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Terminal nerve in the mouse-eared bat Myotis myotisOntogenetic aspects.

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THE ANATOMICAL RECORD PART A 288A:1201–1215 (2006)
Terminal Nerve in the Mouse-Eared Bat
(Myotis myotis): Ontogenetic Aspects
HOLGER JASTROW,1* AND HELMUT HERMANN AUGUST OELSCHLÄGER2
Department of Anatomy and Cell Biology, Histology, Johannes Gutenberg University,
Mainz, Germany
2
Department of Anatomy III (Dr. Senckenbergische Anatomie), J.W. Goethe University,
Frankfurt am Main, Germany
1
ABSTRACT
As in other mammals, ontogenesis of the terminal nerve (TN) in the
mouse-eared bat (Myotis myotis) starts shortly after the formation of the
olfactory placode, a derivative of the ectoderm. During development of
the olfactory pit, proliferating neuroblasts thicken the placodal epithelium and one cell population migrates toward the rostroventral tip of the
telencephalon. Here they accumulate in a primordial terminal ganglion,
which successively divides into smaller units. Initial fibers of the TN can
be distinguished from olfactory fibers in the mid-embryonic period. The
main TN fiber bundle (mfb) originates from the anteriormost ganglion in
the nasal roof, whereas one or more inconstant smaller fiber bundles (sfb)
originate from one or more smaller ganglia in the basal part of the rostral
nasal septum. The fibers of the mfb and sfbs join in the posterior quarter
of the nasal roof before reaching the central ganglion (M) located in the
meninges medial to the olfactory bulb. From the mid-fetal period onward,
a thin TN fiber bundle with some intermingled perikarya connects M to the
brain by penetrating its wall rostral to the olfactory tubercle. Additional
smaller ganglia may occur in this region. The TN and its ganglia persist
in postnatal and adult bats but the number of perikarya is reduced
here. Moreover, the different potential functions of the TN are discussed
briefly. Anat Rec Part A, 288A:1201–1215, 2006. Ó 2006 Wiley-Liss, Inc.
Key words:
Myotis myotis; nervus terminalis; olfactory placode; development; neuron count
The terminal nerve (TN; nervus terminalis or cranial
nerve zero) is located medial to the olfactory bulb and
the olfactory fibers. It was found in all mammals investigated so far (with few questionable exceptions) (Brown,
1987). Whether or not the gonadotropin-releasing hormone-immunoreactive (GnRH) neurons arise from the
olfactory placode or neural crest, they are the main
source of GnRH (Krey and Silverman, 1978; King et al.,
1984; Schwanzel-Fukuda et al., 1985, 1988, 1994; Caldani et al., 1987; Schwanzel-Fukuda and Pfaff, 1988,
1989, 1990; Zheng et al., 1988; Jennes, 1989; Wray
et al., 1989a, 1989b; Demski et al., 1990; Ronnekeiv and
Resco, 1990; Oelschläger and Northcutt, 1992; Muske,
1993; Northcutt and Muske, 1994; Jastrow et al., 1998).
Recently, it was demonstrated in zebrafish that all hypothalamic GnRH cells arise from the neural crest (Whitlock et al., 2003). Here, the neuroendocrine population
originates from the adenohypophyseal region of the
developing anterior neural plate, whereas their neuroÓ 2006 WILEY-LISS, INC.
modulatory neurons originate from the cranial neural
crest. The latter population becomes associated with the
olfactory placode and from there migrates into the diencephalon as part of the TN.
The terminal nerve participates in the innervation
and function of the nasal apparatus in general and
hence, among other aspects, in olfaction and in the autonomic regulation of blood flow in the nasal mucosa.
Thus, evolutionary changes in this area may result in
modifications of the TN system.
*Correspondence to: Holger Jastrow, Raiffeisenstrasse 11,
55239 Gau-Odernheim, Germany. Fax: 49-6733-949540.
E-mail: info@drjastrow.de
Received 23 December 2005; Accepted 8 August 2006
DOI 10.1002/ar.a.20390
Published online 9 October 2006 in Wiley InterScience
(www.interscience.wiley.com).
1202
JASTROW AND OELSCHLÄGER
TABLE 1. List of investigated microslide series of the mouse-eared
bat (Myotis myotis)
No.
CRL (mm)
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
6.5
9
10
11
12
12
12
12
13
13
14
14
15
16
18.3
19
21
22
22
23
23
23
27
30
subadult 1
subadult 2
adult
HL (mm)
Stage
Age (D)
Orientation
4
5
5
5
6
6
6
6
6
6
6
6
7
7
8
8
8
8
8
8
8
8
9
H
E
E
E
33
37
39
40
41
41
41
42
42
43
43
43
44
45
47
47
50
52
52
52
53
53
57
60
younger subadult
older subadult
adult
sagittal
transverse
transverse
sagittal
transverse
transverse
transverse
transverse
transverse
transverse
transverse
transverse
transverse
sagittal
transverse
sagittal
transverse
transverse
sagittal
transverse
transverse
sagittal
sagittal
frontal
sagittal
transverse
sagittal
–
–
6
6.5
7
7
7
8
7.5
8.5
9
9
10
13
13
13
14
15
15
14
15
15
16
18
–
–
–
CRL, crown-rump length; HL, head length; Stage, ontogenetic stage according to Štěrba (1990);
Age (D), estimated days after fertilization using tables from Štěrba (1990); H, ‘‘Hairs on body’’
stage according to Štěrba (1990); E, ‘‘Eyelids open’’ stage according to Štěrba (1990).
Considering the close topographical relationship of the
TN to the olfactory and vomeronasal systems, it is interesting to note that some bats such as Myotis motis completely lack a vomeronasal organ (Mann, 1961), as is
known of toothed and baleen whales. In these species,
the TN may have taken over functions of the vomeronasal system, particularly in the whales, which lack olfactory fila and an olfactory bulb from the early fetal period
onward (Sinclair, 1951a, 1966; Oelschläger and Buhl,
1985a, 1985b; Oelschläger et al., 1987; Ridgway et al.,
1987; Oelschläger, 1989). In this article, the development
of the TN in the mouse-eared bat (Myotis myotis) from
the mid-embryonic period to the adult stage is monitored.
The data of this investigation confirm the high variability of the terminal nerve (Huber and Guild, 1913;
McCotter, 1913, 1915; Brookover, 1914, 1917; Johnston,
1914; Larsell, 1918, 1950; Humphrey, 1940; Pearson,
1941; Sinclair, 1951a, 1951b, 1951c; Bojsen-Møller, 1975;
Cooper and Bhatnagar, 1976; Brown, 1980, 1987; Haymaker et al., 1982; Wirsig, 1985; Buhl and Oelschläger,
1986; Wirsig and Leonard, 1986a, 1986b; Jastrow, 1995),
including the fact that the TN may be unilateral (Jastrow et al., 1998). Analysis of many ontogenetic stages
shows a concentration of neurons in some ganglia and
along fiber bundles and the persistence of a considerable
number of TN neurons up to the adult mouse-eared bat.
MATERIALS AND METHODS
The terminal nerve and its ganglia were analyzed in
27 complete microslide series of the mouse-eared bat
(Myotis myotis; Table 1). Most of these series belong to
the collection of the late Professor Dietrich Starck. The
deeply anesthetized animals had been fixed in formaldehyde, dehydrated in ethanol, transferred to xylene, and
embedded in paraffin wax. Blocks were cut on a sled
microtome at a thickness of 10–40 mm. Sections were consecutively mounted and stained mostly with azocarmine
and aniline blue (Azan) or with hematoxylin-eosin (HE).
