Institute of Zoology, University of Cologne, Cologne 50674, Germany.
Department of Animal Physiology, Institute of Zoology, University of Cologne, Cologne 50674, Germany.
J Neurosci. 2022 Jun 15;42(24):4841-4851. doi: 10.1523/JNEUROSCI.2290-20.2022. Epub 2022 May 11.
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 , 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. 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.
在多节段运动中，所有附肢的协调对于产生适当的运动输出至关重要。例如，在跑步中，腿部协调主要基于中央节律生成网络（称为中央模式发生器（CPG））的相互作用。然而，在较慢的运动形式中，起源于检测腿部节段位置、速度和负载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。感觉反馈如何影响 CPG 的活动以建立功能性神经元连接尚不完全清楚。使用雌性竹节虫，我们首次表明存在长距离头尾感觉连接，并强调作为感觉信号的负载足以使最头端的运动神经元（MN）活动同步。到目前为止，主要研究了头尾影响途径，其中通过胸部神经节中的 MN 活动表达的激活强度随着与这些神经节的距离增加而降低。在这里，我们通过使用毒蕈碱激动剂毛果芸香碱激活 CPG，在胸部神经节中产生节律性神经元活动，并强制单个剩余的腿进行踏步，从而产生节律性的神经元活动。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，与不同胸部神经节中伸缩 CPG 的距离相关的激活相反，单个踏步腿对活跃的伸缩 CPG 网络的节律性活动的同步没有这种依赖性。我们首次表明，感觉信息不仅传递到相邻的节段性神经节，而且传递到更远的节段，这表明存在头尾长距离感觉影响。这种影响取决于踏步方向，但与腿是主动还是被动移动无关。我们认为，感觉信息来自腿部的非特异性负载信号，由腿部的表皮机械感受器（ campaniform 感觉器）感知。我们的结果为昆虫腿部协调的长期确立的行为规则提供了神经基础。因此，我们在理解多足运动的神经网络方面取得了突破，并为动物王国中多节段运动系统的神经元功能连接开辟了新的视角。
