Neuroscience Institute, Georgia State University, Atlanta, Georgia, United States of America.
School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, United States of America.
PLoS Comput Biol. 2021 Dec 28;17(12):e1009677. doi: 10.1371/journal.pcbi.1009677. eCollection 2021 Dec.
Mutually inhibitory populations of neurons, half-center oscillators (HCOs), are commonly involved in the dynamics of the central pattern generators (CPGs) driving various rhythmic movements. Previously, we developed a multifunctional, multistable symmetric HCO model which produced slow locomotor-like and fast paw-shake-like activity patterns. Here, we describe asymmetric features of paw-shake responses in a symmetric HCO model and test these predictions experimentally. We considered bursting properties of the two model half-centers during transient paw-shake-like responses to short perturbations during locomotor-like activity. We found that when a current pulse was applied during the spiking phase of one half-center, let's call it #1, the consecutive burst durations (BDs) of that half-center increased throughout the paw-shake response, while BDs of the other half-center, let's call it #2, only changed slightly. In contrast, the consecutive interburst intervals (IBIs) of half-center #1 changed little, while IBIs of half-center #2 increased. We demonstrated that this asymmetry between the half-centers depends on the phase of the locomotor-like rhythm at which the perturbation was applied. We suggest that the fast transient response reflects functional asymmetries of slow processes that underly the locomotor-like pattern; e.g., asymmetric levels of inactivation across the two half-centers for a slowly inactivating inward current. We compared model results with those of in-vivo paw-shake responses evoked in locomoting cats and found similar asymmetries. Electromyographic (EMG) BDs of anterior hindlimb muscles with flexor-related activity increased in consecutive paw-shake cycles, while BD of posterior muscles with extensor-related activity did not change, and vice versa for IBIs of anterior flexors and posterior extensors. We conclude that EMG activity patterns during paw-shaking are consistent with the proposed mechanism producing transient paw-shake-like bursting patterns found in our multistable HCO model. We suggest that the described asymmetry of paw-shaking responses could implicate a multifunctional CPG controlling both locomotion and paw-shaking.
相互抑制的神经元群体，即半中心振荡器（HCO），通常参与驱动各种节律运动的中枢模式发生器（CPG）的动力学。以前，我们开发了一种多功能、多稳态对称 HCO 模型，该模型产生缓慢的类似运动和快速的爪子抖动样活动模式。在这里，我们描述了对称 HCO 模型中爪子抖动反应的不对称特征，并通过实验验证了这些预测。我们考虑了在类似运动活动期间短暂的爪子抖动样反应中，两个模型半中心的爆发特性。我们发现，当在一个半中心（我们称之为#1）的尖峰阶段施加电流脉冲时，该半中心的连续爆发持续时间（BD）在整个爪子抖动反应中增加，而另一个半中心（我们称之为#2）的 BD 仅略有变化。相比之下，半中心#1 的连续爆发间隔（IBI）变化不大，而半中心#2 的 IBI 增加。我们证明了这种半中心之间的不对称性取决于施加扰动时类似运动节律的相位。我们认为，快速瞬态反应反映了潜在运动模式的缓慢过程的功能不对称性；例如，对于一个缓慢失活的内向电流，两个半中心之间的失活水平不对称。我们将模型结果与在运动猫中诱发的爪子抖动的体内反应进行了比较，并发现了类似的不对称性。具有屈肌相关活动的前肢后肌的肌电图（EMG）BD 在连续的爪子抖动周期中增加，而具有伸肌相关活动的后肌的 BD 没有变化，反之亦然，前肢屈肌和后肢伸肌的 IBI 也是如此。我们得出结论，在爪子抖动期间的 EMG 活动模式与我们的多稳态 HCO 模型中发现的产生短暂的爪子抖动样爆发模式的建议机制一致。我们认为，描述的爪子抖动反应的不对称性可能暗示着控制运动和爪子抖动的多功能 CPG。
