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Histological Determination of the Areas Enriched in Cholinergic Terminals and m2 and m3 Muscarinic Receptors in the Mouse Central Auditory System.

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THE ANATOMICAL RECORD 293:1393–1399 (2010)
Histological Determination of the Areas
Enriched in Cholinergic Terminals and
m2 and m3 Muscarinic Receptors in the
Mouse Central Auditory System
SATOKO HAMADA,1,2 TAKESHI HOUTANI,1 STEFAN TRIFONOV,1
MASAHIKO KASE,1 MASATO MARUYAMA,1 JUN-ICHI SHIMIZU,1,2
TOSHIO YAMASHITA,2 KOICHI TOMODA,2 AND TETSUO SUGIMOTO1*
1
Department of Anatomy and Brain Science, Kansai Medical University,
Moriguchi, Osaka, Japan
2
Department of Otolaryngology, Kansai Medical University, Moriguchi, Osaka, Japan
ABSTRACT
Cholinergic projections to auditory system are vital for coupling
arousal with sound processing. Systematic search with in situ hybridization and immunohistochemistry indicated that the ventral nucleus of
the medial geniculate body and the nucleus of the brachium of the inferior colliculus constituted cholinergic synaptic sites in the brainstem auditory system, containing a significant number of cholinergic axon
terminals and m2 receptor-expressing cell bodies. Anat Rec, 293:1393–
C 2010 Wiley-Liss, Inc.
1399, 2010. V
Key words: central auditory system; muscarinic receptors;
vesicular acetylcholine transporter
Cholinergic neuronal connections in the central auditory system have been known to play essential roles not
only in basic neuromodulatory processes (Habbicht and
Vater, 1996; Yigit et al., 2003) but also in behavioral
arousal or attention (Metherate and Ashe, 1993; Hsieh
et al., 2000), plastic response (Ji et al., 2001, 2005; Ji
and Suga, 2008), and cognitive functions. In Alzheimer
disease, marked degenerative changes are frequently
found throughout major sites of the ascending auditory
pathway including the primary auditory cortex, the ventral nucleus of the medial geniculate body, and the central nucleus of the inferior colliculus (Ohm and Braak,
1989; Sinha et al., 1993).
At the earlier stages of Alzheimer disease, O’Mahony
et al. (1994) found a significant dysfunction in the midlatency response, indicating an impairment of the ascending cholinergic system that originates in the
pedunculopontine tegmental nucleus and mostly terminates in the thalamus. Buchwald et al. (1991) also
observed a close relation between the auditory and
ascending cholinergic systems by pharmacological
manipulation with a cholinergic agonist and antagonist.
Morphologic evaluation of the cholinergic fibers and
receptors responsible for the function of the central auditory system has been little accomplished except for the
C 2010 WILEY-LISS, INC.
V
cochlear nucleus, where the distribution density of cholinergic fiber–receptor systems has been reported to be
regionally variable (Frostholm and Rotter, 1986; Chen
et al., 1995; Yao and Godfrey, 1995, 1999; Yao et al.,
1996; Jin et al., 2005; Jin and Godfrey, 2006). Tsutsumi
et al. (2007) studied the distribution of cholinergic components in the precerebellar nuclei by using vesicular acetylcholine transporter (VAChT) immunohistochemistry
and provided evidence that mesopontine cholinergic neurons negatively regulate neocortico-ponto-cerebellar projections at the level of pontine nuclei. Because VAChT is
synthesized in major cholinergic neurons and localized
Grant sponsors: The Ministry of Education, Culture, Sports,
Science and Technology of Japan, The Science Research
Promotion Fund of the Japan Private School Promotion
Foundation.
*Correspondence to: Tetsuo Sugimoto, Department of Anatomy and Brain Science, Kansai Medical University, Moriguchi,
Osaka 570-8506, Japan. Fax: þ81-6-6995-2708.
E-mail: sugimoto@takii.kmu.ac.jp
Received 1 September 2009; Accepted 11 March 2010
DOI 10.1002/ar.21186
Published online 17 May 2010 in Wiley InterScience (www.
interscience.wiley.com).
1394
HAMADA ET AL.
to synaptic vesicles for acetylcholine transport (Erickson
et al., 1994; Roghani et al., 1994, 1996; Schafer et al.,
1994; Usdin et al., 1995), this molecule is used as a cholinergic marker to delineate terminals and preterminal
axons (Schafer et al., 1995, 1998; Gilmor et al., 1996;
Weihe et al., 1996; Arvidsson et al., 1997; Ichikawa
et al., 1997; Roghani et al., 1998).
