Differences in flexor and extensor activity during locomotor‐related leg movements in chick embryos

Abstract

Prior to hatching, chick embryos spontaneously produce repetitive limb movements (RLMs), a developmental precursor to walking. During RLMs, flexor and extensor muscles are alternately active as during stance and swing phases of gait. However, previous studies of RLMs observed that flexor muscles were rhythmically active for many cycles, whereas extensors often failed to be recruited. Thus, we asked if flexor muscles are preferentially recruited during RLMs in chick embryos 1 day before hatching and onset of walking. Using a within-subject design, we compared EMG burst parameters for flexor and extensor muscles acting at the hip or ankle. Findings indicated that flexor burst count exceeded extensor count. Also, flexor muscles were consistently recruited at the lowest levels of neural drive. We conclude that there is a bias favoring flexor muscle recruitment and drive during spontaneously produced RLMs. Potential neural mechanisms and developmental implications of our findings are discussed.

Ankle muscle tenotomy does not alter ankle flexor muscle recruitment bias during locomotor‐related repetitive limb movement in late‐stage chick embryos

“…Another key finding was that neither tenotomy nor removal of spatial restraint altered the scaling of integrated burst amplitude during RLMs (Sun & Bradley, ). Normalized TA integrated amplitude during RLMs under all conditions was least in the absence of LG activity and greatest when LG was consistently recruited.…”

“…Normalized TA integrated amplitude during RLMs under all conditions was least in the absence of LG activity and greatest when LG was consistently recruited. Given that burst amplitude is an indicator of excitatory neural drive (Farina, Merletti, & Enoka, ; Staudenmann, van Dieen, Stegeman, & Enoka, ), we recently proposed that amplitude scaling and consistent flexor bursting across all levels of drive are indicative of an excitatory drive favoring flexor motor pools during RLMs (Sun & Bradley, ). Thus, current results lead us to conclude that muscle afference does not significantly contribute to the flexor bias in neural drive during RLMs in E20 chicks.…”

“…Embryos were prepared for electromyography (EMG) and synchronized video recording of spontaneous leg movements in ovo. Procedures are briefly summarized, as detailed descriptions have been published (Sindhurakar & Bradley, ; Sun & Bradley, ). An analgesic (Buprenex®, 0.01 mg/kg) was given prior to EMG implantation, and had no apparent impact on behavior following implantation, for embryos were typically active and often initiated RLMs upon placement in the recording chamber.…”

“…Further, leg muscles are repetitively recruited at frequencies observed in posthatching locomotion (Bradley, Ryu, & Lin, 2008;Ryu & Bradley, 2009;Sindhurakar & Bradley, 2012). One feature that distinguishes RLM EMG activity from posthatching locomotion is a bias in recruitment and drive of flexor muscles (Sun & Bradley, 2017). Flexor muscles are more consistently recruited than the antagonist extensors during FIGURE 1 Embryonic postures, kinematic preparations and EMG burst detection.…”

“…Extensor II afferents participate in the flexor reflex afferent circuit, inhibiting homonymous extensor motor pools, and exciting antagonist flexor motor pools (Jankowska, 1992;Lundberg, Malmgren, & Schomburg, 1987;Matthews, 1972). Extensor 1a afferents may also be active during homonymous muscle activity, however, extensor recruitment is relatively infrequent during most RLMs (Bradley et al, 2008;Sun & Bradley, 2017), and extensor 1a imposes only weak reciprocal inhibition on antagonist flexor motor neurons (Nichols, 1989). Alternatively, flexor 1a afferents may enhance flexor bias owing to the extremely small joint excursions during RLMs (Bradley et al, 2014), in that limited movement during vigorous flexor activity can impose isometric contractions that reinforce flexor 1a afferent activity (Edin & Vallbo, 1990;Hagbarth, Wallin, & Lofstedt, 1975).…”