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First published online July 14, 2008
Journal of Experimental Biology 211, 2371-2378 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.010587
Commentary |
New developments on gill innervation: insights from a model vertebrate
1 Department of Biology, University of Ottawa, Ottawa, ON, Canada, K1N 6N5
2 Department of Biology, McMaster University, Hamilton, ON, Canada, L8S
4K1
* Author for correspondence (e-mail: mjonz{at}uottawa.ca)
Accepted 28 May 2008
 |
Summary |
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 TOP Summary IntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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Key words: innervation, gill, neuroepithelial cell, NEC, mitochondria-rich cell, MRC, pseudobranch, zebrafish, oxygen sensing, ion regulation
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Introduction |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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) allows
labelling of the entire branchial nervous system.
Several pioneering histological and ultrastructural studies have
established the cellular morphology and innervation of the branchial
structures in fish, particularly those of Pierre Laurent and colleagues
(Laurent and Rouzeau, 1972;
Laurent and Dunel-Erb, 1984;
Dunel-Erb et al., 1982;
Dunel-Erb et al., 1989;
Bailly et al., 1989;
Bailly et al., 1992). However,
as it is not the goal of this Commentary, we will not attempt to review this
extensive body of work. The purpose of this Commentary is to briefly introduce
important concepts of nervous innervation of the fish gill to the
non-specialist reader and to highlight recent contributions in the field that
have made an impact on our current understanding of the functional
significance of this innervation. The present article will draw from selected
studies and reviews, as well as recent investigations by the authors that have
used confocal microscopy to map branchial innervation patterns in the
zebrafish, and indicate how these may provide insights into the fields of
oxygen sensing and ion regulation.
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Organization of the gills and branchial nerves |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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) and are differentiated to perform specialized homeostatic
functions in an aquatic environment (Fig.
1A). In teleost fish, each of four bilateral pairs of arches gives
rise to two parallel rows (hemibranchs) of gill filaments that are each
further subdivided into a series of secondary lamellae
(Fig. 1A,B). The filaments and
lamellae are covered by a thin epithelium composed of several cell types that
perform such processes as gas exchange, ion regulation, acid–base
balance and excretion (for a review, see
Evans et al., 2005). The gill
arches connect the ventral aorta to the paired dorsal aortae
(Fig. 1A,C). The heart,
therefore, pumps deoxygenated blood rostrally and dorsally for gas exchange
and other processes across the gill epithelium and for delivery of oxygenated
blood to tissues via the systemic circulation. Afferent and efferent
branchial arteries carry blood through the gill arches, while afferent and
efferent filament arteries carry blood to and from the lamellae, respectively
(Fig. 1B). Lamellar arterioles
allow passage of blood to a vascular sinus of the lamellae and back to the
filament arteries (Olson,
2002).
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The organization of gill innervation is discussed only briefly here, but
the reader is referred to other reviews
(Nilsson, 1984;
Sundin and Nilsson, 2002) for
a more detailed account. Eleven pairs of cranial nerves are found in fish.
These include the terminal (0), olfactory (I), optic (II), oculomotor (III),
trochlear (IV), trigeminal (V), abducens (VI), facial (VII), acoustic (VIII),
glossopharyngeal (IX) and vagus (X) nerves
(Nilsson, 1984;
Sundin and Nilsson, 2002). In
addition, the cranial nerves may carry somatic sensory, somatic motor,
visceral sensory or visceral motor fibres
(Nilsson, 1984;
Sundin and Nilsson, 2002).
However, only the facial, glossopharyngeal and vagus nerves innervate the gill
region and are therefore called the `branchial nerves'. In jawed fishes, such
as teleosts, the glossopharyngeal and vagus nerves primarily innervate the
gill arches and form large nerve trunks that enter the gill arches dorsally
(Fig. 1C). Branches of the
branchial nerves are further divided into pre-trematic (anterior) and
post-trematic (posterior) rami that straddle the gill slits
(Nilsson, 1984;
Sundin and Nilsson, 2002).