The aim of this study was to delineate a relative abundance of the fiber–receptor system in specific regions of
the central auditory system by means of histochemical
detection of cholinergic fibers and receptors. VAChT
immunohistochemistry was used to examine cholinergic
fibers. Based on the specific nucleotide sequence for m2
and m3 subtypes, digoxigenin-labeled cRNA probes were
designed. With these riboprobes, in situ hybridization
was conducted to investigate the distribution of their
mRNAs. The regional densities of immunoreactive fibers
and hybridization-positive neurons were analyzed in the
distribution field of the auditory system.
Of the five subtypes of muscarinic receptors (m1–m5),
the m2 and m3 subtypes were selected to examine in
this study, because these two subtypes have been shown
to be abundantly expressed in the cerebral cortex and
brainstem regions including some nuclei of the ascending auditory pathway (Buckley et al., 1988; Weiner
et al., 1990; Levey et al., 1991, 1994). The m2 and m3
subtypes show different properties in coupling to G-protein and cellular effects (Felder, 1995; Murthy and
Makhlouf, 1997; Frazier et al., 2008). The m2 subtypes
prefer to be located presynaptic to cholinergic cells and
coupled to inhibition of cAMP elevation, whereas m3
subtypes are dominantly located postsynaptic on cholinoceptive cells in forebrain and couple to activation of
phosphatidyl inositol turnover.
MATERIALS AND METHODS
Animals
All experiments were performed in compliance with
the National Institute of Health Guide for the Care and
Use of Laboratory Animals (NIH Publications No. 80-23,
revised 1996), and all procedures were approved by the
Institutional Animal Care and Use Committee. Tenweek-old male C57BL6/J mice (CLEA Japan, Tokyo, Japan) in which Preyer reflex could readily be elicited by
hand clap were used in this study.
Immunohistochemistry
The brain was sliced into 40-lm coronal sections with
Cryotome according to Kase et al. (2007). These sections
were immunostained for VAChT with essentially the
same method as described previously (Tsutsumi et al.,
2007).
RT-PCR
The animals were deeply anesthetized with sodium
pentobarbital (100 mg kg1, i.p.). The brain and spinal
cord were dissected. Total RNA was extracted from the
tissues by the guanidium thiocyanate method. A 10-lg
aliquot of the RNA was reverse-transcribed with 5 pmol
of oligo(dT)30 as a primer, 1 mM dNTP, and 100 U of
ReverTra Ace (Toyobo, Tokyo, Japan) in 20 lL of the
reaction mix for 1 hr at 42 C. One microliter aliquot of
the RT product was amplified by PCR. The reaction mixture (20 lL) contained 1 lM forward and reverse primers, 200 lM dNTP, and 0.5 U of Ex Taq Hot Start
Version (Takara, Otsu, Japan). The PCR conditions were
as follows: pretreatment at 94 C for 2 min; 35 cycles of
PCR (denaturation, 0.5 min at 94 C; annealing, 0.5 min
at 68 C; and extension, 0.5 min at 72 C). The primers
mM2 (forward) 50 -atatcccgggcgagcaagagcagaataaag-30
(30-mer) and mM2 (reverse) 50 -acaggatagccaagattg
tcctggtcac-30 (28-mer) were used to amplify the 556-bp
fragment, corresponding to the nucleotide 625–1180
from the translation initiation site of mouse m2 muscarinic receptor cDNA (NM_203491; 1401 bp). The primers
mM3 (forward) 50 -gtagcagctatgagctacaacagcaagg-30 (28mer) and mM3 (reverse) 50 -cttctggtcttgagagcaaacctcttagcc-30 (30-mer) were used to amplify the 550-bp fragment, corresponding to the nucleotide 866–1415 from
the translation initiation site of mouse m3 muscarinic
receptor cDNA (NM_033269; 3168 bp). The PCR-amplified fragments corresponded to the third cytoplasmic
loop manifesting a low level of amino acid homology
among m1–m5 muscarinic receptors derived from rodent
and several other species.
These fragments were subcloned into pGEM-T Easy
plasmid (Promega, Madison, WI) and sequenced with
ABI PRISM BigDye Terminator Cycle Sequencing Ready
Reaction Kits (Applied Biosystems, Tokyo, Japan).