Using an Olympus BHS microscope, all TN perikarya
were drawn with the help of a camera lucida at a magnification of 400–1,0003. Only a few specimens [18.3, 19,
22 mm crown-rump length (CRL), including the adult]
were not entirely drawn since here the neurons of the
terminal nerve could be unambiguously identified as a
continuum of cells and connecting fibers. TN neurons
were distinguished from other tissues by their large,
intensely stained acidophilic perikarya as well as by the
size and morphology of their nuclei and nucleoli. Nevertheless, from mid-embryonic to early fetal stages, it was
not always possible to make a clear distinction between
single perikarya of the TN and immature cells of Bowman’s glands in the nasal mucosa. In sagittal series,
graphic reconstructions of the terminal nerve and its
ganglia were drawn by adding relevant structures from
parasagittal microslides to the image of a mid-sagittal
section with a Makropromar microprojector (Leitz, Germany). In case of other sectional planes (horizontal,
transverse), such reconstructions obtained from the preceding and the following sagittal series were superimposed on one paper and adapted to each other in order
to create a new sagittal view. Thereby outlines were
TERMINAL NERVE IN BATS
interpolated regarding the size of other structures, e.g.,
the nasal septum as well as differences in CRL. The
new mediosagittal image was then modified according to
the topography of TN structures in the microslide series
under scrutiny. Finally all drawings were digitized using
an HP ScanJet 4c.
For better comparison, all animals had been classified
as to their ontogenetic stage with the method of Štěrba
(1985, 1990). This method uses the CRL, total length,
head length, and morphological/histological criteria as,
e.g., branchial arches, the development of hands and
feet, eye and ear, as well as hair and cartilage/bone formation. The relevant criteria were described in detail
for Myotis myotis by Štěrba (1990). The main characteristics of Štěrba’s ontogenetic levels in correlation with
the staging of the Carnegie system (referring to embryos
only) are as follows: level 1 stage 6, primitive streak;
level 2 stage 9, first somites (1–7); level 3 stage 13,
limb buds, four branchial arches, otic vesicle closed;
level 4 stage 16, retinal pigment present, handplate,
distinct hemispheres, detached lens vesicle; level 5 stage 19, marked pinna, indented handplate, obliterated
lens cavity, follicles of tactile hair (vibrissae) on upper
lip; level 6 stage 23, fused palate, separated toes, first
ossification, hair follicles on body; level 7 (fetal period),
eyelids fused, retroposition of umbilical hernia; level 8,
numerous skinfolds present; level 9, eruption of tactile
hairs on lip; level H, hair growth all over body; level E,
eyelids separated; level N ¼ newborn. In addition, developmental criteria of the brain and the olfactory bulb
were used (Jastrow, 1995).
1203
Fig. 1. Mouse-eared bat (Myotis myotis) specimen of 6.5 mm CRL.
Parasagittal section demonstrating the vicinity of the telencephalic wall
(T) and the olfactory placode (OP). The primordial ganglion of the terminal nerve (between arrows) is located in the mesenchyme (Me)
close to the immature meninx (M) and the rostrobasal wall of the telencephalic vesicle (T). A, artifacts; nc, primitive nasal cavity; bv, region
of blood (vessel) formation from mesenchyme; V, primitive ventricle.
RESULTS
The youngest specimen [6.5 mm CRL; stage 4, after
Štěrba (1990)] shows neuroblasts of the terminal nerve
(Nervus terminalis) in one large irregular primordial
ganglion near the rostrobasal wall of the telencephalic
vesicle (Fig. 1, arrows). Some neuroblasts are leaving
the olfactory placode (OP; Fig. 2), whereas neuron clusters and single cells are located in the mesenchyme
between the placode and the ganglion (Fig. 1). Only one
nasal pit is present in this specimen, indicating a malformation of the nasal region anlage. In principle, neurons are assembled here in a continuum from the placode to the brain wall. Whereas very few outgrowing olfactory nerve fibers are obvious, still no distinct fiber
bundle can be recognized as the terminal nerve. On the
other hand, immature neurons of the TN do not show
any mitotic figures; such are only seen in neuroblasts
located in the superficial layer of the olfactory placode
as one (?) source of TN neurons. The early neuroblasts
of the TN are spherical to ovoid in shape, with a maximal diameter of about 10 mm. Their nucleus represents
up to 90% of the perikaryon area in transverse section;
cell processes are hardly detectable and the nuclear
membrane stains more intensely for Azan than the cell
membrane. The average diameter of cells is about 12
mm. Apart from this, the darker cytoplasm and the
higher nucleus-to-cytoplasm ratio allow the discrimination of immature TN neurons from surrounding or interposed mesenchyme cells. Nasal and meningeal portions
of the TN cannot be recognized here because no anlagen
of the nasal septum and the cribriform plate are detectable.
Fig. 2. Mouse-eared bat specimen of 6.5 mm CRL. Evasion of
potential terminal nerve neurons (between arrows) from the olfactory
placode (OP) into neighboring mesenchyme (Me). Note some mitotic
figures (Mi) near the surface of P bordering the nasal cavity (nc).
The embryo of 9 mm CRL (stage 5) has an elongated
nasal pit with the olfactory placode as a thickening of
its dorsomedial epithelium. There are still many mitotic
figures near its luminal surface and few TN neuroblasts
were seen penetrating the basement membrane of the
1204
JASTROW AND OELSCHLÄGER
Fig. 3. Reconstruction of a parasagittal section through the forehead of a 10 mm CRL embryo of Myotis myotis showing the terminal
nerve (TN), its ganglia and fiber bundles, the anlage of the large lateral
nasal gland1 (arrow), the nasal cavity (nc), and cartilage structures of
the nose (ca). The main fiber bundle (mfb) connects the main nasal
ganglion (N) in the nasal roof to the meningeal ganglion (M) located
rostral to the telencephalic wall (T) and near the superior sagittal sinus
(sss). Outside the sectional plane, in the submucosa of the nasal septum, the small fiber bundle (sfb) runs from the small nasal ganglion (S)
to join the mfb in the caudal roof of the nose. The olfactory bulb and
olfactory nerve fibers are omitted.
placode. The number of TN neuroblasts in the submucosa of the upper septal region is smaller than in the
6.5 mm embryo described above. Single cells and small
cell clusters are present along distinct fiber bundles running in the dorsomedial submucosa toward the primordial terminal ganglion, which now exhibits a higher neuron number and density. The olfactory fibers are much
more abundant in this than in the preceding embryo but
a complete TN is still not obvious. A slight protrusion of
the rostroventral surface of the telencephalic vesicle is
the first sign of the primordial olfactory bulb, the formation of which is induced by olfactory fibers entering the
brain wall in this region. Some TN neurons (diameter of
perikaryon about 12 mm) exhibit first processes, some
small chromatin granules in the nucleus, and one or two
larger nucleoli.
The embryo of 10 mm CRL (stage 5; parasagittal
reconstruction in Fig. 3) has a much larger nasal cavity,
cartilaginous anlagen of cranial bones, and shows the
beginning of desmal ossification (Frick, 1954; Jastrow,
1995). The volume of the developing olfactory bulbs is
about three times larger than in the 9 mm CRL specimen and olfactory fila are much more prominent. Mitotic
figures are no longer seen in the OP, which is more difficult to discriminate from surrounding respiratory epithelium and terminal neuroblasts penetrating the basal
membrane of the OP are no longer encountered. A small
recess is the first sign of the developing duct of the first
large lateral nasal gland (Frick, 1954). There is one
large nasal TN ganglion (N) in the submucosa dorsal
and caudal to the recess just mentioned. This ganglion
seems to have about the same amount of neurons as the
rostral clusters of neuroblasts encountered in the 9 mm
CRL specimen but there may be a lot of variability in
the migration of the neuroblasts and in the formation of
the TN ganglia.