Thus, each gill arch is innervated by a post-trematic and pre-trematic ramus
from two different cranial nerve branches (see
Fig. 1C). Gill arches 2, 3 and
4 are innervated entirely by branches of the vagus nerve, while the first gill
arch is innervated by both the glossopharyngeal and vagus nerves
(Fig. 1C). In addition to
innervation of the gill arches (i.e. arches 1–4), a vestigial gill-like
structure, called the `pseudobranch', primarily receives innervation from the
pre-trematic branch of the glossopharyngeal nerve and may receive additional
innervation from the post-trematic branch of the more anterior facial nerve
(Laurent and Dunel-Erb, 1984;
Nilsson, 1984).
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Innervation of the gill filaments and secondary lamellae |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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). The
nerve bundle of the filament continues distally and runs adjacent to the
efferent filament artery (eFA). Furthermore, fibres of this nerve bundle give
rise to an extensive nerve plexus that wraps around the eFA, heavily
innervating the superficial and interlamellar regions of the filament, and
extends branches into the secondary lamellae
(Fig. 2B,C). Previous studies
have described nerve fibres of the gill filaments, including those identified
as adrenergic, cholinergic, nitrergic and peptidergic
(Donald, 1984;
Donald, 1987;
Dunel-Erb et al., 1982;
Dunel-Erb et al., 1989;
Bailly et al., 1989;
Bailly et al., 1992;
Sundin et al., 1998a;
Zaccone et al., 2006). Only
recently was innervation of the secondary lamellae characterized in zebrafish
with zn-12 (Jonz and Nurse,
2003), and similar nerve fibres of the lamellae were identified in
goldfish and catfish (Saltys et al.,
2006; Zaccone et al.,
2006). However, only minimal labelling of nerve fibres in the
lamellae of trout was observed with zn-12
(Saltys et al., 2006), and in
the tropical species traira and trairao no lamellar nerve fibres were observed
(Coolidge et al., 2008). This
suggests that innervation of the secondary lamellae in fish may be species
specific. The implications of the presence or absence of innervation in the
secondary lamellae are discussed further in a subsequent section, but these
species differences may be related to adaptation to different aquatic
environments or conditions, such as temperature, oxygen availability and
salinity.
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). This class of nerve fibre represents the majority of
innervation to the zebrafish gill and is summarized in
Fig. 3A. These experiments in
the zebrafish gill also indicated the presence of intrinsic innervation, i.e.
those nerve fibres whose parent cell bodies are located within the gill
filaments, and indicated the presence of three populations of intrinsic
neurons. These observations confirmed previous reports of intrinsic neurons in
teleosts (Bailly et al., 1989;
Sundin et al., 1998a). The
intrinsic innervation in the zebrafish gill is summarized in
Fig. 3B. Labelling of
whole-mount gill preparations in zebrafish with zn-12 revealed the presence of
two populations of neurons that were clustered near the proximal regions of
the filaments. These neurons are depicted in
Fig. 4 and are referred to as
`deep' or `superficial proximal neurons' (DPNs or SPNs) in zebrafish based on
their location relative to the eFA (Jonz
and Nurse, 2003). These proximal neurons in the filaments are
multipolar and have also been labelled with antibodies against the synaptic
vesicle protein SV2 (Fig.