Riboprobe
The constructs were linearized and subjected to
in vitro transcription. The reaction was carried out for
2 hr at 37 C in 20 lL of the transcription buffer, pH 8.0,
containing 1 lg of template DNA, 10 mM dithiothreitol,
1 mM GTP, 1 mM ATP, 1 mM CTP, 0.65 mM UTP, 0.35
mM digoxigenin-11-UTP (Roche Diagnostics, Mannheim,
Germany), 20 U of ribonuclease inhibitor (Toyobo), and
40 U of T7 RNA polymerase (Stratagene, La Jolla, CA).
Then, the DNA template was digested with DNase I for
15 min at 37 C. Riboprobes were precipitated with ethanol and LiCl, resuspended in diethylpyrocarbonate
(DEPC)-treated distilled water, and adjusted to a concentration of 200 ng lL1.
In Situ Hybridization
The method followed those developed by Braissant
and Wahli (1998) and was modified as described in detail
previously (Trifonov et al., 2009). All solutions used for
in situ hybridization were treated with 0.02% DEPC.
Mice were perfused with 25 mL of 0.9% saline and
50 mL of a fixative containing 4% paraformaldehyde in
0.1 M sodium phosphate buffer (PB; pH 7.4). The brain
and spinal cord were saturated with 30% sucrose in
0.1 M PB overnight at 4 C. They were frozen on a sliding
microtome and cut into coronal sections of 40-lm thickness. The tissue sections were stored in cryoprotection
buffer (30% sucrose, 30% ethylene glycol, and 50 mM
PB) at 20 C. Free-floating sections were rinsed in 0.1%
DEPC-activated 0.1 M PB-0.9% saline (PBS, pH 7.4)
twice for 15 min. They were equilibrated in 5 standard
saline citrate (0.15 M sodium chloride and 0.015 M sodium citrate, pH 7.0; SSC) for 15 min and incubated in
hybridization buffer (50% deionized formamide, 40 lg
mL1 salmon sperm DNA, 5 SSC) at 55 C for 2 hr.
AUDITORY CHOLINERGIC FIBERS AND RECEPTORS
1395
Fig. 1. Differential expression of m2 (a, c) and m3 (b, d) muscarinic
receptor mRNA detected by in situ hybridization in mouse brain. (a, b)
Levels of thalamus showing hybridization-positive cells in the rostral
auditory cortex (*r), lateral habenular nucleus (LHb), and hippocampal
CA1–3. The hybridization-positive cells are also seen in wider cortical
areas and some regions in the thalamus and hypothalamus. (c, d) Lev-
els of superior colliculus (SC) showing hybridization-positive cells in
the caudal auditory cortex (*c), SC, parabigeminal nucleus (PBG),
pedunculopontine tegmental nucleus (PPTg), and pontine nuclei (Pn).
The borders of the rostral and caudal parts of the auditory cortex are
indicated by solid triangles. Scale bar ¼ 100 lm.
Hybridization was carried out overnight at 55 C. The
hybridization mixture contained 1 ng lL1 digoxigenin
(Dig)-labeled riboprobe in the hybridization buffer.
Hybridized sections were then rinsed with 2 SSC at
room temperature for 30 min, with 2 SSC at 65 C for
60 min, and with 0.1 SSC at 65 C twice for 30 min.
They were equilibrated with Dig buffer 1 (0.1 M Tris
hydrochloride, 0.15 M sodium chloride, pH 7.5) for 5 min.
Subsequently, the tissue sections were reacted with alkaline phosphatase-labeled anti-Dig antibody (Roche Diagnostics; diluted 1:5,000) in Dig buffer 1 containing 1%
blocking reagent for 2 hr. Sections were rinsed in Dig
buffer 1 twice for 15 min. For alkaline phosphatase histochemistry, the tissue sections were equilibrated with Dig
buffer 2 (0.1 M Tris hydrochloride, 0.1 M sodium chloride, 0.05 M magnesium chloride, pH 9.5) for 5 min and
incubated overnight in a light-protected condition with a
reaction mixture containing 450 lg mL1 nitroblue tetrazolium and 175 lg mL1 5-bromo-4-chloro-3-indolylphosphate in Dig buffer 2 at 37 C. The enzyme reaction was
terminated by rinsing sections in TE buffer, pH 8.0, for
15 min. Finally, the tissue sections were thoroughly
washed in 0.9% saline, mounted onto gelatin-coated glass
slides, air dried, equilibrated with 50%, 70%, 95%, 100%,
and 100% ethanol, clarified in xylene three times, and
coverslipped with Canada balsam. The hybridized sections were examined with Nikon E800M light microscope
under brightfield illumination. For the studies of
cytoarchitecture, some adjacent sections were stained
with 0.1% cresyl violet. The nomenclature of the nuclei
and related fiber systems and the approximate locations
of primary auditory cortex were according to Paxinos and
Franklin (2001).
