1873

The Journal of Experimental Biology 200, 18731879 (1997)

Printed in Great Britain The Company of Biologists Limited 1997
JEB0905

CENTRAL PROJECTIONS OF THE MAXILLARY AND ANTENNAL NERVES IN THE

MOSQUITO AEDES AEGYPTI
PAUL G. DISTLER* AND JRGEN BOECKH
Institut fr Zoologie, Universitt Regensburg, D-93040 Regensburg, Germany
Accepted 23 April 1997

Summary
In the mosquito Aedes aegypti, CO2-sensitive receptor
neurones are located together with two other types of
chemoreceptor neurones in club-shaped sensilla basiconica
on the most distal segment of the maxillary palps. In order
to identify the central target neuropiles of these neurones
and to determine whether antennal receptor neurones
project into the same area, the palpal and antennal nerves
were labelled by anterograde staining with horseradish
peroxidase and by experimentally induced degeneration.
The different methods revealed a consistent projection
pattern. (1) Maxillary afferents project into the
suboesophageal ganglion and ascend further into the

Introduction
Mosquitoes, like a number of other blood-sucking insects, are
equipped with sensory cells responding to host emanations such
as moisture, heat and, of particular importance, body odours.
Among the latter, lactic acid and carbon dioxide have been
shown to alarm and/or attract female mosquitoes (e.g. Daykin
et al. 1965; Mayer and James, 1969; Smith et al. 1969; Friend
and Smith, 1977; Galun, 1977; Gillies, 1980; for reviews, see
Bowen, 1991; Takken, 1991; for more recent results, see Geier,
1995; Steib, 1995). Behavioural and electrophysiological
studies have shown that the yellow fever mosquito Aedes
aegypti (Diptera: Culicidae) has receptor organs that detect very
low concentrations and also extremely small changes in carbon
dioxide (CO2) concentration in air (Kellogg, 1970; Grant et al.
1995; Geier, 1995; Steib, 1995). The CO2-detecting primary
receptor neurones are located on the most distal, fourth segment
of the maxillary palps (Fig. 1). Fine-structure and
electrophysiological studies have shown that these neurones lie
in triads together with other types of chemosensory receptor
cells within club-shaped sensilla basiconica (also referred to as
palpal pegs). Approximately 30 such sensilla are found on a
single maxillary palp of a female A. aegypti (McIver and
Charlton, 1970; Chaika, 1977; McIver, 1982). More recently,
tracing of the axonal projections of these neurones with
fluorescent dye has revealed their projections in a very distinct
glomerulus-like terminal region within the ipsilateral antennal
*e-mail: Paul.Distler@biologie.uni-regensburg.de.

ipsilateral antennal lobe. There, they terminate within

an identified glomerulus of the ventroposterior lobe.
(2) Afferents of the antennal flagellum project into all
glomeruli of the ipsilateral antennal lobe, with the
exception of the glomerulus innervated by the maxillary
nerve. The present anatomical findings suggest that
primary processing of information about CO2 levels takes
place in a defined glomerulus which also receives input
from other palpal chemoreceptor neurones.
Key words: insect, olfactory system, carbon dioxide, palpal
projections, mosquito, Aedes aegypti.

lobe (Anton, 1996). Basically similar projection patterns exist

in other insects. Both physiological and anatomical evidence for
a single and specifically reserved glomerulus in the antennal
lobe for CO2 input from the labial palps has been reported in
an arctiid moth, Rhodogastria luteibarba (Bogner et al. 1986),
and in two other lepidopteran species, Manduca sexta (Kent et
al. 1986) and Pieris rapae (Lee and Altner, 1986).
Our interest in the neuronal processing of host odorants in
mosquitoes has led us to the question of the location of CO2elicited activity in the brain of A. aegypti. As a first step in
answering this question, we have studied the afferent
projections of the maxillary and antennal nerves using two
different labelling techniques: (1) anterograde horseradish
peroxidase (HRP) labelling and (2) experimentally induced
degeneration. In the second step, nerve cell activity elicited by
CO2 stimulation in the central nervous system is located using
2-deoxyglucose labelling (B. Bausenwein and J. Boeckh,
unpublished) in order to identify further the pathway for the
processing of this important olfactory input.
Materials and methods
Animals
Adult 1- to 2-week-old females of the yellow fever mosquito
Aedes aegypti L. (Diptera: Culicidae) were used as