The TN of the 10 mm CRL embryo can be followed
throughout the sections from the caudal end of N to the
main ganglion (Fig. 3), which is much larger than in the
previous specimen. From now on, it can be distinguished
more easily from neighboring connective tissue due to
the increasing concentration of neurons. Because this
ganglion is located in the developing dura mater and
arachnoidea, it is referred to as the meningeal ganglion
(M), which corresponds to the anterior or rostral TN
ganglion in the literature (e.g., Larsell, 1918, 1950; Grüneberg, 1973). The thin but distinct fiber bundle connecting the ganglia N and M is called the main fiber
bundle (mfb) of the terminal nerve since it is much
thicker than TN fiber bundles running in the submucosa
of the middle and lower nasal septum. The mfb corresponds to the rostral or anterior branch of the TN in the
literature. Some neurons and small TN cell clusters are
present along its course. In the submucosa of the ventral
nasal septum, a small TN ganglion (S) with its small
fiber bundle (sfb) is located near the place where a vomeronasal organ is found in most vertebrates (for reviews,
see Wysocki 1979). According to Frick (1954) and Mann
(1961), this organ is lacking in Myotis myotis. In the
deep submucosa on both sides of the nasal septum, sfbs
course from S in the dorsal and caudal direction to join
the mfb near the end of the nasal cavity (Fig. 3). This
figure also shows that the combined fiber bundles (mfb,
sfb) terminate in the main TN ganglion, which is now
clearly delineated by a sheath of connective tissue. Ganglion M is located in the developing meninges between
the mesethmoid spine (not shown in Fig. 3) (Frick, 1954)
and the thickened rostromedial wall of the telencephalic
hemisphere (T). The rostralmost part of the unpaired
superior sagittal sinus (SSS) is encountered about 100–
250 mm dorsomedial to the ganglia M. Interestingly, the
perikarya of the TN neurons seem to be more mature
than those of the telencephalic wall in that they are a
little larger, no longer spherical, and show distinct processes as predominantly multipolar neurons. Some TN
neurons only show one or two processes indicative of
(pseudo)unipolar, bipolar, or immature multipolar cells;
their average cell diameter is about 14 mm. With a diameter of 7–10 mm, the nuclei make up about 70% of the
perikarya in cross-section. This increase in cytoplasm
volume together with a stronger basophilia is caused by
an increase of RER and ribosomes, indicating the onset
of neuronal function.
The 11 mm CRL (late stage 5) specimen shows a tiny
lumen in the blind-ending duct of the developing first
large lateral nasal gland (Lng1), which is now about 150
mm in length (Fig. 4). The olfactory placode is no longer
distinct from the future respiratory epithelium, indicating that neurogenesis has stopped.
At 12 mm (early stage 6), the rapidly growing Lng1 is
located in the dorsorostral quarter of the nasal roof. The
main nasal TN ganglion (N) is situated mediocaudal to
it. Each TN ganglion comprises about 300–400 neurons
TERMINAL NERVE IN BATS
Fig. 4. Parasagittal section through the anterior nasal roof of the
11 mm CRL Myotis myotis embryo (A). The main fiber bundle (mfb)
and the small nasal ganglion (S) are located close to the cartilage of
the nasal septum. B shows the opening and a part of the duct of the
large lateral nasal gland1 (Lng1) in close vicinity to the main TN nasal
ganglion (N). A, artifacts; nc, nasal cavity.
(number of nasal TN perikarya estimated in these animals). The mfb shows 40–50 mostly spindle-shaped neurons along its course, some of which lie scattered,
whereas others are grouped in clusters of up to 15 perikarya. The TN fiber bundles run parasagittally in the
gutter between the nasal septum and the nasal roof,
close to the perichondrium. Here they pass the mesenchyme of the future cribriform plate and reach the
developing meninges, where they end in the ganglion M.
One small nasal ganglion S was present near the incisive canal dorsal to the anterior paraseptal process
(Frick, 1954). On each side, an sfb with about 20 neurons along its course originates from this ganglion to
join the mfb in the caudal third of the nose. The ovoid
ganglia M are bordered by meningeal fibroblasts; each is
situated between the mesethmoid spine and the developing olfactory bulb, which is much larger in the 12 mm
specimen. As to the blood vessels in this area, the rostrobasal portion of the sss is encountered about 50 mm dor-
1205
somedial to the meningeal ganglia (M) and some
branches of the posterior cerebral artery (Grosser, 1904;
Oelschläger, 1988) are seen in close vicinity. In all the
ganglia mentioned, perikarya of the TN are associated
in groups of 4–30 cells and the groups separated from
each other by thin nerve or connective tissue fiber bundles. Most of the somata have diameters of 12–15 mm
and show three to four processes. The nucleus (diameter:
10–12 mm) covers 50%–70% of the cross-sectional area in
these perikarya. One larger or up to four smaller nucleoli are located in the heterogeneous nucleoplasm.
Regarding the shape of their somata and processes as
well as their staining characteristics, TN neurons are
advanced in differentiation compared to those of the
CNS.
The two embryos of 13 mm CRL (stage 6) show the
differentiation of additional large lateral nasal glands
(Frick, 1954; Jastrow, 1995). In the olfactory bulb, some
layers can be distinguished now: glomerular layer (about
25 mm thick), external plexiform layer (thickness 20 mm),
internal plexiform layer and inner granular layer (together about 130 mm), and subependymal layer (60 mm).
The characteristic mitral cells (mitral cell layer), however, are not yet encountered in these specimens. The
duct of Lng1 turns from the mediorostral opening at the
anterior third of the nasal roof laterocaudally to its blind
end (Fig. 5). The main nasal TN ganglia (N), situated
mediodorsal to it, cause slight protrusions of the epithelium in the rostral nasal roof into the nasal cavity (not
shown). Along a single mfb, only about 15 spindleshaped terminalis neurons are seen in very small ganglia. On both sides, an sfb originates from a small ganglion (S). The TN enters the cranial vault through the
anteriormost and medialmost foramen of the incipient
cribriform plate, together with a thin olfactory fiber bundle (Foramen olfacto-terminale) and a tiny artery next
to the mfb. Further caudally, each mfb enters the main
ganglion (M). These two ganglia are spherical to ovoid
and have several processes; among typical TN neurons
they contain about 15 cells with a strikingly large perikaryon (diameter: up to 22 mm; nuclear diameter: up to
18 mm).
In the two 14 mm CRL (late stage 6) specimens, the
entire cribriform plate is present for the first time. Apart
from that, morphological findings are similar to those in
the younger animals but the number of neurons along
the nasal fiber bundles is smaller and the meningeal
ganglia have some plump protrusions. The main nasal
ganglia exhibit 10 neurons of noticeable larger perikaryon size (diameter: up to 22 mm).
The 15 mm CRL (early stage 7) specimen for the first
time shows Bowman’s glands in the medial nasal submucosa. In principle, the olfactory bulb and the cerebral
cortex now exhibit the characteristic layers, although
typical mitral or pyramidal neurons are still not obvious.
The course of the TN and the location of its ganglia
resemble previous stages but the ganglia S are smaller,
and there are thin extensions of the meningeal ganglia
M. Somata are no more located along fiber bundles (mfb,
sfb) in the deep nasal submucosa. When neurons are
sectioned at their maximum diameter, the nucleus comprises about 60% of the whole perikaryon. Most of the
TN neurons are multipolar and the few particularly
large somata found in the two preceding embryos are no
longer detectable.
1206
JASTROW AND OELSCHLÄGER
Fig. 5. Horizontal reconstruction of the anterior nasal roof in a 13
mm CRL Myotis myotis demonstrating the course of the large lateral
nasal gland1 (Lng1), the main TN nasal ganglia (N), from which the
main nasal fiber bundles (mfb) run caudally. Whereas Lng1, N, and
mfb are located in the nasal roof, the small nasal ganglia (S) as the
origins of the small TN fiber bundles (sfb) are located close to the
base of the nasal septum. From here the sfb ascends to join mfb in
the caudal third of the nasal roof (asterisk).
The 16 mm CRL specimen (stage 7) has a large main
nasal ganglion (N) on each side with 1,236 cells on an
average. Both ganglia are situated in the rostral quarter
of the nasal roof immediately medial to the duct of Lng1
(Fig. 6) and are surrounded by a plexus of small blood
vessels. Next to a thin artery, the mfb runs from the
caudal end of N to the meningeal ganglion (M). There
are not only one but even two sfbs on both sides, each
with two ganglia, a larger (S1) and a smaller one (S2).