4A,B). This antibody identifies a highly conserved protein of
synaptic vesicle membranes (necessary for neurosecretion) found in neurons and
other neurosecretory cells (Buckley and
Kelly, 1985). The significance of proximal neurons in
chemoreception, and potentially in the regulation of blood flow within the
gill, will be discussed in the following sections. A third group of intrinsic
neurons in zebrafish was reported and these cells are referred to as `chain
neurons' because of their apparent linear organization adjacent to the eFA
along the entire length of the gill filament
(Jonz and Nurse, 2003). A role
for these neurons has not been proposed, but the presence of distinct
varicosities along chain neuron fibres suggests that these bipolar neurons may
form synaptic connections with other structures. For example, in other
teleosts, intrinsic neurons innervate afferent lamellar arterioles and may
provide a means of vascular or hemodynamic control
(Bailly et al., 1989;
Dunel-Erb et al., 1989). All
three populations of intrinsic neurons in zebrafish have been shown to contain
synaptic vesicles and the neurotransmitter serotonin [5-hydroxytryptamine
(5-HT)] (Jonz and Nurse,
2003). In addition, serotonergic neurons in the gill filaments
have been previously described and appear to be typical in teleost fish
(Bailly et al., 1989;
Sundin et al., 1998a;
Sundin et al., 1998b;
Sundin and Nilsson, 2002).
Thus, the prevalence of this neurotransmitter in the cytoplasm of intrinsic
gill neurons suggests that release of 5-HT via neurosecretion from
these cells may play an important physiological role in the gill. For example,
it has been shown that exogenous application of 5-HT induced vasoconstriction
of the eFA and modified blood flow (Sundin
et al., 1995). Having now established the organization and innervation of the fish gill, the following three sections will discuss further the physiological significance of this innervation within the context of O2 sensing, vascular control during periods of hypoxia, and ion regulation.
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Role of innervation in O2 sensing |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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;
Nilsson and Sundin, 1998;
Burleson and Milsom, 2003). A
group of neurosecretory paraneurons, called neuroepithelial cells (NECs), are
found in the primary epithelium of the gill filaments, where they are exposed
to the incident flow of water over the gills during ventilation (see
Fig. 1B,
Fig. 5), and have long been
implicated in O2 chemoreception and respiratory regulation in fish
(Burleson and Milsom, 2003).
NECs store 5-HT in cytoplasmic synaptic vesicles near the plasma membrane
(Fig. 5) and have a morphology
and distribution that is highly conserved among fish
(Dunel-Erb et al., 1982;
Zaccone et al., 1994;
Zaccone et al., 1997;
Sundin et al., 1998a;
Jonz and Nurse, 2003;
Saltys et al., 2006;
Coolidge et al., 2008).
Experiments have demonstrated that gill NECs isolated from zebrafish respond
to hypoxia with K+ channel inhibition and membrane depolarization,
thus confirming their O2 sensitivity, and a cellular model for
O2 sensing in fish has been proposed where
Ca2+-dependent release of neurotransmitter results in activation of
postsynaptic sensory nerve fibres (Jonz et
al., 2004). Such a process would ultimately lead to a
physiological response to hypoxia, such as hyperventilation. Thus, because of
these morphological and physiological characteristics, NECs are strongly
believed to bear a phylogenetic relationship with mammalian
O2-chemoreceptors (see
González et al., 1994;
López-Barneo, 2001) and allow for O2 chemosensory responses
in the gill.
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The innervation of NECs in the gill filaments represents an important
feature of peripheral O2 chemoreception because it provides a
pathway through which the transmission of the cellular response to hypoxia may
occur from the periphery to other sites, such as the central nervous system
(CNS). Similarly, mammalian O2 chemoreceptors, such as the type I
cells of the carotid body and neuroepithelial bodies (NEBs) of the lung,
receive extensive innervation primarily from fibres of the glossopharyngeal
and vagus nerves, respectively
(González et al., 1994;
Cutz and Jackson, 1999). NEC
innervation has been verified at the ultrastructural level in teleosts
(Dunel-Erb et al., 1982;
Bailly et al., 1992) and has
more recently been studied using confocal microscopy in whole-mount gill
preparations (Jonz and Nurse,
2003; Saltys et al.,
2006), facilitating identification of entire populations of nerve
fibres and innervation patterns. These studies have shown that NECs of the
gill filaments receive innervation from both extrinsic and intrinsic sources
(see Fig. 3), indicating a
complex pattern of innervation. Since gill NECs retain both synaptic vesicles
and the neurotransmitter, 5-HT (Dunel-Erb
et al., 1982), they can be identified using antibodies against
these antigens. In zebrafish, gill NECs labelled with antibodies against 5-HT
or the synaptic vesicle protein SV2 are intimately associated with
zn-12-positive fibres of a nerve plexus that branches from a large nerve
bundle of the filament (Fig.