1874 P. G. DISTLER AND J. BOECKH

experimental animals. They were taken from a colony reared
in the Institutes vivarium under standard conditions (Geier,
1995).
Anterograde tracing of the maxillary and antennal nerves
HRP labelling
The animals were immobilized by exposure to cold air (8 C)
and subsequently fixed in a position favourable for
manipulations on the maxillary palps. In 20 mosquitoes, the
fourth segment of one maxillary palp was cut off just distal to
its base using a fine blade. A small drop of a 5 % aqueous
solution of HRP (Boehringer, Mannheim, Germany) was
immediately placed onto the lesion and allowed to infiltrate for
a few seconds. Finally, the preparation was sealed with Vaseline.
A similar labelling procedure had been used previously to trace
the central projections of the cockroach antennal nerve (Kirn,
1996). To label the antennal nerve with HRP, the flagellum was
cut off just distal to the pedicel in 14 specimen, and HRP was
applied onto the lesioned site as described above. The animals
were kept in a moist chamber for between 2.5 and 8 h at room
temperature (20 C) before the preparations were fixed.
Induced degeneration
Degeneration studies (see Boeckh et al. 1970) of both the
maxillary and the antennal nerve projections were performed
in four specimens each. The fourth segment of the maxillary
palp or the flagellum, respectively, was removed according to
the procedure described above, in order to induce degeneration
of receptor axons. These preparations were fixed 24 or 48 h
post lesion. During the degeneration period, the animals could
move freely.
Fixation of the brains
After decapitation of the mosquitoes, the head capsules were
fixed using rapid-setting glue on their posterior surface and
superfused with 2.5 % glutaraldehyde in 0.1 mol l1 phosphate
buffer (PB), pH 7.4. In order to achieve immediate fixation of
the brain, the head capsules were carefully opened by ablating
small areas of cuticle in the dorsal region using sharp glass
capillary tips. The free-floating heads were fixed for
approximately 11.5 h at room temperature (RT). Preparations
that had been induced to degenerate were subsequently post-

Fig. 1. Scanning electron micrographs of the

head and mouthparts of a female Aedes
aegypti (photographs kindly provided by A.
Khn). (A) Head with antenna (an) and
maxillary palps (mp). (B) Distal (fourth)
segment of the maxillary palp showing the
sensilla basiconica (arrow) and noninnervated hairs (arrowhead). (C) Single
basiconic sensillum (arrow) at higher
magnification. Scale bars, A, 200 m; B,
50 m; C, 10 m.

fixed in OsO4 and embedded in resin (see below). HRPlabelled brains were embedded in a mixture of
ovalbumin/gelatin, fixed for a further 10 min, and transferred
into 0.01 mol l1 PB, pH 7.4.
Histochemical reaction of HRP
HRP-labelled brains were cut into 30 m thick serial
sections in a horizontal plane using a vibroslicer. The sections
were collected in 0.05 mol l1 TrisHCl buffer (pH 7.5). HRP
was visualized by reaction with nickel-intensified
diaminobenzidine (Ni-DAB) (0.02 % DAB in TrisHCl buffer,
pH 7.5, with 0.1 % nickel ammonium sulphate and 0.003 %
hydrogen peroxide). The reaction was monitored under the
microscope and stopped after 5 min by removing the Ni-DAB
solution. The sections were postfixed in 1 % OsO4 dissolved in
distilled water for 20 min at RT and, after dehydration in
ethanol, embedded in Epon 812. The polymerization
temperature was 57 C.
Semi- and ultrathin sectioning
For reconstruction of the nerve projections, 3 m thick
semithin section series were cut from whole brains (induced
degeneration) or from selected 30 m thick sections (HRP
labelling) and counterstained with Richardson Blue. For
maxillary nerve labelling, three brains with induced degeneration
(24 and 48 h) and five brains with HRP labelling (between 5 and
8 h) were studied. For antennal nerve labelling, three brains with
induced degeneration (24 and 48 h) and six brains with HRP
labelling (between 5 and 8 h) were studied. In addition, ultrathin
sections were cut from (a) the ventroposterior glomerulus with
the terminal arborizations of the maxillary afferents (three
different preparations) and (b) the nerve bundle in the
suboesophageal ganglion (one preparation). These sections were
counterstained with uranyl acetate (20 min) and lead citrate
(3 min), and examined in a Zeiss electron microscope (EM 109).
Results
Anterograde tract tracing of the maxillary palp nerve
HRP labelling of maxillary afferents revealed a distinct fibre
bundle that projected into the suboesophageal ganglion and
ascended further into the ipsilateral antennal lobe. There, all