The unusually large ganglion S1 with over 1,000 neurons is present at the base of the nasal septum in the
right nasal submucosa. A rostral sfb, adjacent to blood
vessels, ascends from the dorsocaudal end of S1 and
runs rather straight to the nasal roof to join the mfb.
The small ganglion S2 with only 23 neurons is attached
to the rostral sfb about 200 mm caudal to N. A second
smaller sfb rising from S2 is free of TN neurons and
joins the mfb further caudally. A similar situation is
present on the left side, with a much smaller ganglion
S1 (110 neurons), whereas ganglion S2, located dorsocaudal to S1, contains 33 neurons. Both meningeal ganglia (M) are ovoid, with extensions toward the mfbs.
From a ventrocaudal protrusion of the ganglia M, a few
fibers can be followed a short distance along medial olfactory fila in the direction of the medial brain wall, but
an entrance of the TN into the CNS is not detectable.
The perikarya of 20 TN neurons located in M and N are
probably precursors of the type 2 neurons (see below,
specimens of 21 mm CRL) and are hardly stained.
Whereas in younger specimens, one or two nucleoli are
predominating, TN neurons of this animal show three to
four nucleoli in their nucleoplasm. The majority of neurons are multipolar with three to five processes; only
some are bipolar.
In the 18.3 mm CRL mouse-eared bat (early stage 8,
Fig. 7), the TN can be followed into the brain wall for
the first time. Moreover, initial mitral cells are now
obvious in the olfactory bulbs. There are no ganglia S or
sfbs in this animal. Each ganglion N (not shown in
Fig. 7) gives rise to a long mfb lacking any perikarya
Fig. 6. Parasagittal reconstruction of the anterolateral nasal roof of
a 16 mm CRL mouse-eared bat specimen with a projection of the
large lateral nasal gland1 (Lng1), which is situated lateral to the sectional plane, the main TN nasal ganglion (N) from which the main nasal
fiber bundle (mfb) runs caudally and some Bowman’s glands (B). Note
the length of the duct and the bulbous blind ending of the large lateral
nasal gland1.
Fig. 7. Three-dimensional reconstruction of the rostral neurocranium of a 18.3 mm CRL Myotis myotis specimen showing the meningeal ganglion (M), the central fiber bundle (c), its ganglion (C), and the
entrance (asterisk) of the terminal nerve (TN) into the medioventral telencephalon (T). The main TN fiber bundle (mfb), which runs from the
main nasal ganglion rostralward, is accompanied by a branch of the
posterior cerebral artery (a), another branch of which penetrates the
meningeal ganglion (M). The bizarre ganglion with its finger-like protrusions is located between the olfactory bulb (ob), the spina mesethmoidalis (sme, cut), and the rostroventral part of the superior sagittal sinus
(sss). II, optic nerve; cc, corpus callosum; V, septal ventricle.
along its course toward the bizarre ganglion M. The central part of each TN (c) originates from a posterior projection of M, runs close to the medialmost olfactory fila,
and enters the brain wall (asterisk) immediately caudal
to a small central ganglion (C; 10 and 11 perikarya,
respectively) in the area of the primordial anterior olfactory nucleus (Fig. 7). The multipolar neurons in C do
not differ from other neurons of the TN and are somewhat larger than the neurons in the brain wall, which
begin to develop initial processes.
The fetus of 19 mm CRL (early stage 8) lacks the ganglia N and the sfbs on both sides. Other findings largely
correspond to those reported for the previous specimen.
However, the duct of the Lng1 is now considerably longer and extends over 15 mm from its opening in the anterior medial to the lateral nasal roof and further caudal
TERMINAL NERVE IN BATS
to the lateral nasal wall. It ends in the body of the
gland, which has been formed in the middle third of the
deep submucosa, some millimeters above the nasal floor
(Frick, 1954). Five neurons of the left ganglion C seem
to have entered the brain wall in the direction of the
septum and hypothalamus. These immigrated peripheral
TN cells differ from cerebral neurons by the larger size
of their perikarya and nuclei and slightly more intense
staining of the cytoplasma.
The Myotis specimens of 21 mm CRL (stage 8) show
some larger mucus glands in the nasal submucosa near
the ganglia N. The irregular ganglia M show several finger-like extensions. The small ganglia C are located in
the pia mater and comprise 10 neurons per side. In contrast to the younger specimens, there is a new cell type
present in all the ganglia except for C. These type 2 cells
(for potential precursor cells, cf. 16 mm specimen above)
make up about 30% of all TN neurons and differ from
the type 1 cells by a nearly unstained cytoplasm, a
darker nucleus with condensed chromatin, only 1–2 bigger instead of 2–4 smaller nucleoli, and slightly reduced
average cell and nuclear diameters. About 2% of the
neurons are intermediate in appearance, with a more or
less spherical perikaryon and maximal diameters of 16–
20 mm, hardly staining cytoplasm, and a karyoplasm
darker than in type 1 cells. The great majority of all
cells are multipolar; few are bipolar.
The two fetuses of 22 mm CRL (stage 8) lack the small
ganglia (S) and their fiber bundles (sfb). Apart from
their processes and topography, it is rather difficult to
discriminate fetal nasal TN neurons from epithelial cells
of Bowman’s glands, which now are present throughout
the nasal submucosa. As in the 21 mm CRL specimen,
there are no perikarya along the course of the mfb. The
branched meningeal ganglia M are elongated rostrocaudally and located close to the frontal part of the superior
sagittal sinus, the medialmost olfactory fiber bundles,
and branches of the posterior cerebral artery. Central
fiber bundles (c) are only found in one of the two specimens. One central ganglion (C) with 10 perikarya is
present on the right. It is located close to the entrance
of c into the brain, i.e., in the area of the prospective anterior olfactory nucleus. On the left, the situation is similar. About 60% of the TN neurons belong to type 1, 38%
to type 2, and 2% are intermediate. As in the previous
specimen (21 mm CRL), perikarya of a single type are
not clustered in the ganglia but mixed with the other
types and cell groups are separated from each other by
delicate fibers with small intermingled cells resembling
fibrocytes.
The three specimens of 23 mm CRL (late stage 8)
show first mitral cells in their thickened olfactory bulbs
and pyramidal neurons can now be distinguished in the
prospective cortex of the enlarged cerebral hemisphere.
In the rostral quarter of the nasal roof, medial to the
duct of the first large lateral nasal gland, all three animals show main nasal ganglia (N), which do not consist
of one compact cluster of cells but have bizarre fingerlike protrusions, and all of them show slender, elongated
nasal ganglia S on both sides. The latter ganglia occur
in the deep submucosa at about half-length of the basal
nasal septum close to larger vessels and in the vicinity
of larger glands (Fig. 8a). The bizarre meningeal ganglia
M consist of type 1 cells (about 60%) and type 2 cells
(40%; Fig. 8b), whereas the ganglia N and S have
1207
Fig. 8. Oblique sagittal section of the nose of a 23 mm CRL Myotis
specimen with the cartilaginous nasal septum (center) as a bridge
between the two nasal cavities (nc). A: Overview of the nose showing
part of the duct of the large lateral nasal gland1 (Lng1), a small portion
of the main TN nasal ganglion (N), the small nasal ganglion (S), the
small fiber bundle (sfb), and the meningeal ganglion (M) of the other
side. B: Detail of M. Note that type 2 TN neurons (2) have more condensed nuclei and nearly unstained cytoplasm in comparison to type
1 neurons (1). T, Telencephalon.
slightly more type 1 neurons ( 70%). No TN perikarya
are obvious along any TN fiber bundles here (mfb, sfb,
c). Small central ganglia (C) are situated on both sides
in all animals, in close vicinity to the entrance of the
central TN fiber bundle (c) into the brain. This entrance
is located either in the ventral lamina terminalis, i.e.,
medial to the basis of the olfactory bulb and corresponding with the situation shown in Figure 7 (asterisk), or a
few hundred micrometers further rostralward in the
area of the anterior olfactory nucleus.
