Download The distribution of vestibular efferent neurons receiving innervation

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Rhinological and Otological Society, Inc.
The Distribution of Vestibular Efferent Neurons Receiving Innervation
of Secondary Vestibular Afferent Nerves in Rats
Jing Wang, MD, PhD; Fang-lu Chi, MD, PhD; Yuan Xin, MD, PhD; Michael F. Regner, PhD
Objectives/Hypothesis: To explore the innervation areas of the medial vestibular nucleus (MVN) afferent neurons onto
vestibular efferent neurons in the brain stem of rats.
Study Design: A morphology study in the central vestibular system.
Methods: Two neuronal tracers were used. Lectin PHA-L Conjugates (PHA-L, Invitrogen L - 11270,) was injected into
the MVN as an anterograde tracer, and 5% FluoSpheres carboxylate-modified microspheres (MFS, Molecular Probe F-8793)
was injected into the contralateral peripheral vestibule using as a retrograde tracer. All animals were allowed to recover for
12 days to facilitate sufficient transportation of the tracers. Then brain stems were sliced coronally on a freezing microtome
and observed under a fluorescence microscope and laser confocal microscopy.
Results: Neurons in the MVN labeled with PHA-L exhibited green fluorescence, and their axons were distributed near
the genu of the facial nerve (g7) and in the reticulation structure, as well as in the cerebellum or oculomotor-related nuclei.
Neurons labeled with red fluorescence of MFS were mainly located dorsomedial and dorsolateral to g7 and in the caudal pontine reticular nucleus (PnC) bilaterally and presented different morphologies at different locations. The synaptic junctions
would display color overlap (fluoresced yellow). Under three-dimensional reconstruction of the confocal laser microscopy, the
synaptic junctions were visualized dorsomedial and dorsolateral to g7 bilaterally, predominantly ipsilateral to the MVN injection site.
Conclusions: Morphologic evidence of the distribution of vestibular efferent neurons synapsed by afferent nerves from
MVN was demonstrated. These efferent neurons constitute short closed-loop circuits with neurons in the MVN.
Key Words: Vestibular nuclei, afferent, efferent, neural pathways, neuroanatomic tract-tracing techniques, innervation.
Laryngoscope, 123:1266–1271, 2013
INTRODUCTION
The vestibular nervous system consists of both
afferent and efferent vestibular projection pathways.
The afferent vestibular nervous system conducts electrical impulses from the peripheral vestibular sensory
organs and synapses in the vestibular nuclei, sending
signals that ascend to the cortical balance center where
information concerning equilibrium and positioning
sense are processed. By functioning as the primary information integrating center, the vestibular nuclei play a
From the Department of Otology and Skull Base Surgery (J.W., F.Eye and ENT Hospital, Fudan University, Shanghai; Shanghai
Key Laboratory of Forensic Medicine (J.W.), Institute of Forensic Science,
Ministry of Justice, Shanghai, China; and Department of Surgery–
Divisions of Otolaryngology, Head and Neck Surgery (M.F.R.), University
of Wisconsin School of Medicine and Public Health, Madison, Wisconsin,
U.S.A.
Editor’s Note: This Manuscript was accepted for publication
October 3, 2012.
This research was supported by grants from the National Natural
Science Foundation of China (30572018) and the Science and Technology
Committee of Shanghai Municipality (KF1204).
The authors have no other funding, financial relationships, or
conflicts of interest to disclose.
Jing Wang, MD, and Fang-lu Chi, MD, PhD, participated equally
in this work.
Send correspondence to Dr. Fang-lu Chi, Department of Otology
and Skull Base Surgery, Eye Ear Nose and Throat Hospital, Fudan
University, 83 Fenyang Road, Shanghai, China 200031.
E-mail: [email protected]
L.C., Y.X.),
DOI: 10.1002/lary.23847
Laryngoscope 123: May 2013
1266
role in modulating reflexive eye movement as well as
limb movement and can elicit physiologic or pathologic
reactions of the autonomic nervous system.