5). This indicates a putative sensory pathway through which NECs
stimulated by hypoxia may communicate with the nervous system. In addition,
NECs are positioned in a linear arrangement along a separate bundle of nerve
fibres that lies superficial to the eFA and originates from the superficial
proximal neurons (described in the previous section) near the filament base
(Fig. 3B). In zebrafish, these
fibres also make contact with NECs (Fig.
5A,B) (see Jonz and Nurse,
2003). Morphological evidence suggests that at least part of the
innervation to NECs is sensory, as would be required for O2
sensing, and indeed extracellular nerve recordings have identified sensory
fibres of the branchial nerves that increased their discharge during hypoxia
(Burleson and Milsom, 1993).
Early studies indicated that NECs in the trout gill were degranulated at the
ultrastructural level, suggestive of exocytosis, following exposure to hypoxia
(Dunel-Erb et al., 1982). In
zebrafish, synaptic vesicles were localized to the basal cytoplasm of NECs,
adjacent to nerve fibres, and a greater number of NECs devoid of a detectable
amount of 5-HT was found following chronic exposure to hypoxia, suggesting
hypoxic release of 5-HT (Jonz and Nurse,
2003; Jonz et al.,
2004). These morphological features may implicate the
neurosecretion of 5-HT induced by hypoxia and a sensory role for nerve fibres
that innervate NECs. Furthermore, in developing zebrafish, the correlation
between innervation of gill NECs and a significant rise in the
hyperventilatory response to hypoxia at 7 days post-fertilization (d.p.f.)
(Jonz and Nurse, 2005)
suggests that these nerves are indeed sensory. Therefore, in the case of
stimulation of gill NECs in fish during periods of hypoxic exposure, the
release of neurotransmitters from NECs following membrane depolarization would
potentially activate postsynaptic sensory nerve fibres and induce centrally
mediated changes in ventilation or heart rate via the extrinsic
neural pathway (Fig. 3A) or
lead to changes in gill vascular resistance via the intrinsic neural
pathway (Fig. 3B).
While there is a wealth of evidence indicating that NECs of the teleost
gill contain 5-HT (see above references), the neurotransmitter underlying
hypoxic signalling from NEC to sensory nerve fibre is currently unknown.
Several studies have indicated that other neurochemical candidates may include
nitric oxide or catecholamines (Zaccone et
al., 2006; Burleson et al.,
2006; Milsom and Burleson,
2007), and a variety of neuropeptides may also be involved (for
reviews, see Zaccone et al.,
1994; Zaccone et al.,
1997). It is conceivable that the neurochemical basis of
O2 sensing in the gill may involve multiple neurotransmitters or
neuropeptides and, perhaps, a diversity of excitatory, inhibitory and
modulatory mechanisms, as has been described in the mammalian
O2-sensing organ, the carotid body
(González et al., 1994;
Nurse, 2005;
Prabhakar, 2006;
Lahiri et al., 2006).
Interestingly, a variety of neurochemicals, such as acetylcholine, 5-HT and
dopamine, applied exogenously to the fish gill have been shown to have
stimulatory effects on sensory nerve fibres and cardiorespiratory reflexes
(Burleson and Milsom, 1995a;
Burleson and Milsom,
1995b).
