Embryonic control of heart rate: Examining developmental patterns and temperature and oxygenation influences using embryonic avian models

Long-term measurements (days and weeks) of heart rate (HR) have elucidated infradian rhythms in chicken embryos and circadian rhythms in chicken hatchlings. However, such rhythms are lacking in emu embryos and only rarely observed in emu hatchlings. Parasympathetic control of HR (instantaneous heart rate (IHR) decelerations) occurs at ∼60% of incubation in both precocial and altricial avian embryos, with sympathetic control (IHR accelerations) becoming more prevalent close to hatching. A large increase in avian embryonic HR occurs during hatching (presumably an energetically expensive process, i.e. increased oxygen consumption (Ṁ_O2)), beginning during pipping when a physical barrier to O₂ conductance is removed. Alterations in ambient O₂ have little effect on early embryonic HR, likely due to the low rate of Ṁ_O2 of early embryos and the fact that adequate O₂ delivery can occur via diffusion. As Ṁ_O2 increases in advanced embryos and circulatory convection becomes important for O₂ delivery, alterations in ambient O₂ have more profound effects on embryonic HR. Early embryos demonstrate a wide ambient temperature (T_a) tolerance range compared with older embryos. In response to a rapid decrease in T_a, embryonic HR decreases (stroke volume and blood flow are preserved) in an exponential fashion to a steady state (from which it can potentially recover if re-warmed). A more severe decrease in T_a results in complete cessation of HR; however, depending on developmental age, embryos are able to survive severe cold exposure and cessation of HR for up to 24 h in some instances. The development of endothermy can be tracked by measuring baseline HR during T_a changes. HR patterns change from thermo-conformity to thermoregulation (reverse to T_a changes). Further, IHR low frequency oscillations mediated by the autonomic nervous system are augmented at low T_as in hatchlings. Transitions of baseline HR during endothermic development are unique to individual avian species (e.g. chickens, ducks and emu), reflecting differences in life history.