低。在这里,我们激活了 CPG,通过使用毒蕈碱激动剂毛果芸香碱在胸神经节中产生有节律的神经元活动,并强制单条剩余腿迈步。这使我们能够研究感觉对 CPG 振荡活动的影响。使用这种方法,我们表明,与不同胸神经节中量角器-牵开器 CPG 的距离依赖性激活相比,

重要性声明我们首次表明,感觉信息不仅会转移到直接相邻的节段神经节,还会转移到更远的节段,表明存在远程尾端感觉影响。这种影响取决于踏步方向,但与腿是主动移动还是被动移动无关。我们建议感觉信息来自腿部角质层机械感受器(钟状感受器)感知的非特异性负荷信号。我们的研究结果为昆虫腿部协调的长期行为规则提供了神经元基础。因此,我们在理解多足运动的神经元网络方面提供了突破,并为整个动物王国的多节运动系统的神经元功能连接开辟了新的前景。

更新日期:2022-06-16
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