Despite the evidence for afferent innervation, the possible contribution of
efferent nerve fibres to NEC innervation must also be considered. Many nerve
fibres associated with NECs of the zebrafish gill, especially the intrinsic
fibres, contain synaptic vesicles and may potentially release
neurotransmitters onto NECs (Jonz and
Nurse, 2003). In addition, serotonergic and nitrergic fibres in
the gill filaments contact NECs (Jonz and
Nurse, 2003; Zaccone et al.,
2006). These results may suggest an additional neuroendocrine role
for NECs in the gill, whereby NEC stimulation would result in local vascular
changes, or a role for efferent nerve fibres in modulating the chemosensory
response to hypoxia. Similarly, pulmonary NEBs receive afferent and efferent
innervation (Adriaensen and Scheuermann,
1993), and a mechanism of modulation of O2 sensing
via efferent glossopharyngeal nerve fibres has been described in the
mammal carotid body (Campanucci and Nurse,
2007).
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Role of innervation in vascular control during hypoxia |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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). Control of
vascular resistance in the gill is, therefore, of particular interest because
homeostatic processes, such as respiration, are dependent on haemodynamic
changes (Evans et al., 2005).
The autonomic and pharmacological control of vascular changes within the gill
of several fish taxa has been extensively reviewed
(Nilsson, 1984;
Sundin and Nilsson, 2002;
Evans et al., 2005;
Zaccone et al., 2006), but
recent studies in zebrafish have identified potential roles for intrinsic and
extrinsic sources of innervation in vascular control and respiratory
regulation during hypoxic stress (Jonz and
Nurse, 2003). Interestingly, in zebrafish, the intrinsic proximal
neurons, which also send fibres distally to innervate
O2-chemoreceptive NECs (Fig.
5A,B), appear to be the same neurons that send fibres rich in
secretory vesicles proximally to terminate at a muscular segment at the base
of the eFA (Fig. 3B,
Fig. 4A,B)
(Jonz and Nurse, 2003). Such a
relationship between NECs and intrinsic neurons was previously proposed
(Bailly et al., 1992). This
evidence suggests that SPNs may mediate adjustments in vascular tone through
vasomotor control of the eFA during hypoxic stimulation of NECs. This putative
sensory pathway would indicate a mechanism of local neural control within the
gill and allow for modulation of gill blood flow without involvement of the
CNS. Innervation of the contractile segment of the eFA by filament neurons has
been previously described in other species and may operate through
serotonergic or cholinergic mechanisms
(Bailly et al., 1989;
Dunel-Erb et al., 1989).
Furthermore, vasoconstriction of the proximal region of the eFA appears to
occur during hypoxia (Sundin and Nilsson,
1997) and may contribute to the hypoxic increase in gill vascular
resistance observed in teleosts (Nilsson
and Sundin, 1998; Smith et
al., 2001). A subsequent elevation in lamellar perfusion pressure
may lead to a process known as `lamellar recruitment' that may underlie
perfusion of distal lamellae (which are apparently not normally utilized)
during periods of hypoxia to increase respiratory surface area and gas
exchange (Booth, 1978;
Booth, 1979;
Sundin and Nilsson, 1997). It
should be noted that since nitrergic and serotonergic nerve fibres in the
gills contact NECs (Jonz and Nurse,
2003; Zaccone et al.,
2006), a presynaptic role for these fibres cannot be ruled out.
Such a role may release stored neurochemicals from NECs, having an effect on
surrounding tissue, or modify the cellular response to hypoxia.
The discovery of a rich network of extrinsic nerve fibres in the secondary
lamellae in zebrafish (Jonz and Nurse,
2003) (Fig. 5)
suggests that other cell types of the lamellae in this and other species may
be innervated and under neural control, possibly affecting respiratory or
osmoregulatory functions of the gill. Pillar cells of the lamellae, which
provide structural support and allow deoxygenated blood to pass through the
vascular sinus, contain proteins that allow these cells to contract and
increase gill vascular resistance (Smith
and Chamley-Campbell, 1981;
Stensløkken et al.,
1999; Mistry et al.,
2004). If extrinsic nerve fibres of the lamellae contact pillar
cells, this innervation may allow for pillar cell contraction and provide a
mechanism by which blood flow through the respiratory lamellae could be
rapidly adjusted by the CNS as needed during changes in ambient or arterial
O2.