In mammals, efferent vestibular neurons are mainly
located in the dorsolateral (DL group) and dorsomedial
(DM group) aspects of the genu of facial nerve (g7), the
caudal pontine reticular nucleus (PnC), and a fraction of
neurons in the ventral aspect near the genu of the facial
nerve.1–4 The vestibular efferent nervous system projects
descending fibers bilaterally to peripheral vestibular
organs, capable of modulating the excitabilities of both
vestibular hair cells and afferent nerves.5,6 Electrophysiologic experiments show that the vestibular efferent
nervous system can either stimulate or inhibit the vestibular afferent nervous system. In a previous study,7
electrical stimulation to squirrel monkeys’ vestibular
efferent nervous system resulted in increased release
rate of spontaneous electrical activities of most vestibular
afferent nerves, and less than 1% exhibited an inhibitory
effect. Whether an afferent nerve demonstrates excitatory or inhibitory responses after being stimulated,
stimulating the corresponding efferent nerve can
decrease the response magnitude of the afferent nerve.7,8
Modification by vestibular efferent nerves may contribute to vestibular compensation, and some studies
have found that stimulation of the vestibular end organs
by stimuli such as rotations can excite the vestibular
efferent neurons.9,10 These results suggest that the
Wang et al.: Brain Stem Vestibular Central Pathways
function of the vestibular efferent neurons is regulated
in part by the activity of the vestibular end organs and/
or vestibular afferent neurons in a feedback system.
Injected neurobiotin and biotinylated dextran amine
into the superior vestibular ganglion of Sprague-Dawley
rats, labeled fibers, and boutonlike endings were found
distributed within the dorsolateral vestibular efferent
nucleus on the ipsilateral side.11 This suggested that
vestibular primary afferent neurons in Scarpa’s ganglion
may exert direct influence on vestibular efferent
neurons.
In our previous study, it was found that DL group
neurons may be innervated directly by the vestibular
nuclei neurons.12,13 However, synapse connections, the
direct evidence of that vestibular afferent nerves
synapse on efferent neurons, were not shown. The distribution of the efferent neurons innervated by vestibular
afferent nerves also was not explored.
The present study was designed to investigate this
problem. Anterograde and retrograde neuron-tracing
techniques as well as three-dimensional reconstruction
techniques under confocal laser microscopy were used to
investigate direct innervations of the medial vestibular
nucleus (MVN) afferent neurons to the cells in the
vestibular efferent nuclei.
MATERIALS AND METHODS
Animals
Adult male Wistar rats (N ¼ 12; weight, 290 6 5 g; obtained
from Animals Laboratories of Shanghai Medical College, Fudan
University, China) were included in the sample population. Wistar
rats were housed in cages in groups on a 12-hour lighting cycle
(lights on at 08:00 hours, lights off at 20:00 hours). Three rats
were housed in each cage. The handling of animals and experimental procedures were approved by the Institutional Animal
Care and Use Committee at Fudan University.
Fig. 1. Injection site of the PHA-L in the medial vestibular nucleus
under laser confocal microscopy. Deposits of the anterograde tracer
are primarily confined to the nucleus. 4V ¼ fourth ventricle; g7 ¼ facial nerve genu. Scale bar is 200 lm. [Color figure can be viewed in
the online issue, which is available at wileyonlinelibrary.com.]
immediately, postfixed overnight at 4 C in the same fixative,
and then stored in a 30% sucrose solution overnight. Coronal
sections were cut of the brain stem near the rhomboid fossa
with a freezing microtome at a thickness of 8 lm. The slices
were observed and photographed under fluorescence microscopy
(Leica DMR; Leica Camera AG, Solms, Germany) and laser confocal microscopy (Leica DMIRZ2, Leica Camera AG, Solms,
Germany). Positive cell density counts were conducted on every
fourth slice from 10.5 to 11.0 mm posterior to bregma. Three
different fields were counted: 1) DM group cells, 2) DL group
cells, and 3) cells in the PnC.