The situation in the 27 mm CRL bat fetus (stage 9) is
quite similar to that of the previous specimens, but with
the following exceptions: there are two and three ganglia
S (left, right), respectively, in the middle part of the
nasal septum and two sfbs on the right side (Fig. 9). The
fan-shaped elongate main nasal ganglia (N) are
extremely large. On both sides, each ganglion is situated
medial to the opening and initial part of the Lng1, which
now has a total length of about 2,5 mm. Processes of
the large meningeal ganglia (M; Fig. 10) with densely
packed neurons extend forward to the medialmost fila
olfactoria and backward to the central fiber bundle of
the TN (c), which lacks ganglia on both sides.
Compared to the preceding animals, there are no
major differences in the 30 mm CRL specimen (stage H).
A small nasal ganglion (S) is only present on the left
1208
JASTROW AND OELSCHLÄGER
Fig. 9. Parasagittal reconstruction of the nose of the 27 mm CRL
Myotis myotis specimen showing the large TN nasal ganglion (N), the
two small nasal ganglia (S1, S2), and their two fiber strands (sfb1,
sfb2) joining the main fiber bundle (mfb), which enters the cranial vault
through the cribriform plate (cp) to reach the meningeal ganglion (M).
From here, a small central fiber bundle (c) runs to the entrance of the
terminal nerve into the rostromedioventral telencephalon (asterisk).
Fig. 10. Myotis myotis of 27 mm CRL. A: Original parasagittal section with the maximal sectional area of the largest TN meningeal ganglion (M) of all specimens investigated. Note the duct of the large lateral nasal gland1 (Lng1) sectioned as well. B: Detail. A, cutting artifacts; a, branch of A. cerebri posterior; cp, cribriform plate; nc, nasal
cavity; of, olfactory fila; sss, superior sagittal sinus; T, telencephalon.
and lacking on the right side, and so is its fiber bundle
(sfb). The larger TN ganglia contain less neurons than
in the 27 mm specimen. The shape of the bizarre ganglion M, situated close to a rostral (nasal) branch of the
Fig. 11. Myotis myotis of 30 mm CRL. Three-dimensional reconstruction of the right meningeal ganglion (M) and its topographical
relations seen from rostral, dorsal, and the right. Note some terminal
nerve (TN) neurons (asterisk) located along the main fiber bundle (mfb)
near the Foramen olfacto-terminale of the cribriform plate (cp), which
contains bundles of terminal and medialmost olfactory fibers (of) and
a small artery (a; nasal branch of the posterior cerebral artery). The
central terminal fiber bundle (c) enters the brain some millimeters further caudally and more ventrally (not shown). Olfactory bulbs were
omitted for clarity. cd, caudal; d, dorsal.
posterior cerebral artery, is shown in Figure 10. Central
ganglia (C) are lacking. Type 2 TN neurons are no longer detectable in the nasal ganglia N and S and there
are only a few of them left in the meningeal ganglion M.
Some spindle-shaped TN neurons appear mainly in
the ganglia N and S. On the right side, a few TN neurons are scattered along the main fiber bundle (mfb)
rostral to a finger-like extension of the ganglion M.
Some of these cells are located in the rostralmost and
medialmost foramen of the cribriform plate (Fig. 11,
Foramen olfacto-terminale), in close vicinity to a small
artery and the rostral- and medialmost olfactory fiber
bundles. A few other TN neurons lie further rostrally
in the caudalmost part of the nasal roof (Fig. 11,
asterisk).
The two subadult bats (stage E) have their main nasal
ganglia (N) located in the rostral sixth of the nose, which
is considerably elongated in comparison with the preceding fetuses. The duct of Lng1 extends further caudally,
where its body is located some millimeters above the
nasal floor on the basal lateral wall of the nose. The initial segment of the duct is located lateral to the ganglia N
for a few mm but does not seem to have any connections
to it. Small nasal ganglia and sfbs are not detectable in
both animals. Two of the main ganglia (M) are of a bizarre appearance, whereas the main nasal ganglia (N)
seem to have dissolved into 3–4 smaller ganglia of different size, all of them being located in close vicinity to a
nasal branch of the posterior cerebral artery. Central
fiber strands (c) and their ganglia, for the most part, are
not obvious in the sections, some of which are destroyed
in the region of interest in both specimens. In one animal
strand c can be followed as far as the mid-basal forebrain;
TERMINAL NERVE IN BATS
1209
DISCUSSION
Topography and Development of TN
Fig. 12. Original parasagittal section of the adult Myotis myotis. A:
Survey demonstrating the topography of the TN meningeal ganglion
(M) with the adjacent posterior cerebral artery (Acp) and olfactory
fibers (of). B: Detail of the meningeal ganglion with the entrance of the
main TN fiber bundle (mfb; arrows) and a few scattered TN neurons
(asterisks). Note that there are no longer different types of TN neurons.
A, artifact; nc, nasal cavity; T, telencephalon.
however, the area of entry into the brain wall is
destroyed. No type 2 TN neurons are present here.
In the adult bat (late stage E), the main TN nasal
ganglia (N) are still located in the rostral sixth of the
medial nasal roof, medial to the first few mm of the duct
of Lng1. The ganglia N, which are usually fan-like in
younger animals, on both sides seem to have divided
into two neighboring ganglia. Each ganglion N is elongated toward the mfb, which joins its neighbor a few
hundred mm further caudally. Together, the fibers run
along the medial nasal roof and enter the cranial vault
through the Foramen olfacto-terminale (cf. Fig. 11). No
neurons are encountered along the course of the mfbs.
Small nasal ganglia or fiber bundles are not present.
Only in this adult specimen, the large meningeal ganglion (M) on both sides is directly attached to the posterior cerebral artery (Fig. 12). Whereas on the right, the
ganglion is nearly spherical, it is more elongate on the
left. In addition, some single TN neurons are scattered
in the meninges close to the ganglia M. A central fiber
strand (c) is not obvious. All of the multipolar TN neurons belong to cell type 1 (Fig. 12b).
In mammals, olfactory placodes become evident as
oval-shaped, thickened areas of the anterolateral ectoderm of the head in the late ontogenetic stage 2 of Štěrba’s (1985, 1990) classification system. In the mouseeared bat, Myotis myotis, this should happen at about
gestational day (D) 25 and at a CRL of about 3.8 mm
[calculated on the basis of Štěrba (1990)]. In early stage
3, the OPs show horseshoe-like ridges and begin to develop simple olfactory pits. In Myotis myotis, this presumably takes place at about D27 and a CRL of 4 mm.
In recent studies, Whitlock et al. (2003, 2004) demonstrated the origin of at least the GnRH- immunopositive
subset of TN cells from the anteriormost edge of the
neural crest in D3 zebrafish [probably corresponds to
stage 3 of Štěrba (1990)]. In human embryos, the neural
crest was first observed by Müller and O’Rahilly (2004)
in the Carnegie stage 13 [about D27, which corresponds
to stage 3 of Štěrba (1990)]. Müller and O’Rahilly (2004)
investigated over 300 serially sectioned human embryos
and clearly demonstrated nasal crest material in several
Štěrba stage 4 specimens directly underneath the basement membrane of the olfactory placode. This material
originates from the nasal plate at the neurosomatic junction, as does the neural crest, and contains LHRH precursor cells (Verney et al., 2002). Müller and O’Rahilly
(2004) observed that crest cells began to adhere to each
other and to form cords, which a little later began to
migrate toward the region of the olfactory tubercle. In
this context, one can assume that the majority of TN
neurons, particularly the endocrine cell populations of
the TN in humans, originate from crest material of the
neurosomatic junction, which is a major source of endocrine cells in general (von Bartheld and Baker, 2004;
Whitlock, 2004). In contrast to this, a most recent investigation of the Indian major carp (Cirrhinus mrigala) by
Biju et al. (2005) very clearly demonstrated GNRH peptide only in surprisingly well-differentiated bipolar epithelial cells of the olfactory placode and not in the neural crest on D1 [probably corresponding to stage 3 of
Štěrba (1990)]. In this context, it should be noted that
neural crest cells may also invade the placode (von Bartheld and Baker, 2004). Almost certainly the cells that
were noted to leave the placode in the youngest specimens (6.5 and 9 mm CRL) of this investigation belong to
another, probably nonendocrine cell population of the
TN that probably is by far larger than the endocrine
one. In bats, initial terminal nerve neuroblasts (TNn)
and Schwann cells, ensheathing the olfactory and TN
fibers later, leave the medial wall of the OP in stage 4.