Image Analysis
Levels of VAChT-immunostained material and digoxigenin labeling were quantified by digitized image analysis using Image J software ver. 1.39. Gray levels were
converted to optical densities by using standard internal
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HAMADA ET AL.
Fig. 2. Distribution of VAChT-immunoreactive varicose fibers and
muscarinic receptor mRNA hybridization-positive cells in mouse brain.
(a–c) VAChT-immunoreactive varicose fibers in the medial geniculate
nucleus, ventral part (a), nucleus of the brachium of the inferior colliculus (b), and anteroventral cochlear nucleus (c). Expression of m2 (d–h)
and m3 (i) muscarinic receptor mRNA in the ventral nucleus of the
medial geniculate body (d), nucleus of the brachium of the inferior col-
liculus (e), inferior colliculus (f), pontine nuclei (g), facial nucleus (h),
and auditory cortex (i). Profiles of m2 subtype expression in the pontine nuclei (g) and facial nucleus (h) represent typical labeling of noncholinergic and cholinergic neurons, respectively. CIC, central nucleus
of the inferior colliculus; DCIC, dorsal cortex of the inferior colliculus;
ECIC, external cortex of the inferior colliculus. Scale bar ¼ 50 lm (a–
c), 100 lm (d, e, h, i), and 250 lm (f, g).
curves. The background signal was determined by the
values obtained from the area of the optic tract and subtracted from values obtained in all brain sites harboring
hybridized cells. Three to six subregions were measured
per site and the mean optical density determined. Data
are expressed as the mean of the values determined
from three animals and calculated as signal intensity
per unit area.
tegmental nucleus is regarded as a robust cholinergic
cell group that supplies axons to the thalamus and
many brainstem structures (see Tsutsumi et al., 2007 for
further refs.). A vast majority of neurons expressing m2
receptors were also present in the pontine nuclei (Figs.
1c, 2g) and in motor nuclei of the cranial nerves, including the facial nucleus (Fig. 2h). The pontine nuclei have
been shown to receive abundant VAChT-immunoreactive
fibers traveling from the pedunculopontine tegmental
nucleus (Tsutsumi et al., 2007). On the other hand, the
hybridization-positive neurons preferring m3 subtypes
could be seen principally in the cerebral cortex and hippocampus (Fig. 1b,d). In most of the neocortical areas,
m3 receptors were localized to cortical layers II and III
(Fig. 2i) and, to a lesser degree, to layers V and VI. The
m2 receptors were expressed much more weakly in cortical layers IV and V (Fig. 1a,c). In the hippocampus, m3
receptors were present most prominently in CA1-3
RESULTS AND DISCUSSION
The tissue sections hybridized with riboprobes for m2
and m3 muscarinic receptor subtypes showed distinct
signals with differential expression patterns (Fig. 1).
Neurons expressing m2 subtypes were predominantly
found in the lateral habenular nucleus, superior colliculus, parabigeminal nucleus, and pedunculopontine tegmental nucleus (Fig. 1a,c). The pedunculopontine
AUDITORY CHOLINERGIC FIBERS AND RECEPTORS
1397
rior colliculus, nucleus of the brachium of the inferior
colliculus, ventral nucleus of the medial geniculate body,
and primary auditory cortex (Fig. 2d–f,i). These sites
were subjected to densitometric analysis (Fig. 3) because
considerable amounts of VAChT-immunoreactive varicose fibers and terminal-like structures were detectable
in some of these sites (Fig. 2a–c).
VAChT-Immunoreactive Varicose Fibers
The densest accumulation of VAChT-immunoreactive
varicose fibers was seen in the cochlear nuclei, especially
on the margin of the anteroventral cochlear nucleus
(Fig. 2c). In the anteroventral cochlear nucleus and in
the posteroventral cochlear nucleus, however, a vast majority of the nuclear territories were virtually free from
such varicose fibers (Fig. 3a). Thus, the VAChT immunoreactivity in the entire cochlear nucleus was presumed
to be less intense than that indicated by densitometry in
the cochlear nuclear areas containing the densest accumulation of VAChT-immunoreactive fibers. Immunolabeled fibers and terminal-like structures were present at
moderate levels in the primary auditory cortex, the ventral nucleus of the medial geniculate body (Fig. 2a), and
the nucleus of the brachium of the inferior colliculus
(Fig. 2b). VAChT-immunoreactive varicose fibers were
seen at low levels in the remaining sites.
m2 Hybridization-Positive Cells
The highest density of distribution of neurons expressing m2 subtypes was observed in the dorsal cochlear nucleus in accordance with earlier observations in the
cochlear nucleus (Yao et al., 1996; Jin and Godfrey,
2006) (Fig. 3b). The distribution density of cells with m2
hybridization signal was moderate in the primary auditory cortex, the ventral nucleus of the medial geniculate
body (Fig. 2d), the nucleus of the brachium of the inferior colliculus (Fig. 2e), and the dorsal and external cortex of the inferior colliculus (Fig. 2f). In the remaining
sites, the distribution density of neurons expressing m2
subtype was low.
