Asymmetric and transient properties of reciprocal activity of antagonists during the paw-shake response in the cat

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.Author summary: The existence of multifunctional central pattern generators (CPGs), circuits which control more than one rhythmic motor behavior, is an intriguing hypothesis. We suggest that the cat paw-shaking response could be a transient response of the locomotor CPG. Our general prediction is that this CPG is multifunctional, and in addition to the locomotor rhythm, it can generate a transient, ten-times faster, paw-shake-like response to a stimulus. In our multistable half-center oscillator (HCO) CPG model, we applied perturbations to the locomotor pattern which resulted in a transient paw-shake-like pattern that eventually returned back to the locomotor pattern. We showed that the inactivation of the slow inward current that drives the locomotor rhythm produced asymmetry of the transient flexor and extensor activity in a symmetric HCO model. To test predictions from our model about the transient nature of the paw-shake response, we compared burst durations (BDs) and interburst intervals (IBIs) of the model half-centers in consecutive cycles of paw-shake-like responses with the BD and IBI of electromyographic (EMG) activity bursts of cat hindlimb flexors and extensors recorded during a paw-shake response. In both cases, we found similar asymmetric trends in the BD and IBI throughout a paw-shake response.