Phylogenetic investigation of Dogiel's pericellular nests and Cajal's initial glomeruli in the dorsal root ganglion

Seiji Matsuda, Naoto Kobayashi, Takehiro Terashita, Tetsuya Shimokawa, Kazuhiro Shigemoto, Katsumi Mominoki, Hiroyuki Wakisaka, Shouichiro Saito, Kyoujy Miyawaki, Kyoko Saito, Fumiki Kushihata, Jie Chen, Shuang Yan Gao, Chun Yu Li, Min Wang, Takashi Fujiwara

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12 Citations (Scopus)

Abstract

Cajal's initial glomeruli (IG) and Dogiel's pericellular nests (PCNs) were first described from methylene blue preparations of healthy animal tissues around the beginning of the last century. Since that time, although many reports have been published concerning these structures, few have focused on their development and phylogeny in healthy animals. The aim of this study was to examine the phylogenetic development of the sensory neurons in Cajal's IG (also called axonal glomeruli) and Dogiel's PCNs in the dorsal root ganglion (DRG) of the healthy adult frog, chick, rat, and rabbit. The three-dimensional architecture of the neurons was observed in ganglia by scanning electron microscopy after removal of the connective tissue. The neurons in the DRG of fish are known to be bipolar, but DRG neurons in the species examined here were found to be pseudounipolar, with single stem processes. The proportion of neurons having IG or PCNs increased with increasing phylogenetic complexity in the species examined here. Cajal's initial glomeruli, the convolution of the stem process near the parent cell body: In frogs, the ganglia were small and the neuronal stem processes were very short and straight. In chicks, the stem processes were longer; sometimes very long, tortuous processes were observed. However, no neurons with typical IG were observed in either species. Typical IG were observed in rats and rabbits; their occurrence was much more frequent in rabbits. Pseudounipolarization, i.e., the transition from bipolar to pseudounipolar neurons, is thought to save space, limit the length of neuronal processes, and reduce conduction time. However, an explanation of the evolutionary advantage of the IG, which is formed by the excessive prolongation of the stem process, remains elusive. The cytological and electrophysiological importance of IG has been discussed. Dogiel's pericellular nests (PCNs), which resemble balls of yarn made of thin unmyelinated nerve fibers around DRG neurons, have been observed in the DRG of rats and rabbits, but not in frogs or chicks. This interesting structure shows not only ontogenetic development in healthy animals but also phylogenetic development among species. The nerve fibers in the PCNs were less than 1.2 μm in diameter and had some varicosities. An immunohistochemical study using anti-tyrosine hydroxylase (TH) antibody revealed that some PCNs contain TH-positive nerve fibers and varicosities. Such TH-positive PCNs disappear after sympathectomy. These results suggest that the PCNs are made up of autonomic nerve fibers.

Original languageEnglish
Pages (from-to)234-245
Number of pages12
JournalJournal of Comparative Neurology
Volume491
Issue number3
DOIs
Publication statusPublished - Oct 24 2005

Keywords

  • Differentiation
  • Phylogeny
  • Scanning electron microscopy
  • Sensory ganglia
  • Spinal ganglia

ASJC Scopus subject areas

  • Neuroscience(all)

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    Matsuda, S., Kobayashi, N., Terashita, T., Shimokawa, T., Shigemoto, K., Mominoki, K., Wakisaka, H., Saito, S., Miyawaki, K., Saito, K., Kushihata, F., Chen, J., Gao, S. Y., Li, C. Y., Wang, M., & Fujiwara, T. (2005). Phylogenetic investigation of Dogiel's pericellular nests and Cajal's initial glomeruli in the dorsal root ganglion. Journal of Comparative Neurology, 491(3), 234-245. https://doi.org/10.1002/cne.20713