Some immature neurons penetrate the internal limiting
membrane of the OP in the two youngest specimens
investigated by Brown (1980). The smallest embryo of
this study (stage 4; 6.5 mm CRL) already shows an
aggregation of TNn near the surface of the telencephalic
vesicle; thus, the onset of TNn migration must have
happened earlier in ontogenesis, probably early in stage
4. This is confirmed by Brown (1980), who could not
detect any TN material in smaller/younger embryos of
other bats (Tadarida brasiliensis, Myotis velifer, and
Myotis lucifugus) of 6 mm CRL (stage 3), whereas bats
of more than 7 mm CRL (stage 4 and later) exhibit large
1210
JASTROW AND OELSCHLÄGER
numbers of TNn adjacent to the OP (Brown, 1980;
Oelschläger, 1988). In case neural crest material would
be an important source of the TN cells in bats, the relevant neuroblasts should have appeared before stage 4
and Brown should have encountered them; therefore, a
placodal origin of the TN material seems more convincing for the moment.
In the next stage (5), when the first fila olfactoria can
be detected (Brown, 1980; Oelschläger, 1988; Jastrow,
1995; this study), outgrowing TN fibers gather in the
mesenchyme rostral, ventral, and medial to the location
where the primordial olfactory bulb will protrude from
the telencephalic wall after being induced by olfactory
fibers (Oelschläger and Buhl, 1985a, 1985b; Oelschläger,
1989). At small pit is found close to the rostral end of
the OP (Fig. 3), when the majority of the TNn have left
the OP. It indicates the formation of the first large lateral nasal gland. In the 9 mm CRL specimen (stage 5),
most TN neurons seem to be present. Some of them are
still on their way to the ganglion situated medial and
rostroventral to the telencephalic vesicle. For the first
time, the TN is traceable as a distinct fiber bundle in
the 11 mm CRL embryo, whereas the formation of the
main nasal ganglia begins at 10 mm CRL with the association of cell clusters (Brown, 1980; Oelschläger, 1988;
this study). Additional smaller ganglia (S) are present
on both sides of the nasal septum in the region where a
vomeronasal organ normally would be expected. The
central portion of the terminal nerve develops slightly
later; in this study, it was first seen at 18.3 mm CRL
(early stage 8): TN perikarya migrate and fibers grow
out from the meningeal ganglion (M) in the direction of
the future attachment site of the terminal nerve.
Finally, TN neurons penetrate the leptomeninx. In part,
the migration of neurons and the extension of the nerve
are supplemented by a passive shift due to allometric
phenomena since structures exceedingly growing next to
the TN (e.g., the nasal septum) tend to stretch its fibers.
Thus, the more or less spherical ganglion M of younger
specimens may lengthen mainly by considerable proliferation of neighboring connective tissue in older specimens
(Jastrow, 1995). Brown (1980) followed two central fiber
bundles in embryos of 8 mm CRL (early stage 5) in the
bat species mentioned above, one of the bundles entering
the brain close to the primordial medial septal nucleus
and the other in the area of the olfactory tubercle. In
the material of this investigation, the first reliable central fibers are encountered at 18.3 mm CRL (early stage
8). In contrast to the findings of Brown (1980), who
investigated Tadarida brasiliensis, Myotis velifer, and
Myotis lucifugus, there is always one central TN fiber
strand on each side in the mouse-eared bat.
From stages 5 to 8, the transformation of migrating
young round cells into differentiated neurons seems to
be achieved [cell processes much more prominent, increased
volume of perikaryon, LHRH synthesis (Schwanzel-Fukuda and Pfaff, 1990)]. The ability of the cell somata to
migrate is reduced and seems to come to an end by the
development of cell processes, retaining the mostly multipolar TNn in their locations. It is surprising that
Brown (1980) found Tadarida embryos of 13 mm CRL
(stage 6) to be the oldest animals showing a TN in this
species. Maybe this author did not investigate the anterior nasal roof in older bats where, in the present material, the majority of the TNn are found. There is consid-
erable variation in the small septal nasal ganglia (S)
and their fiber bundles (sfb), which may be lacking, even
on both sides (18.3, 19, 22 mm CRL specimens), or can
contain up to 1,357 TN neurons. Usually, one ganglion S
is seen per side, but two ganglia of different size in combination with two sfbs are encountered as well. Most
probably these ganglia persist even if a vomeronasal
organ is not present in its vicinity because the neurons
are involved in quick operation of the local (respiratory)
nasal mucosa. For instance, they could be involved in
local reflex mechanisms as discussed later in Functional
Aspects. The meningeal ganglion (M) and its main fiber
bundle (mfb) were found in all bats investigated in this
study. In contrast to other species such as, e.g., the
human or cat (Brookover, 1914, 1917; Larsell, 1918; Jastrow, 1995), there is no nasal fiber plexus with integrated small ganglia in adult Myotis myotis.
In the bat species investigated, the meningeal ganglia
(M) seem to change in shape during ontogenesis; the initially irregular aggregation of cells (stages 4 and 5) becomes spherical (stage 6), develops processes of increasing length, and finally dissolves into two or more compact ganglia in the adult bat.
No Vomeronasal Organ But a Large Gland
The vomeronasal organ (VNO) is lacking in Myotis
myotis (Frick, 1954), as is the case in other bats of the
family Vespertilionidae (Mann, 1961; Baron et al., 1996;
Wible and Bhatnagar, 1996) but not in Miniopterinae
(Wible and Bhatnagar, 1996), such as, e.g., in Miniopterus schreibersi, where the organ exhibits a well-developed sensory epithelium (Cooper and Bhatnagar, 1976).
In other mammals, TN fibers usually reach the VNO
running next to vomeronasal nerve fibers, e.g., in the
human (Brookover, 1917; Jastrow, 1995), cat, horse, and
cattle (Larsell, 1918), rat (Bojsen-Møller, 1975), as well
as rabbit (Huber and Guild, 1913). In the material scrutinized in this study, neither accessory olfactory bulbs
(AOB) nor vomeronasal nerves are present. Conflicting
data in the literature regarding the existence of a VNO
in bats (Humphrey, 1936; Schneider, 1957; Mann, 1961;
Cooper and Bhatnagar, 1976; Kämper and Schmidt, 1977;
Bhatnagar et al., 1982) will not be discussed here. For
reviews on the VNO and AOB, most of which are focused
on bats, see Mann (1961), Wysocki (1979), Frahm and
Bhatnagar (1980), Baron et al. (1996), Wible and Bhatnagar (1996), Bhatnagar and Meisami (1998), and Meisami and Bhatnagar (1998).
On both sides, the investigated Myotis specimens
measuring more than 10 mm CRL show a small duct in
the anterior third of the nasal roof, which opens into the
rostromedial nasal cavity, extends caudalward and lateralward, widens slightly, and has a blind end (Figs. 3–6,
8, and 10). This duct persists up to the adult and
belongs to the large lateral nasal gland I (Frick, 1954), a
fact confirmed in this investigation. In an earlier study
(Jastrow, 1995), the ending of the duct was not scrutinized in later fetal stages up to the adult and erroneously suggested to be a vomeronasal organ in an unusual location. The nasal opening of this duct is situated
some micrometers away from the main nasal ganglion
(N) of the TN, but there is no obvious connection to the
latter. Later the distance between the duct and N
increases to some hundred micrometers.