RESULTS
Anterograde Neuron Tracing
Anterograde and Retrograde Neuron Tracing
Twelve rats were deeply anesthetized with pentobarbital
(40 mg/kg) and placed in a stereotaxic apparatus (David Kopf
Instruments, Tujunga, CA). The anterograde tracer PHA-L
(Invitrogen L-11270, Lectin PHA-L Conjugates, green color
anterograde fluorescent neural tracer, Eugene, OR) was injected
unilaterally into the MVN by iontophoresis through a glass
micropipette (tip diameter: 30 lm), using the coordinate 10.8
mm posterior to and 1.2 mm lateral to bregma and 7.4 mm ventral to the skull surface. A positive driving current of 4 mA at 3
Hz was applied for 10 minutes. After 7 days of survival in the
original environment to allow for sufficient transport of the
tracers, all rats were anesthetized with pentobarbital (40 mg/
kg) again, and 0.1 lL 5% MFS (Molecular Probe F-8793, FluoSpheres carboxylate-modified microspheres, red color retrograde
fluorescent neural tracer, Eugene, OR) was injected into the
contralateral vestibule through the oval window using a Hamilton syringe (0.5 lL) positioned in a microinjection unit (David
Kopf Instruments, Tujunga, CA). Injections were applied slowly
over 1 minute, and the needle was left in place for 5 minutes after injection.
The rats were allowed to survive postinjection for 5 days
in the same environment then anesthetized deeply and transcardially perfused with saline and 4% paraformaldehyde in 0.1
M phosphate-buffered saline (PBS). The brains were removed
Laryngoscope 123: May 2013
In the anterograde experiment, the injection site of
the PHA-L was sharply defined in the MVN (Fig. 1). Anterograde-labeled terminals were observed bilaterally in
the medial and lateral sides of the facial nerve genu,
superior vestibular nucleus (SVN), desending vestibular
nucleus (DVN), dorsomedial part of the reticular formation, and particularly the dorsal paragigantocellular
nuclei area. The projection was equally strong in both
directions. Labeled terminals were also found in the contralateral MVN area (Fig. 2). The projections from the
MVN to the cerebellum or oculomotor-related nuclei
were not reported.
Retrograde Neuron Tracing
The neurons retrograde-labeled by 5% MFS were
distributed bilaterally dorsomedial and dorsolateral to
the facial nerve genu, as well as in the caudal pontine
reticular nucleus, where the efferent vestibular neurons
are organized in the brain stem. Also, there were MFSpositive cells scattered around the ventral side of the
facial nerve genu. More MFS-positive neurons existed in
the contralateral side of the injection than in the ipsilateral side. Labeled neurons presented with different
shapes in different areas: those medial to the genu of
Wang et al.: Brain Stem Vestibular Central Pathways
1267
Fig. 2. Distribution of PHA-L–labeled
axons and endings in the brain stem
(portions of pons and medulla
oblongata). Green dot indicates the
injection site of the PHA-L in the
medial vestibular nucleus. 4V ¼ 4th
ventricle; g7 ¼ genu of the facial
nerve; icp ¼ inferior cerebellar
peduncle; LVe ¼ lateral vestibular
nucleus; MVeMC ¼ medial vestibular
nucleus, magnocellular part; MVePC
¼ medial vestibular nucleus, parvicellular part; PnC ¼ pontine reticular
nucleus, caudal part; py ¼ pyramid;
scp ¼ superior cerebral peduncle;
sn5 ¼ spinal nucleus V; SpVe ¼ spinal vestibular nucleus; st5 ¼ spinal
tract V; SuVe ¼ superior vestibular
nucleus. [Color figure can be viewed
in the online issue, which is available
at wileyonlinelibrary.com.]
the facial nerve were mostly fusiform shaped, with 5- to
15-lm-diameter cell bodies. Those lateral to the genu
of the facial nerve were oval or fusiform shaped, with
10- to 20-lm-diameter cell bodies. And those in the reticular formation were mostly triangular shaped with large
cell bodies 20- to 30-lm in diameter (Fig. 3, Fig. 4A–C).
Table I showed the distribution of neuron terminals in
the brain stem after PHA-L injection into the MVN and
the location and number of positive cells after microfluorosphere injection into the peripheral vestibule (PV).
Overlapping Labeled Positive Cells
If the vestibular afferent nerve endings terminated
on the vestibular efferent neurons, the synaptic junctions would display color overlap under confocal laser
microscopy, presenting as yellow, owing to anterograde
and retrograde neuron tracing. Many PHA-L–labeled
endings terminated on the MFS-labeled cell bodies of
bilateral vestibular efferent neurons (Fig. 5A–F). These
neurons were distributed more ipsilateral to the brainstem injection site than contralateral. The cell count
method was the same as that of MFS-labeled neurons
(Table I). The neurons with a yellow overlap were
located dorsomedial and dorsolateral to the facial nerve
genu and in the caudal pontine reticular nucleus. Threedimensional projections were made under the confocal
laser microscopy so that the synaptic structure could be
inspected at any angle to make sure there was no tissue
or empty pixels between a positive terminal and cell. A
true contact existed dorsomedial and dorsolateral to the
facial nerve genu.
