Confocal imaging and phylogenetic considerations of the
subcutaneous neurons in the Atlantic hagfish Myxine
glutinosa
Giacomo Zaccone,
1
Douglas S. Fudge,
2
Timothy M. Winegard,
2
Gioele Capillo,
1
Michal Kuciel,
3
Kengo Funakoshi
4
and Eugenia Rita Lauriano
1
1
Department of Environmental Science,
Territory, Food and Health Security
(S.A.S.T.A.S.), Viale Stagno d’Alcontres
31, I-98166, Messina, Italy;
2
Department
of Integrative Biology, University of
Guelph, Guelph, ON, N1G-2W1,
Canada;
3
Department of Comparative
Anatomy, Institute of Zoology, Jagiellonian
University, Gronostajowa 9, 30-387,
Krakow, Poland;
4
Department of Neuro-
anatomy, Yokohama City University
School of Medicine, 22-2 Seto, Kanazawa
Ward, Yokohama, Kanagawa Prefecture
236-0027, Japan
Keywords:
subcutaneous neurons, slime glands, striated
muscle, confocal immunohistochemistry,
hagfish, phylogeny
Accepted for publication:
19 December 2013
Abstract
Zaccone, G., Fudge, D.S., Winegard, T.M., Capillo, G., Kuciel, M.,
Funakoshi, K. and Lauriano, E.R. 2014. Confocal imaging and phylogenetic
considerations of the subcutaneous neurons in the Atlantic hagfish Myxine
glutinosa.— Acta Zoologica (Stockholm) 00: 000–000.
We used confocal microscopy and immunohistochemistry to characterize the
morphology of the subcutaneous neurons and the innervation of the slime
glands and striated muscles in the hagfish Myxine glutinosa. A rich plexus of
5HT-, ChAT- and TH-positive neurons is described in the capsule of the
slime glands. These neurons, like those of the subcutaneous plexus, receive
pericellular terminations from the axons of central cells. Capsular neurons
receive innervation from 5HT-positive and nNOS-positive nerve fibres. Other
nerve endings belonging to two separate nerve populations are identified in
the striated muscles. They contain TH and nNOS immunoreactivity. Due to
the lack of any topographical labelling, the cell origin and the projections of
the neurons into the cranial and spinal nerves are unknown. This study pro-
vides anatomical evidence of multiple (5HT and nNOS) peripheral innerva-
tion of the neurons. However, it does not provide information about the
function of these neurons in the hagfish. We suggest that hagfish neurons have
a phylogenetic relationship with the spinal group of the dorsal cells of lam-
preys and the supramedullary cells of teleosts.
Giacomo Zaccone, Department of Environmental Science, Territory, Food and
Health Security (S.A.S.T.A.S.), Viale Stagno d’Alcontres 31, I-98166 Messina,
Italy. E-mails: gzaccone@unime.it; gioelecapilo@hotmail.it;
elauriano@unime.it
Introduction
Cyclostomata comprise the living jawless fishes, hagfishes and
lampreys. Morphological and molecular studies indicate that
hagfishes and lampreys are sister groups, the Cyclostomata
itself being a sister group to the vertebrates. Within Cyclosto-
mata, hagfishes are less evolved than lampreys and constitute
the most primitive craniates available for study (Forey and
Janvier 1993; Mallat et al. 2001; Zardova and Meyer 2001).
In the myotomes of hagfishes, two muscle fibre types are
arranged in a characteristic sandwich pattern. The two fibre
types differ in size, myofibrillar array, blood supply and inner-
vation (Bone 1989). In gnathostomatous fish, the sympathetic
chains are generally well developed, their arrangement resem-
bling that found in the tetrapods. A unique feature in teleosts
and holosteans is that the cephalic portions of the sympathetic
chains that continue into the head bear ganglia in connection
with the glossopharyngeal and vagus nerves. The connections
between the ganglia and the cranial nerves are solely com-
posed of postganglionic fibres (grey rami communicantes)
(Kapoor and Khanna 2004).
An interesting and puzzling feature of the innervation of
myotomes in Cyclostomata is that lampreys have a dual
innervation of muscle fibres whereas hagfishes are innervated
by a single axon type. Hagfishes and lampreys differ in mus-
cle innervation and in the shape of the muscle fibres, the
© 2014 The Royal Swedish Academy of Sciences 1
Acta Zoologica (Stockholm) doi: 10.1111/azo.12068