Cartography of human diaphragmatic innervation: Preliminary data

Abstract

In humans, anatomy indicates that the phrenic nerve mainly arises from the C4 cervical root, with variable C3 and C5 contributions. How this translates into functional innervation is unknown. The diaphragm response to electrical stimulation of C3, C4 and C5 was described in three patients undergoing surgical laryngeal reinnervation with an upper phrenic root (surface chest electrodes at anterior, lateral and posterior sites; oesophageal and gastric pressures (Pes and Pga) to derive transdiaphragmatic pressure (Pdi)). Anatomically, the phrenic nerve predominantly originated from C4. Phrenic stimulation elicited motor responses at the three sites in the three patients, as did C4 stimulation. It produced Pdi values of 9, 11, and 14 cm H₂O in the three patients, respectively, vs. 9, 9, and 7 cm H₂O for C4. C3 stimulation produced modest Pdi responses, whereas C5 stimulation could produce Pdi responses close to those observed with C4 stimulation. These singular observations confirm the dominance of C4 in diaphragm innervation but suggest than C5 can be of importance.

Introduction

Embryologically, the mammalian diaphragm originates in cervical somites. During development and together with the lungs, it migrates caudally to its ultimate location in the thorax. This accounts for the cervical origin of its innervation. Indeed, the phrenic nerve which provides the diaphragmatic motor innervation arises from cervical spinal segments C3–C7, depending on species. The corresponding somatotopic organisation—namely how the cervical roots distribute to the anterior, lateral and posterior regions of the diaphragm—has been described in the rat (C4–C6 in Gottschall and Gruber, 1977), the rabbit (C4–C6 in Marie et al., 1997b, Marie et al., 1999), the cat (C4–C6 in Sant’Ambrogio et al., 1963) and the dog (C5–C7 in De Troyer et al., 1982, Marie et al., 2006). In humans, abundant anatomical data indicate that the phrenic nerve is mainly constituted from a C4 component, with variable contributions of C3 and C5 (Hovelacque, 1927, Rajanna, 1947, Hidayet et al., 1974). How each of these roots innervates the human diaphragm topographically and quantitatively has not been described. This distribution can have both physiological and clinical implications, for example, regarding the use of cervical roots for reinnervation purposes or the consequences and management of spinal cord injuries. In this frame, we herein describe the diaphragm response to electrical stimulation of the C3, C4 and C5 cervical roots in three patients undergoing surgical laryngeal reinnervation.