DISCUSSION
The present study investigated the existence and
distribution of vestibular efferent neurons innervated by
the MVN afferent neurons in the brain stem of rats and
confirmed that the neurons in the DM and DL groups of
Fig. 3. Distribution of MFS-positive
cells. Red dots represent the density of
efferent vestibular neurons. Large red
dots indicate positive cells clustering
together, and small red dots indicate
positive cells dispersing. The side with
more dense dots was contralateral to
the peripheral injection. 4V ¼ 4th ventricle; g7 ¼ genu of the facial nerve; icp
¼ inferior cerebellar peduncle; LVe ¼
lateral vestibular nucleus; MVeMC ¼
medial vestibular nucleus, magnocellular part; MVePC ¼ medial vestibular
nucleus, parvicellular part; PnC ¼ pontine reticular nucleus, caudal part; py
¼ pyramid; scp ¼ superior cerebral
peduncle; sn5 ¼ spinal nucleus V;
SpVe ¼ spinal vestibular nucleus; st5
¼ spinal tract V; SuVe ¼ superior vestibular nucleus. [Color figure can be
viewed in the online issue, which is
available at wileyonlinelibrary.com.]
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Wang et al.: Brain Stem Vestibular Central Pathways
Fig. 4. Photograph of the MFS-positive cells on the medial side (DM group) and lateral side (DL group) of the genu of the facial nerve and
in the caudal pontine reticular nucleus (PnC) under fluorescence microscopy. (A) MFS-positive cells in the DM group were mostly fusiform
shaped, with 5- to 15-lm-diameter cell bodies. (B) MFS-positive cells in the DL group were oval or fusiform shaped, with 10- to 20-lm-diameter cell bodies. (C) MFS-positive cells in the PnC were mostly triangular shaped with large cell bodies 20- to 30-lm in diameter. 4V ¼
fourth ventricle; g7 ¼ facial nerve genu. Scale bar is 100 lm for (A) and 50 lm for (B) and (C). [Color figure can be viewed in the online
issue, which is available at wileyonlinelibrary.com.]
ments can be adequately identified.15 Our results also
showed that nerve fibers from the MVN neurons
bilaterally project to regions of efferent vestibular
neurons in the DM and the DL groups as well as in
the PnC, but with ipsilateral projections dominantly.
Under confocal laser microscopy, the connection sites
only in the DM and the DL groups presented yellow
in color without any tissue or empty pixels between
the green fibers and red cell bodies. These cells with
yellow connection sites were distributed bilaterally in
the DM and the DL groups of the efferent vestibular
neurons, mainly ipsilateral to the central injection
site (contralateral to the peripheral injection site).
This novel finding suggests that neurons in DM and
DL groups of efferent vestibular nuclei receive fiber
projections from afferent neurons bilaterally in the
MVN (albeit more ipsilaterally) and send out nerve
fibers bilaterally to the peripheral vestibular system
(primarily to the contralateral system). The vestibular
afferent neurons receive the information from the vestibular end organs and send modulating signals to
vestibular efferent neurons through their innervations, allowing vestibular efferent neurons to send
feedback regulation signals to the vestibular end
organs by a short closed-loop circuit. These projections may play an important part in fine integration
and modulation of vestibular functions, as well as in
compensation after vestibular damage.
vestibular efferent nuclei were innervated by the MVN
secondary afferent neurons.
Efferent vestibular neurons are located in regions
around the facial nerve genu and PnC in the brain stem,
and their axons synapse in vestibular terminal organs.
FluoSpheres carboxylate-modified microspheres, as a
nontranssynaptic retrograde tracer, has a wide range of
survival times and is combined with a red fluorescent
substance to facilitate visualization, so it is accepted and
used widely.14 It can be absorbed by the peripheral vestibular organs and retrogradely transmitted to the cell
bodies of vestibular efferent neurons. It can also be
transmitted to the cell bodies of primary afferent neurons that lie in the vestibular or Scarpa’s ganglion,
which lies in the internal auditory meatus. Because the
vestibular ganglion lies not in the brain stem, the labeled vestibular efferent neurons would not be confused
with the stained primary afferent neurons. Therefore,
MFS can be used to trace and locate efferent vestibular
neurons.
