Histochemistry (1991) 95:397-402
030155649100025Q
Histochemistrv
© Springer-Verlag 1991 ~
The innervation of the gastrointestinal tract of a chelonian reptile,
Pseudemys scripta elegans
I. Structure and topography of the enteric nerve
plexuses using neuron-specific enolase immunohistochemistry*
J.-P. Timmermans 1, D.W. Scheuermann 1, R. Gabriel 2, D. Adriaensen 1, E. Fekete 2,
and M.H.A. De Groodt-LasseeP
1 Institute of Histology and Microscopic Anatomy, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium
2 Department of Zoology, Jozsef Attila University, Sz6ged, Hungary
Accepted November 12, 1990
Summary. The general morphological features of the in-
tramural enteric nervous system of a chelonian species,
i.e. the red-eared turtle, Pseudemys scripta elegans, has
been studied in whole-mounts and cryosections by
means of neuron-specific enolase immunohistochemis-
try. A clear visualization of both neuronal cell bodies
and nerve fibres allows the recognition of a myenteric
plexus as well as a submucous plexus in several gut re-
gions, namely the stomach, midgut and hindgut. The
highest innervation density was found in the midgut por-
tion. In contrast to other lower vertebrates, such as am-
phibians and other reptilian groups, the present study
clearly demonstrates the occurrence of neuronal cell
bodies in the submucous plexus of all regions investigat-
ed. The neurons stained for neuron-specific enolase har-
boured smooth-contoured perikarya from which one or
more processes emerge, as demonstrated for the mam-
malian enteric nervous system.
Introduction
Heretofore, the knowledge of the general morphology
of the enteric nervous system (ENS) is mainly deduced
from studies on mammals. These are small laboratory
animals (for review see Gabella 1979; Furness and Costa
1987), larger mammals (Gunn 1968; Stach 1977a, b,
1989; Mannl etal. 1986; Scheuermann etal. 1989a;
Timmermans et al. 1989, 1990), and man (Hoyle and
Burnstock 1989). In 1933 Kondratjew briefly com-
mented on the presence of a submucosal nerve network
in a turtle. Other, more recent, studies on the intramural
innervation of the reptilian gastrointestinal tract dealt
exclusively with such restricted topics as the demonstra-
tion of adrenergic nerve fibres in the large intestine of
a lizard (Read and Burnstock 1968), of bombesin immu-
* Supported by grant no. 3.0005.89 (to D.W.S.) from the Fund
for Medical Scientific Research (Belgium)
Offprint requests to: D.W. Scheuermann
noreactivity in the gut of a caiman (Holmgren et al.
1989), of VIP-immunoreactivity in the small intestine
of a viper (Masini 1986) and of a number of regulatory
peptides in the gastrointestinal tract of an alligator (Bu-
chan et al. 1983). None of these investigations, however,
discuss the general morphological features of the differ-
ent enteric nerve networks in the reptiles studied.
In the last decade, the study of the architecture and
the structure of the ENS of lower vertebrates (for review
see Nilsson and Holmgren 1989) and of some inverte-
brates (Gabriel et al. 1988) has proved to be valid from
an evolutionary and functional point of view because
of the considerably lower number of intrinsic neurons
involved. From a comparative morphological viewpoint,
it is rather surprising that the reptiles, and in particular
the chelonians, have been ignored so far. The present
study offers the first extensive description of the archi-
tecture and the topographical organization of the ENS
of a chelonian species, i.e. the red-eared turtle, Pseu-
demys scripta elegans, by means of immunocytochem-
istry using an antiserum raised against neuron-specific
enolase (NSE).
Materials and methods
Specimens of both sexes of the red-eared turtle, Pseudemys scripta
elegans, weighing 10-400 g, were obtained from the Antwerp Zoo-
logical Garden and from commercial dealers. The animals were
fed ad libitum. Anesthesia was performed by an intraperitoneal
injection of Nembutal (30 mg/kg body weight).
Segments from several regions of the gastrointestinal tract,
i.e. the stomach, midgut and hindgut, were prelevated, ligated and
filled with phosphate buffered saline (PBS). The samples were then
immersed in 4% paraformaldehyde containing 0.2% picric acid
in phosphate buffer (pH = 7,2 ; 0.01 M) for 2 h at room temperature
and subsequently processed as described earlier (Scheuermann
et al. 1987). Accordingly, the whole-mount preparations contained
either (1.) the tela submucosa or (2.) the tela submucosa with the
circular muscle layer and the adhering myenteric plexus or (3.)
the longitudinal muscle layer with the adhering myenteric plexus.
The tissues were preincubated in 10% normal donkey serum (017-
000-121, Jackson Immunoresearch Laboratories) for 30 min, fot-