TERMINAL NERVE IN BATS
Functional Aspects
Criteria for defining what neural components can be
included as constituents of the TN were discussed by
von Bartheld (2004) with respect to the multitude of
potential markers for its cells. When considering the
ontogenetic development, topographical relationships,
cytological criteria, and immunohistochemical data, it is
obvious that the terminal nerve must have different
functional implications, which in part may overlap with
those of the main olfactory and accessory olfactory systems. Moreover, regarding these aspects, there are differences between species and groups of animals and
there is even considerable inter- and intraindividual variation; thus, e.g., the complete TN may be absent on one
side (Jastrow, 1995; Jastrow et al., 1998; this study).
It is interesting to note that TN neurons precede those
of the telencephalon as to developmental criteria: up to
a CRL of about 19 mm, these peripheral neurons have
larger perikarya, develop processes much earlier, and
stain more intensely than central neurons (Jastrow,
1995; Müller and O’Rahilly, 2004). It was only for this
reason that in the mouse-eared bat of 18.3 mm CRL,
some TN neurons that were continuous with the central
TN fiber tract could be detected inside the telencephalic
wall with routine stain.
As to their morphology, terminal nerve neurons comprise unipolar cells with pericellular baskets of gliocytes
or fibrocytes, bipolar or multipolar perikarya, which may
have two nuclei (Larsell, 1918; Filogamo and Robecchi,
1969; Bojsen-Møller, 1975; Mendoza et al., 1982; Wirsig
and Leonard, 1986b; Zheng et al., 1988, 1990; WirsigWiechmann, 1990; Oelschläger and Northcutt, 1992). In
the material scrutinized in this investigation, apart from
some spindle-shaped bipolar cells, multipolar TNn
clearly predominated. This situation may be typical for
bats in general (Brown, 1980, 1987; Oelschläger, 1988;
this study), and such neurons may have a sensory or
vegetative function. In their study on the TN of different
mammals, Huber and Guild (1913) suggest that TN neurons mostly resemble those of cervical sympathetic ganglia. Accordingly, Larsell (1918) mentions a morphological similarity of the TNn to sympathetic neurons in that
they also have pericellular baskets. In contrast to this,
Brown (1980), who compared TN neurons to those of
other ganglia in bats, found the best correspondence
with small somata in the ganglia of cranial nerves V and
IX. As a consequence, he favors a sensory function of the
TN, which is supported by their placodal origin and fiber
terminations between epithelial cells of the nasal mucosa. Ridgway et al. (1987) depicted TNn in the adult
bottlenose dolphin with large diameters, sparse processes, and a dense sheath of potential gliocytes around their
perikarya. These features are indicative of pseudounipolar neurons and may have a (somato?) sensory function
(Oelschläger et al., 1987; Oelschläger and Northcutt,
1992). Interestingly, between these numerous large and
rounded perikarya, a few bipolar LHRH-immunoreactive
(ir) cells exist (Ridgway et al., 1987; Oelschläger and
Northcutt, 1992).
During ontogenesis, the TN is an important source of
LHRH (¼ mGnRH) neurons that innervate/invade the
hypothalamus to establish the hypothalamo-hypophysial-gonadal axis (Schwanzel-Fukuda et al., 1981, 1985;
Oelschläger and Northcutt, 1992; Jastrow, 1995; Schwanzel-
1211
Fukuda, 1999). This outstanding developmental phenomenon seems to be obligatory for all mammals; disturbances in the formation of the TN result in sterile individuals with the olfacto-genital (Kallmann) syndrome
(Kallmann et al., 1944; Gauthier, 1960; SchwanzelFukuda et al., 1989). The claim that GnRH neurons of
the terminal nerve arise from the neural crest, however,
should be viewed with caution as it is impossible to discriminate neural crest from placodal ectoderm in teleosts
and because this is in contrast to the findings of Biju
et al. (2005), who report that, in the Indian major carp,
GnRH first and only appears in cells of the olfactory placode.
It was shown in zebrafish that only the neuromodulatory mGnRH-positive cells are part of the terminal nerve
(Whitlock et al., 2003). As mentioned above, these cells
originate from the rostralmost edge of the neural crest
(Whitlock, 2004). In early embryonal stages they associate with the material of the olfactory placode before it is
morphologically distinct, and they migrate along TN
fibers into the hypothalamus during early fetal development. In contrast, the immediately endocrine hypothalamic GnRH neurons that express species-dependent
forms of GnRH (Dubois et al., 2002) constitute another
cell population originating from the anteriormost neural
crest (adenohypophysial placode) and reach the hypothalamus independent of the TN (Kouki et al., 2001;
Whitlock et al., 2003; Whitlock, 2004). Among the prenatal bats under scrutiny, there were no specimens from
ontogenetic stages early enough to check what happens
to cranial neural crest material.
In teleost GnRH- and FMRFamide immunoreactive
cells of the TN form a plexus in the upper inner plexiform layer of the retina before terminating on dopaminergic interplexiform amacrine cells or ganglion cells.
By this and the fact that locally secreted GnRH causes
horizontal processes to invaginate deeper into terminals
(of cones only), the TN exerts a modulatory effect on the
retina reducing its sensitivity during light adaptation
processes (Behrens and Wagner, 2004). In this context,
the topography of the TN fibers can explain why odorants of food extracts influence the b-wave of electroretinograms, demonstrating an olfactory influence on the
visually guided behavior in fish (Weiss and Meyer, 1988).
Other implications of the terminal nerve may come via
colocalized GnRH/FMRFamide fibers, which innervate
the basal forebrain and hypothalamus, including the
hypothalamo-hypophyseal-gonadal axis, and influence
the mating behavior (Oelschläger et al., 1998; Helpert,
2006). The GnRH component of the TN alone is not sufficient to explain how this system manages peripheral
and central sensory and motor functions related to
behavior and reproduction (Wirsig-Wiechmann, 2004). In
fact, the GnRH-immunoreactive cells comprise only a
minor population (10%) of all TN neurons while other
TN cell populations are labeled by a large variety of
other markers as reviewed by von Bartheld (2004). This
is not surprising since the neural crest is known to generate several types of endocrine/neuroendocrine cells
(von Bartheld and Baker, 2004; Whitlock, 2004).
Due to the fact that the present investigation could
not involve any immunohistochemistry, the discussion
was not extended beyond the essential issue of LHRH
neurons and their migration.
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JASTROW AND OELSCHLÄGER
A TN function related to olfaction is highly probable
since the areas where the nerve enters the brain, i.e.,
the medial septal nucleus or its primordium, olfactory
tubercle (Brown, 1980; Buhl and Oelschläger, 1986;
Oelschläger et al., 1987; Oelschläger, 1988; Oelschläger
and Northcutt, 1992; this study) are part of or related to
the olfactory system. Free TN endings in and immediately beneath the mucosa of the nasal septum and in
the vomeronasal organ were interpreted as part of a
general visceroafferent system consisting of uni- and
bipolar neurons (Huber and Guild, 1913; Larsell, 1918,
1950; Stewart, 1920; Simonetta, 1932; Simonetta and
Magnoni, 1939; Pearson, 1941). Allen (1936) assumed that
TN neurons are receptive to stimuli other than those
adequate for trigeminal nerve terminals. Most probably,
TN-specific odorants do not bind to superficial cell surface receptors reaching into the nasal mucus as is the
case in olfactory sensory cells but, in this case, agents
must be able to penetrate somewhat deeper to reach free
nerve endings between epithelial cells. It is possible that
in Myotis myotis and other bat species that lack a vomeronasal organ, TN terminals can perceive pheromones
so that a vomeronasal system is not required. However,
it seems premature to suggest that the TN takes over
the vomeronasal function when the main olfactory system is another candidate and by far more similar to the
VN system. All primates have a functional main olfactory system, and this appears to be true for bats as well.