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Do branchial nerves contribute to ion regulation? |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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). The gill is a major site of osmotic and ion regulation in
fish, and the primary functional unit of ion regulation in the teleost gill is
the mitochondria-rich cell (MRC). MRCs are located in the interlamellar region
of the gill filament epithelium (Fig.
6A) and are specialized for ion transport. These cells are
characterized by a high density of mitochondria, an abundance of the enzyme
Na+/K+-ATPase and a complement of ion channels,
exchangers and pumps (Perry,
1997; Wilson and Laurent,
2002; Evans et al.,
2005). In freshwater teleosts, they mediate Na+,
Ca2+ and Cl– uptake across the epithelium into the
blood, while in saltwater teleosts MRCs (also called `chloride cells') mediate
ion extrusion (Perry, 1997;
Marshall, 2002;
Evans et al., 2005).
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The control of ionoregulatory mechanisms by the gill is a vibrant field of
research, but this process is not completely understood. The movement of ions
across gill or opercular epithelia appears to be mediated by circulating
hormones and neurotransmitters (McCormick,
2001; Evans, 2002;
Marshall, 2003), and evidence
has accumulated suggesting that ion transport by MRCs may be under neural
control. Nerve stimulation in isolated gill and opercular membrane
preparations has been shown to result in alterations in Ca2+ and
Cl– flux across epithelia
(Donald, 1989;
Marshall et al., 1998). In
addition, earlier studies demonstrated that cutting the branchial nerves
produced a depletion of gill MRCs and altered ion transport and water
permeability (Pequignot and Gas,
1971; Mayer-Gostan and Hirano,
1976), suggestive of MRC innervation and neural control. A more
recent study used confocal immunofluorescence techniques and provided
morphological evidence for such innervation of MRCs in zebrafish
(Fig. 6A)
(Jonz and Nurse, 2006). MRCs
of the efferent filament epithelium appeared to make contact with only
extrinsic fibres derived from the nerve plexus of the filament, which would
indicate the presence of a mixed nerve supply in the gill since similar fibres
also innervate O2-chemoreceptive NECs. Developmental studies using
zebrafish showed that gill filament primordia receive innervation as early as
3 d.p.f., but the site of termination of these fibres was not determined at
this stage (Jonz and Nurse,
2005). However, nerve fibres in zebrafish larvae were found to
make contact with MRCs as early as 5 d.p.f.
(Jonz and Nurse, 2006),
suggesting that ion regulatory neural pathways may be established in the gill
during larval development before O2-chemosensory pathways, which
occur at 7 d.p.f. These results were consistent with an earlier study that
reported that the gills are needed for ion regulation before they are
functional as respiratory organs
(Rombough, 2002).
While MRC innervation has not been investigated in other species,
collectively, the above studies point to the neural control of ion regulation
in the gill. Similarly, the neural control of ion homeostasis in the mammalian
kidney is well established (DiBona and
Kopp, 1997). Nerve fibres in the fish gill are associated with the
basolateral regions of MRCs (Fig.
6A), where Na+/K+-ATPase activity is
localized (Evans et al.,
2005), and apical regions of MRCs are positioned toward the
external environment. This may suggest that putative presynaptic nerve
terminals release neurochemicals to influence the activity of membrane-bound
ion channels, or other intracellular processes of postsynaptic MRCs, thereby
controlling ion regulation across the gill epithelium. Neurotransmitters and
neuropeptides, such as catecholamines, acetylcholine, nitric oxide, vasoactive
intestinal polypeptide, endothelin and prostaglandins, have been shown to
mediate the movement of ions across gill and opercular epithelia, and
stimulation of Cl– extrusion is mediated by adrenergic
receptors (Evans, 2002;
Marshall, 2003;
Evans et al., 2004).
