Light Accelerates Morphogenesis and Acquisition of Interlimb Stepping in Chick Embryos

Abstract

Chicks are bipedal precocious vertebrates that achieve adaptive locomotor skill within hours after hatching. Development of limb movement has been extensively studied in the chicken embryo, but few studies have focused on the preparations leading to precocious locomotor skill. Chicks typically hatch after 21 days of incubation, and recent studies provided evidence that the neural circuits for intralimb control of stepping are established between embryonic days (E) 18–20. It has also been shown that variations in light exposure during embryogenesis can accelerate or delay the onset of hatching and walking by 1 to 2 days. Our earlier work revealed that despite these differences in time to hatch, chicks incubated in different light conditions achieved similar locomotor skill on the day of hatching. Results suggested to us that light exposure during incubation may have accelerated development of locomotor circuits in register with earlier hatching. Thus, in this study, embryos were incubated in 1 of 3 light conditions to determine if development of interlimb coordination at a common time point, 19 days of incubation, varied with light exposure during embryogenesis. Leg muscle activity was recorded bilaterally and burst analyses were performed for sequences of spontaneous locomotor-related activity in one or more ankle muscles to quantify the extent of interlimb coordination in ovo. We report findings indicating that the extent of interlimb coordination varied with light exposure, and left-right alternating steps were a more reliable attribute of interlimb coordination for embryos incubated in constant bright light. We provide evidence that morphological development of the leg varied with light exposure. Based on these findings, we propose that light can accelerate the development of interlimb coordination in register with earlier hatching. Our results lead us to further propose that alternating left-right stepping is the default pattern of interlimb coordination produced by locomotor circuits during embryogenesis.

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

“…Left and right homologous muscles burst alternately, as observed during the stepping of left and right legs. Further, left-right alternation of leg muscle activity was more commonly observed in flexors than extensors 1 day prior to hatching and onset of walking (Sindhurakar & Bradley, 2012). These studies also observed that extensors frequently dropped out or failed to burst rhythmically during RLMs.…”

“…However, in many sequences, one muscle was consistently active, and the antagonist muscle failed to produce one or more bursts. EMG bursts were detected and analyzed based on previously established criteria (Bradley et al, 2008;Bradley, Ryu, & Yeseta, 2014;Ryu & Bradley, 2009;Sindhurakar & Bradley, 2012 five rhythmic bursts, and the right TA (r-TA) failed to produce bursts during three of the RLM cycles (asterisks). For example, in Figure 2B, the hip flexor (SA) produced 11 bursts (10 cycles), and its antagonist (CF) failed to produce bursts that met detection criteria in four cycles (noted by asterisks).…”

Drift during overground locomotion in newly hatched chicks varies with light exposure during embryogenesis

“…Though there were no differences in egg weight, body weight or toe length, tibia length varied positively with light exposure and was significantly shorter for chicks incubated in 24D compared to 24L. Further, differences in muscle activity and practice of locomotor-related leg movements in ovo (Sindhurakar & Bradley, 2012), might have contributed to differences in balance control at hatching. Both muscle fiber development and muscle activity are enhanced by light exposure and also contribute to bone maturation (Liu, Wang, & Chen, 2010; Hall & Herring, 1990).…”

“…Incubation conditions for this study were previously described (Sindhurakar & Bradley, 2010, 2012). In brief, incubators were configured for 1 of 3 light exposures that varied light intensity and exposure duration: 650-3000 lux, 12 hr daily (12L); 4000-7000 lux, 24 hr daily (24L); or ≤ 1 lux, 24 hr daily (24D).…”

“…Studies have examined the effects of light exposure in the final days before hatching, providing evidence that light is a salient stimulus capable of influencing vision-mediated behavior (Casey & Lickliter, 1998; Rogers, 1982; Rogers & Bolden, 1991), hemispheric specialization (Casey & Martino, 2000; Casey, 2005; Rogers, 1982), and social behavior (Rogers, 1982). A few studies in domestic chicks have also shown that extended light exposure during embryogenesis can accelerate development of respiratory control (Bradley and Jahng, 2003), interlimb stepping prior to hatching (Ryu & Bradley, 2009; Sindhurakar & Bradley, 2012), and overground locomotion at hatching (Sindhurakar & Bradley, 2010). However, it has yet to be determined if this acceleration in motor development is associated with any immediate or longer term negative behavioral or other biological consequences.…”