Fig. 3. Density of signals representative of VAChT-immunoreactive
varicose fibers (a) and neurons expressing m2 (b) and m3 (c) mRNA in
nine regions of mouse central auditory system. The cortex (Cx) in
which measurements were done denotes the primary auditory cortex.
In each brain region, signal density was measured at five subregions
and averaged. (a) The highest density of VAChT-immunoreactive varicose fibers was obtained in the anteroventral cochlear nucleus (AVCN)
followed by the Cx, posteroventral cochlear nucleus (PVCN), and nucleus of the brachium of the inferior colliculus (BIC). (b) The highest
density of m2 hybridization-positive cells was detected in the dorsal
cochlear nucleus (DCN) followed by the Cx, dorsal cortex of the inferior colliculus (DCIC), BIC, ventral nucleus of the medial geniculate
body (MGV), and external cortex of the inferior colliculus (ECIC). (c)
The Cx especially showed a dense accumulation of m3 hybridizationpositive cells. All the other regions measured had a very low level of
the density.
(Fig. 1b), whereas m2 receptors were marked in the dentate gyrus (Fig. 1a).
The m2 and m3 subtypes were expressed in the central auditory system including the cochlear nuclei, infe-
m3 Hybridization-Positive Cells
Many neurons expressing m3 muscarinic receptor
mRNA were seen in the primary auditory cortex and
mainly localized to the layers II and III (Fig. 2i). The
neurons expressing m3 receptors were only seen at low
levels in all the other sites of the central auditory system (Fig. 3c).
In view of the fact that the density of distribution of
cholinergic terminal-like structures and neurons with
m2 hybridization signal was moderate in layers IV and
V of the primary auditory cortex, the ventral nucleus of
the medial geniculate body, and the nucleus of brachium
of the inferior colliculus, it was assumed that the signaling in these regions might be implemented by m2-mediated cholinergic transmission. In the inferior colliculus
and the dorsal cochlear nucleus, the distribution density
of cells with m2 hybridization signal was moderate and
cholinergic axon terminals were small in number. Thus,
it was supposed that the m2-mediated signaling in these
regions might not be dominant.
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HAMADA ET AL.
The nucleus of the brachium of the inferior colliculus
contains auditory neurons subserving the coding for auditory space in association with neurons located in the
deep layers of the superior colliculus (Kudo et al., 1984;
Schnupp and King, 1997; King et al., 1998; Doubell
et al., 2000; Nodal et al, 2005). Nevertheless, the chemical architecture of the nucleus of the brachium of the inferior colliculus has been little elucidated. Our findings
revealed the relative abundance of m2-receptor subtype
and cholinergic terminal-like elements in the nucleus of
the brachium of the inferior colliculus (Fig. 2e) and m2
subtype-expressing neurons in the deep layer of superior
colliculus (Fig. 1c), thus implicating an important contribution of m2 muscarinic receptors for the coding of auditory space information.
The cerebral cortex and thalamus have been shown to
express multiple types of muscarinic receptors including
m2 and m3 subtypes (Buckley et al., 1988; Levey et al.,
1991, 1994). Our results suggest that the m3 muscarinic
receptor is the predominant subtype in the cortex,
expressed in the neurons of the superficial cortical
layers. Neurons of the auditory cortex and medial geniculate nucleus are vulnerable to neurodegeneration characteristic to Alzheimer disease (Sinha et al., 1993).
Important question is whether the neurons expressing
m3 subtypes might be one of the most vulnerable types.
In normal cortices, stimulation of the neurons of the nucleus basalis facilitates auditory thalamocortical synaptic transmission (Metherate and Ashe, 1993; Hsieh
et al., 2000). Activation of m3 receptors in the superficial
layers of the cerebral cortex might be involved in the
process of the synaptic transmission in the auditory thalamocortical system.
ACKNOWLEDGMENTS
The authors thank Fumio Yamashita and Tetsuji
Yamamoto for technical assistance and Yuki Okada for
expert secretarial work. Stefan Trifonov is supported by
the Japanese Government Monbukagakusho (MEXT)
Scholarship Program.
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central, area, auditors, mouse, determination, terminal, receptors, enriched, system, muscarinic, histological, cholinergic
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