Although evidence appears to suggest efferent innervation of MRCs, sensory
innervation of these cells must also be considered. Evidence suggests the
presence of ionoreceptors in fish that are sensitive to changes in plasma ion
concentration that may elicit rapid ion transfer during adaptation to salinity
change (Evans et al., 2005;
Marshall et al., 2005).
Moreover, sensory receptors and afferent innervation of transport epithelia in
the mammalian kidney have been described, including nerve fibres near the
renal tubules and vagal innervation
(DiBona and Kopp, 1997).
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The pseudobranch |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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)]. While pseudobranch structure is variable
between fish species, it resides within the cranial portion of the opercular
epithelium, where it is not exposed to the external environment, and its
primary cellular component is that of the pseudobranch cell (PBC). These cells
are characterized by apical localization of the enzyme
Na+/K+-ATPase and an extensive cytoplasmic tubular
network (Fig. 6B;
Laurent and Dunel-Erb, 1984;
Quinn et al., 2003;
Jonz and Nurse, 2006). Early
studies investigating the function of the pseudobranch suggested that it may
act as a gland, a sensory organ involved in O2 chemoreception, or
take part in osmoregulation (Laurent and
Rouzeau, 1972; Laurent and
Dunel-Erb, 1984). It was recently concluded, however, that the
hypoxic release of catecholamines from chromaffin cells mediated by
O2 chemoreceptors did not involve the pseudobranch in trout
(Reid and Perry, 2003), and
only one or two 5-HT-containing cells resembling O2-sensitive gill
NECs were found in each pseudobranch filament in zebrafish
(Jonz and Nurse, 2003). Thus,
it would seem unlikely that the pseudobranch plays any significant role in
O2 sensing, at least in these species. Other recent evidence has
suggested that PBCs supply O2 to the retina and regulate blood pH
(Bridges et al., 1998;
Kern et al., 2002) and that a
role for these cells in osmoregulation, if any, is limited
(Quinn et al., 2003).
Most striking, however, is the extensive innervation found in the
pseudobranch and the fact that the physiological significance of this
innervation has not yet been determined. Pseudobranch innervation was
characterized at the ultrastructural level
(Laurent and Dunel-Erb, 1984)
and, more recently, in zebrafish with confocal microscopy
(Jonz and Nurse, 2006). In
zebrafish, PBCs are densely packed within the fused lamellae and are
innervated by a rich network of nerve fibres that arise from supportive
filaments (Jonz and Nurse,
2006). There is evidence that the teleost pseudobranch receives
afferent innervation (Laurent and Rouzeau,
1972; Laurent and Dunel-Erb,
1984), but similar nerve fibres in zebrafish are immunopositive
for the synaptic vesicle protein SV2 (Jonz
and Nurse, 2003), suggesting a neurosecretory or efferent role of
these fibres. Moreover, since innervation of PBCs occurs apically, rather than
basolaterally (Laurent and Dunel-Erb,
1984; Jonz and Nurse,
2006), the physiological significance of these cells would appear
to be limited to internally oriented functions that may take place between the
basolateral membrane and the vasculature, such as hormone secretion or
chemical sensing of the blood. While the precise function of the pseudobranch
and its component cells is currently speculative, further study of the nature
of PBC innervation may reveal significant clues about the role of this
potentially important organ in fish.
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Conclusions and remaining questions |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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Use of the zebrafish as a model system may facilitate studies designed to
solve the above outstanding issues. Whole-mount preparation of gill tissue
coupled with confocal microscopy has allowed complete morphological
characterization of several cell types and innervation patterns in this
species. Moreover, with a growing number of commercially available antibodies,
mutants and the advent of gene knockdown in zebrafish embryos by morpholino
injection (Heasman, 2002), a
more complete physiological and molecular characterization of gill innervation
may be just around the corner.
List of abbreviations and glossary
)
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Acknowledgments |
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References |
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TOPSummaryIntroductionOrganization of the gills...Innervation of the gill...Role of innervation in...Role of innervation in...Do branchial nerves contribute...The pseudobranchConclusions and remaining...References |
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