Thus, the main olfactory system may well take over for
the missing VNO in both Myotis (and many other bats)
as well as in Old World primates (Smith et al., 2001). In
this context, Biju et al. (2005) note that the occurrence
of GnRH in olfactory receptor neuron-like cells of Indian
major carp larvae coincides with the onset of feeding
and suggest a food intake-related chemosensory perception of this TN cell population.
Apart from the suggested shift of postnatal VNO function to the TN, the latter could also take over the prenatal functions of the VNO system, e.g., the generation of
LHRH neurons usually located in the VNO. One could
consider this since this investigation revealed that Myotis myotis not only lacks a VNO, but moreover not even
forms a VNO primordium or an accessory olfactory bulb
(at least in the investigated microslide series) as this is
the case in many other mammals. There is a parallel
provided by Catarrhine primates: adult Old World monkeys, including apes, and some humans lack a VNO,
and lower Old World monkeys lose the VNO earlier in
development than apes or humans, which appear to
retain a vestige (Smith et al., 2001; for a comprehensive
summary of VNO system regression in humans, cf. Trotier et al. 2000). Some studies have reported LHRH neurons in the human VNO or entangled with vomeronasal
nerves during embryonic development (Boehm et al.,
1994; Kjaer and Fisher-Hansen, 1996; SchwanzelFukuda, 1999). These neurons most probably belong to
the terminal nerve. Further, LHRH neurons are associated with the TN of macaques (Quanbeck et al., 1997).
These authors even describe two migratory ‘‘waves’’ of
GnRH neurons in the macaque and related both of them
to the TN. Since the TN provides a documented source
of LHRH migration and a pathway for these neurons, it
is certainly reasonable to suggest that it may make up
for the absence of the VNO in Myotis. The scenario presented above relies on comparison to other taxa with
similar characteristics. In a study on adult humans, no
neurons or vomeronasal nerve fiber bundles were observed by Trotier et al. (2000). This suggests that in this
special case, the VNO may not function as sensory
organ. In contrast, all Old World monkeys studied to
date do not develop a VNO vestige (Smith et al., 2001)
and yet still have a TN.
On the other hand, blood pressure monitoring and
modulation as a function of afferent TN fibers was inferred
from potential sensory terminals that were encountered
between smooth muscle cells in the Tunica media of adjacent cerebral arteries (Larsell, 1918; Pearson, 1941).
In this context, the regulation of blood flow to the olfactory bulb and the nasal submucosa could be realized by
TN branches along the supplying blood vessels. Apart
from this, it is most probable that there are anastomoses
between the TN and autonomic nerve fibers along these
vessels. In the present study, nasal TN fiber bundles
were observed in close vicinity of or directly attached to
blood vessels. Therefore, it can be assumed that thin
nerve terminals enter their walls. In the adult mouseeared bat, the immediate contact of meningeal ganglia
with blood vessels on both sides also implies an innervation of the latter (in the case of M. myotis: posterior cerebral arteries) (Grosser, 1904). Unfortunately, investigated sections were too thick to follow potential TN fiber
endings to their target structures.
The swelling of the nasal mucosa in correlation with
air flow and composition is certainly influenced by free
endings of the TN in the submucosa that may detect
odorants or irritating agents and quickly mediate a reaction via efferent TN fibers (perhaps of the same perikaryon in a nasal ganglion) to relevant glands and vessels (Holmgren, 1920; Larsell, 1950; Graziadei, 1976).
Potential vasomotor fibers terminating at smooth muscle
cells of the tunica media of blood vessels were demonstrated by Larsell (1950) and are also seen along vessels
of the septal mucosa and the anterior brain (Oelschläger,
1988). Haymaker et al. (1982) therefore suggest the
involvement of the TN also in the cyclic swelling of the
nasal mucosa. Although quite probable, with the small
nasal ganglia and their fibers located close to larger
glands of the nasal septum (Fig. 6), a direct innervation
of Bowman’s glands by terminals of multipolar TNn
could not be traced in the sections of the Myotis myotis
presently examined. Perhaps the TN houses the parasympathetic (efferent?) component of innervation leading
to vasoconstriction.
Free TN fiber endings were also considered to serve
thermoreception (Grüneberg, 1973; Bojsen-Møller, 1975).
Such an additional afferent innervation of nasal glands
would allow the moistening of air by a reflex via the TN
and thus serve thermoregulation. In vertebrates, thin
fiber bundles of the TN were reported to be in close association with the nasopalatine nerve via anastomoses
(Brookover, 1917). By this, the TN may modulate the activity of structures as different as glands and blood vessels in the nasal septum as well as the naris constrictor
muscle (Wirsig-Wiechmann and Ebadifar, 2002). From
the fact that, in some of the bats investigated in the
present work, thin TN fibers run from the large ganglion
M into the meninges, it may be assumed that there is a
contribution to their innervation with possible anastomoses to those branches of the trigeminal nerve being
responsible for the meninges.
TERMINAL NERVE IN BATS
In addition to the TN, autonomic nerve fibers carried
by other nerves (mainly trigeminal branches) reach the
nasal submucosa and influence its swelling, nasal air
flow, and secretion. The persistence of the TN into the
adult stage could be a sign that this innervation alone is
not sufficient for the required protective mechanisms.
Despite its connections particularly with the olfactory
nerve, the TN has to be regarded an independent cranial
nerve (Jastrow 1995; von Bartheld, 2004; Wirsig-Wiechmann, 2004). On the one hand, this is obvious from its origin, development, course, and attachment to the brain;
on the other hand, from its presence in toothed whales.
These animals completely lack the vomeronasal system
and lose the anterior olfactory system (olfactory nerves,
bulbs, and peduncles) during early fetal development and
the concomitant total reconstruction of the nasal region as
a consequence of their phylogenetic adaptation to aquatic
habitats (Johnston, 1914; Sinclair, 1951a, 1951c, 1966;
Oelschläger and Buhl, 1985a, 1985b; Buhl and Oelschläger, 1986; Oelschläger et al., 1987; Ridgway et al., 1987;
Oelschläger, 1992; Cranford et al., 1996; Klima, 1999;
Cranford, 2000; Huggenberger, 2003). In toothed whales,
which echolocate by means of their highly modified upper
respiratory tract (epicranial complex, nasal complex) (Cranford et al., 1996, Huggenberger, 2003), the terminal nerve
attains a maximal number of neurons among the Mammalia (Buhl and Oelschläger, 1986; Oelschläger et al.,
1987; Ridgway et al., 1987). The coincidence of this hypertrophy with the loss of the nasal chemoreceptor systems clearly demonstrates the considerable degree of independence of the TN from these systems.
As is the case in the adult bottlenose dolphin (Ridgway
et al., 1987), the terminal neurons in the adult Big Brown
Bat (Eptesicus fuscus) for the most part do not express
LHRH but may have to be attributed to other functional
systems rather in microchiropterans (Oelschläger and
Northcutt, 1992). It was suggested earlier that in toothed
whales the TN innervates parts of the upper respiratory
tract (Buhl and Oelschläger, 1986; Oelschläger et al.,
1987) involved in the generation of sonar signals by
means of a secondary pneumatically driven vocalization
mechanism (Cranford and Amundin, 2004; Goodson et al.,
2004). At the moment, however, it is unclear whether the
TN can possibly play a similar role in the vocalization of
bats. Microchiropterans use ultrasound signals of comparable intensity, directivity, and frequency range (Cranford
and Amundin 2004). However, as the mouse-eared bat
produces ultrasound signals with the larynx and emits
them through the mouth (open-mouth vocalizer) and not
the nose, it appears rather unlikely that the TN should be
involved here in sound emission.
ACKNOWLEDGMENTS
Dedicated to the memory of Prof. Dr. Dietrich Starck
(1908–2001), eminent authority of comparative morphological and embryological research. The authors thank Dr. Pavel
Nĕmec (Biodiversity Research Group, Department of Zoology, Charles University, Prague, Czech Republic) for helpful
discussion and the reviewers for constructive comments.
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