Anatomical study of the neural ganglionated plexus in the canine right atrium: Implications for selective denervation and electrophysiology of the sinoatrial node in dog

Abstract

The aim of the present study was to elucidate the topography and architecture of the intrinsic neural plexus (INP) in the canine right atrium because of its importance for selective denervation of the sinoatrial node (SAN). The morphology of the intrinsic INP was revealed by a histochemical method for acetylcholinesterase in whole hearts of 36 mongrel dogs and examined by stereoscopic, contact, and electron microscopes. At the hilum of the heart, nerves forming a right atrial INP were detected in five sites adjacent to the right superior pulmonary veins and superior vena cava (SVC). Nerves entered the epicardium and formed a INP, the ganglia of which, as a wide ganglionated field, were continuously distributed on the sides of the root of the SVC (RSVC). The epicardiac ganglia located on the RSVC were differentially involved in the innervation of the sinoatrial node, as revealed by epicardiac nerves emanating from its lower ganglia that proceed also into the atrial walls and right auricle. The INP on the RSVC (INP-RSVC) varied from animal to animal and in relation to the age of the animal. The INP-RSVC of juvenile dogs contained more small ganglia than that of adult animals. Generally, the canine INP-RSVC included 434+/-29 small, 17+/-4 medium-sized, and 3+/-1 large epicardiac ganglia that contained an estimated 44,700, 6,400, and 2,800 neurons, respectively. Therefore, the canine right atrium, including the SAN, may be innervated by more than 54,000 intracardiac neurons residing mostly in the INP-RSVC. In conclusion, the present study indicates that epicardiac ganglia that project to the SA-node are distributed more widely and are more abundant than was previously thought. Therefore, both selective and total denervation of the canine SAN should involve the whole region of the RSVC containing the INP-RSVC.

Genesis and Regulation of the Heart Automaticity

“…Autonomic fiber projections to the heart rhythmogenic centers are abundant. The canine SAN is densely innervated by postganglionic fibers of the ICNP, which is formed by nerve fibers entering the epicardium and forming ϳ400 ganglia around the junction between the right atrium and the superior vena cava (384). Pauza et al (384) have estimated that the canine SAN can be innervated by more than 54,000 intracardiac neurons residing in the INP.…”

A combined acetylcholinesterase and immunohistochemical method for precise anatomical analysis of intrinsic cardiac neural structures

“…Chemical pre-fixation of the whole heart All hearts were cleared of blood using room temperature phosphate buffered saline (PBS, 0.01 M), consisting of (in mM): Na 2 HPO 4 , 8.06; NaH 2 PO 4 , 1.94; and NaCl, 137 (pH 7.4). Since the walls of both atria were flabby after perfusion, special handmade balloon-tip catheters inserted through the superior vena cava and left pulmonary veins into the both atrial chambers were utilized to distend the atria via an injection of saline into the balloon-tips of the catheters as previously reported (Pauza et al, 1999). Hearts were prefixed for 60 min using 4% formaldehyde solution in phosphate buffer (PB, 0.01 M, pH 7.4, 4 • C).…”

“…More importantly, this allows the comparison of immunohistochemical reaction intensity at specific time points following AChE staining. The remaining cardiac material was stained for AChE by immersion in a modified Karnovsky-Roots solution (Pauza et al, 1999) at 4 • C. The AChE staining solution contained (in mM): sodium acetate buffer, 60; acetylthiocholine iodide, 2; sodium citrate, 15; CuSO 4 , 3; K 3 Fe(CN) 6 , 0.5 (pH 5.6). Staining was monitored at 30/60 and 90 min by placing hearts into a clear custom-made Perspex chamber containing 4 • C PBS.…”

“…Currently, histochemical staining for acetylcholinesterase (AChE), as initially described by Karnovsky and Roots (1964), remains a popular method to visualize intrinsic nerves and ganglia in whole organs. In the heart, this method allows a distinct and permanent signal that has facilitated uncovering the entire epicardial intrinsic cardiac nervous system from a wide range of species (Pauza et al, 1999). For a complete profile of neurotransmitter content of the epicardial nerve network, detailed immunohistochemistry is essential.…”

Location and variability of epicardiac ganglia in human fetuses

“…From a number of neuroanatomically investigated mammalian species it is known that cardiac ganglia are mainly distributed on certain atrial regions around the sinuatrial node, at the roots of the vena cava and pulmonary veins, above and within the interatrial septum, in the proximity of atrioventricular node and, even in the auricular appendages (King and Coakley 1958;Navaratnam 1965;BojsenMoller and Tranum-Jensen 1971;Baptista and Kirby 1997;Pauza et al 1999Pauza et al , 2000Pauza et al , 2002aBatulevicius et al 2003Batulevicius et al , 2004Batulevicius et al , 2005. Structural organization of the intracardiac nerve plexus of the human and many animal models has been previously described using histological, histochemical and immunohistochemical methods (Bojsen-Moller and Tranum-Jensen 1971;Khabarova 1975;Stropus and Vaicekauskas 1978;Yuan et al 1994;Marron et al 1995;Singh et al 1996;Armour et al 1997;Pauza et al 1999Pauza et al , 2000Pauza et al , 2002aBatulevicius et al 2003Batulevicius et al , 2004Batulevicius et al , 2005Arora et al 2003;Jurgaitiene et al 2004;etc.).…”