Developing innervation of the chick heart: A histofluorescence and light microscopic study of sympathetic innervation

Abstract

The available descriptions of the development of sympathetic innervation of the chick heart conflict with the known sympathetic innervation of the adult chicken heart. The adult heart is innervated by bilateral sympathetic cardiac nerves originating from the first thoracic sympathetic ganglia. These nerves travel lateral and anterior to the lung and join the vagi just before entering the pericardium along the great vessels. Using catecholamine histofluorescence techniques and silver preparations, we have observed the development of the sympathetic cardiac nerves. The sympathetic cardiac nerves arise from the first thoracic sympathetic ganglia on the 7th day of incubation. They grow lateral and then ventral to the developing lungs to join the vagi, and are found in the bulbar region of the heart and atrium on the 10th day of incubation. FLuorescent cells without processes mark the course of the sympathetic cardiac nerves and are present in the bulbar region on the 10th day and thereafter. Sympathetic ganglion cells lose their fluorescence between day 8 and day 16 of incubation. This is presumably due to dilution of the transmitter in the rapidly increasing volume of cytoplasm in the sprouting neurons. Small intensely fluorescent (SIF) and adrenal medullary cells do not undergo a diminution of fluorescence during this period. SIF cells appear well differentiated at 16 days.

Systematic and comparative morphologies of the extrinsic cardiac nervous system in lemurs (Primates: Strepsirrhini: Infraorder Lemuriformes, Gray, 1821) with evolutionary morphological implications

“…The parasympathetic vagal cardiac system and its cardiac branches are consistent among primates. Interestingly, the comparative anatomical findings of the variable sympathetic and constant parasympathetic ECNSs in primates are similar to the mammalian ontogeny of cardiac innervation; however, the sympathetic cardiac innervation has been shown to occur at later stages than the parasympathetic vagal cardiac innervation (Kirby et al, 1980;Shoba and Tay, 2000;Hildreth et al, 2009).…”

“…Experimental and developmental studies of the autonomic cardiac nervous system have also been conducted in animals such as the mouse, rat, rabbit, chick, and dog (Armour et al, 1972;Benítez et al, 1959;Brack et al, 2011;Gomez, 1958;Haws and Burgess, 1978;Hildreth et al, 2008Hildreth et al, , 2009Kirby et al, 1980;Kuratani et al, 1991;Kuratani and Tanaka, 1990;Levy et al, 1966;Mabe and Hoover, 2011;Meyer et al, 2010;Mizeres, 1955Mizeres, , 1957Mizeres, , 1958Mizuno et al, 2010;Oliveira et al, 2010;Roberts, 1991;Schwartz, 2010;Scherlag et al, 2011;Shaner, 1930;Shoba and Tay, 2000;Uchida et al, 2010;Verberne et al, 1998). However, huge differences in the cardiac nervous system between humans and the experimental animals have been recognized (Batulevicius et al, 2003;Brugnaro et al, 2003;Kawashima, 2011;McKibben and Getty, 1968;Rysevaite et al, 2011;Pauza et al, 2002a,b).…”

Comparative Anatomy and Evolution of the Cardiac Innervation in New World Monkeys (Platyrrhini, E. Geoffroy, 1812)

“…In the mouse, the parasympathetic vagal nerves are first seen in the venous porta at E10.5 (10.5 days after fertilization, equivalent to HH20 in the chick) and reach the heart by E12.5 (HH24), whereas the innervation of the outflow (arterial porta) occurs slightly later than seen in the chick (Hildreth et al, 2008). The sympathetic cardiac innervation has been shown to occur at later stages than the parasympathetic vagal cardiac innervation in both avian and mammalian species (Kirby et al, 1980;Shoba and Tay, 2000;Hildreth et al, 2009). …”

“…The mammalian and avian ontogenetic developmental studies of the ACNS are detailed in a number of papers (Kirby et al, 1980;Kuratani and Tanaka, 1990;Verberne et al, 1998;Shoba and Tay, 2000;Hildreth et al, 2008Hildreth et al, , 2009). In the chick, the innervation of the outflow tract (arterial porta) by the parasympathetic cardiac branches occurred between stages 28 and 29 of Humburger and Hamilton (HH), whereas the positive HNK1 staining is first observed at the 24th stage and reaches the venous sinus by the 26th stage, and further vagal cardiac branches develop (Kuratani and Tanaka, 1990;Verberne et al, 1998;Hildreth et al, 2009).…”

Developmentally regulated neural protein EAP‐300 is expressed by myocardium and cardiac neural crest during chick embryogenesis

“…ral tube along pharyngeal arches 3, 4, and 6 , where they provide support for the endothelium and smooth muscle lamina of the aortic arch arteries (Bockman et al, 1989;Miyagawa et al, 1989). Some cells migrate from the pharyngeal arches into the outflow tract, where they contribute to the aorticopulmonary septum, seed the cardiac ganglia, or populate the truncal cushions that differentiate into the ventricular valves and septum (Kirby et al, 1980Sumida et al, 1990). Such populations appear critical to normal septation of the cardiac outlet, since extirpation or ablation of the cardiac neural crest from the neuroectoderm results in ventricular septal defects and persistent truncus arteriosus (Nishibatake et al, 1987).…”