Our results showed that the nerve fibers from
efferent vestibular neurons around the facial nerve
genu and in the PnC have direct, bilateral connections with the peripheral vestibular organs, with a
greater number of connections to the contralateral
side. The anterograde tracer PHA-L combined with
green fluorescent substance defines individual fibers
and axon terminals well; therefore, presynaptic ele-
TABLE I.
The Distribution and Number of Positive Cells and Neuron Terminals in the Brain Stem After Microfluorosphere (Peripheral Vestibule
Injection Site) and PHA-L Injection (Medial Vestibular Nucleus Injection Site).
Ipsilateral to Central Injection Site
Injection Site
Medial
to g7
Lateral
to g7
Contralateral to Central Injection Site
RF
SVN
DVN
Medial
to g7
Lateral
to g7
RF
MVN
SVN
DVN
MVN
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
þ
PV
36
43
76
0
0
19
23
28
0
0
0
Overlap
Synaptic junctions
22
16
25
19
31
0
0
0
0
0
7
5
9
7
8
0
0
0
0
0
0
0
þ ¼ PHA-L labeled fibers; DVN ¼ descending vestibular nucleus; g7 ¼ genu of facial nerve; MVN ¼ medial vestibular nucleus; PV ¼ peripheral vestibule; RF ¼ reticular formation; SVN ¼ superior vestibular nucleus.
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Wang et al.: Brain Stem Vestibular Central Pathways
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Fig. 5. Three-dimensional reconstruction under laser confocal microscopy showing a portion of the vestibular efferent neuron bodies presenting in yellow due to anterogradely labeled PHA-L boutons synapsed on the retrogradely MFS-labeled cells or dendrites (white arrow).
(A) MFS-positive cells in the dorsomedial group. (B) PHA-L–positive boutons in the medial side of the facial nerve genu. (C) Neuroanatomic
tract-tracing combining anterograde tracing with PHA-L and retrograde tracing using MFS in the medial side of the facial nerve genu. (D)
MFS-positive cells in the dorsolateral group. (E) PHA-L–positive boutons in the lateral side of the facial nerve genu. (F) Neuroanatomic
tract-tracing combining anterograde tracing with PHA-L and retrograde tracing using MFS on the lateral side of the facial nerve genu. Scale
bar is 20 lm for all figure parts. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
The majority of the semicircular canals input synapses in the medial and superior vestibular nuclei.
Second-order neurons course ipsilaterally and contralaterally to reach the oculomotor nuclei (the third, fourth,
and sixth cranial nerve nuclei).16,17 This is the basis for
the direct vestibuloocular reflex. The distribution of
efferent neurons participating in the closed-loop circuits
suggested that the DM and DL groups of efferent neurons may play some role in finely regulating the
vestibuloocular reflex. Nevertheless, each group of efferent neurons may receive different afferent nerve
modulation from different semicircular canals and, in
turn, adjust the corresponding end-organ functions differentially. The roles of each vestibular efferent nucleus
may be different in fine integration and modulation of
the afferent vestibular functions.
Vestibular efferent neurons could be found in reptiles, amphibians, fish, birds, and mammals, but the
locations are different between each of them.1–3,7,8,18–20
Mammals have similar locations and neurotransmitters,
as well as having the efferent vestibular system modulate the afferent input from the peripheral vestibular
receptors to the central nervous system.2,7,18 We speculate that maybe higher mammals, such as the squirrel
monkey or human being, have the same or similar anatomic pathways and functions. Additional study is
necessary.
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CONCLUSION
Vestibular efferent neurons that are innervated
directly by afferent nerves projecting from the MVN
locate in the DM and the DL groups. This pathway may
be involved in the regulation of vestibular responses in
physiologic and pathologic conditions. Further study is
required to better understand the function of these
vestibular efferent neurons synapsed by vestibular afferent neurons in the MVN.
Acknowledgments
The authors thank Dr. Susan L. Whitney for helpful
comments and critical review of the manuscript.
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