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
New developments on gill innervation: insights from a model vertebrate
Michael G. Jonz1,* and
Colin A. Nurse2
1 Department of Biology, University of Ottawa, Ottawa, ON, Canada, K1N 6N5
2 Department of Biology, McMaster University, Hamilton, ON, Canada, L8S
4K1
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Fig. 1. Schematic representation of the gill arches, pseudobranch and their
innervation. (A) Ventral view of the organization of the gill arches (numbers
1 to 4) and pseudobranch (PB) in teleosts. VA, ventral aorta; DA, dorsal
aortae. Based on Weichert (Weichert,
1967 ). (B) Illustration of the organization of gill filaments and
lamellae in a typical teleost fish. Large arrows indicate the flow of water
through the gills, and small arrows indicate the flow of blood. aFA, afferent
filament artery; eFA, efferent filament artery; F, filament; L, lamellae.
(Modified from Jonz et al.,
2004.) (C) Left lateral view of the nerve supply to the gill
arches and pseudobranch from cranial nerves (VII, IX and X). Branchial
structures are innervated by postganglionic divisions (red) of pre-trematic
(pr) and post-trematic (po) rami.
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Fig. 2. Innervation of the filament and lamellae of the zebrafish gill, as
indicated by zn-12 confocal immunohistochemistry. (A) zn-12-immunoreactive
nerve trunks (arrows) of the gill arch (GA) extend fibres (arrowheads) into
the filaments (F) and lamellae (L). Scale bar, 50 µm. Modified from
(Jonz and Nurse, 2003). (B)
Higher magnification confocal image showing a nerve bundle (arrow) of the
filament and nerve fibres (arrowheads) of the lamellae in zebrafish gill.
Scale bar, 10 µm. (C) Image in B tilted back 90° showing that the nerve
bundle of the filament sends fibres that wrap around the efferent filament
artery (eFA) to innervate the filament and lamellar epithelium.
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Fig. 3. (A) Summary of extrinsic innervation of the zebrafish gill illustrating
formation of a nerve bundle composed of nerve fibres emanating from the BN of
the gill arch that gives rise to a nerve plexus surrounding the eFA. Fibres of
the nerve plexus associate with NECs (green) and MRCs (blue) and extend out to
the respiratory lamellae (indicated by arrows). (B) Intrinsic innervation
showing nerve endings of SPNs and DPNs terminating at the base of the eFA, and
extension of SPN and DPN nerve fibres towards NECs and ChNs (with varicose
processes), respectively. BN, branchial nerve; eBA, efferent branchial artery;
eFA, efferent filament artery; ChN, chain neuron; DPN, deep proximal neuron;
MRC, mitochondria-rich cell; NEC, neuroepithelial cell, SPN; superficial
proximal neuron. (Modified from Jonz and
Nurse, 2003.)
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Fig. 4. Intrinsic neurons at the proximal region of the gill filaments in zebrafish
innervate the base of the efferent filament artery. Confocal imaging was
performed using antibodies against the synaptic vesicle protein SV2. (A)
Multipolar superficial proximal neurons (SPNs) and deep proximal neurons
(DPNs) extend processes towards the base of the efferent filament artery
(eFA), where SV2-immunoreactive nerve endings (arrowheads) are found.
Extrinsic nerve terminals surrounding the efferent branchial artery (eBA) are
also visible. Scale bar, 20 µm. (B) Image in A rotated 70° depicting
SPNs and DPNs as two distinct neuronal groups. Note the shape of the eFA
outlined by SV2-positive nerve terminals. (Modified from
Jonz and Nurse, 2003.)
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Fig. 5. Confocal imaging of neuroepithelial cells (NECs) and associated innervation
of the gill filaments and lamellae in zebrafish. NECs were labelled with
antibodies against 5-hydroxytryptamine (5-HT; green) and SV2 (red in A; red or
yellow in B), and nerve fibres were identified by zn-12 immunoreactivity
(red). (A) SV2-positive NECs (arrows) were found in the filament (F) and
received innervation from intrinsic nerve fibres (iNF) and a plexus of
extrinsic nerve fibres (eNF). Extrinsic nerve fibres were also found in the
lamellae (L). Scale bar, 20 µm. (B) Dual exposure image in A showing, in
addition, 5-HT-positive immunofluorescence (green) and that some NECs
containing SV2 are also serotonergic.
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© The Company of Biologists Ltd 2008
5 subunit of
Na+/K+-ATPase, and nerve fibres (red) were labelled with
the neuronal marker zn-12. The confocal image illustrates the association of
MRCs (arrows) of the gill filaments (F) with nerve fibres (arrowheads indicate
apparent points of contact). Scale bar, 10 µm. Reprinted with permission
(Jonz and Nurse, 2006