Maxillary and antennal nerve projections 1875

projected over a short distance into the contralateral neuropile.
Experimentally induced degeneration of the maxillary palp
nerve for 24 and 48 h revealed a similar projection pattern (Fig.
2B). The characteristic degeneration granules were found in
the same glomerulus that had been identified by HRP labelling.
Fine-structure analysis showed that the glomerulus was
demarcated within the surrounding neuropile by a thin glial
sheath (Fig. 3). Only laterally, next to the basal antennocerebral tract, was the glial border not clearly identifiable. The
HRP-labelled axon processes were distributed throughout the
glomerulus neuropile. A subdivision of this into regions with
either dense or less-dense innervation was not evident. By
analogy with the light microscopic findings, the corresponding
contralateral glomerulus revealed no (two brains) or only very
few degenerated processes (one brain). Cross sections through
the maxillary nerve in the suboesophageal ganglion revealed
that the majority of fibres were HRP-labelled (Figs 4, 5). The
corresponding unlabelled maxillary nerve in the contralateral
hemibrain contained approximately 110, mostly small, axons.

Fig. 2. Maxillary nerve afferents. (A) 30 m thick horizontal section

through a brain with horseradish-peroxidase (HRP)-labelled maxillary
afferents (right maxillary nerve labelled, 5.5 h). A densely innervated
glomerulus (g) is evident in the ipsilateral ventroposterior region of
the antennal lobe (AL). No labelled fibre processes are present in the
corresponding contralateral brain region. The innervated glomerulus
lies lateral to the basal region of the antenno-cerebral tract (act)
and medial to the oesophagus. For further details, see Fig. 3.
(B) Richardson-Blue-stained 3 m thick horizontal section through a
brain with experimentally induced degeneration of maxillary afferents
(24 h). Degeneration granules are present in only one ventroposterior
glomerulus (g). Note that the corresponding contralateral glomerulus
(asterisk) is not innervated. The spatial positions of both glomeruli
identified by HRP labelling and by induced degeneration are identical.
act, antenno-cerebral tract; cb, central body; PC, protocerebrum. Scale
bars, 50 m.

labelled axons terminated within a single, oval-shaped and

particularly large glomerulus approximately 3050 m in
diameter (Figs 25). This projection pattern was identified in
10 brains. No morphological differences with regard to the
projection site or the number of innervated glomeruli were
evident in brains stained for between 2.5 and 8 h. The
innervated glomerulus was located in the ventroposterior
antennal lobe. Medially, it bordered the oesophagus and
laterally it bordered the root of the antenno-cerebral tract
(Fig. 2A). No axonal projections were detected within the
contralateral antennal lobe. In the suboesophageal ganglion,
however, a few smaller processes crossed the midline and

Anterograde tract tracing of the antennal nerve

HRP labelling of the antennal (flagellar) axons revealed that
such afferents innervated all the antennal lobe glomeruli of the
ipsilateral hemibrain, with the exception of the ventroposterior
glomerulus that had specifically received the maxillary
afferents (Fig. 6A,B). Contralateral projections were not
evident, even after HRP labelling for up to 8 h (14 brains).
Slight differences were found, however, between different
preparations with regard to both the number and the intensity
of labelled receptor cell axons. Induced degeneration of the
antennal nerve for periods of 24 and 48 h (three brains)
revealed a similar projection pattern (Fig. 6C).
Discussion
Morphology of maxillary and antennal afferents
Both HRP labelling and induced degeneration of the
maxillary afferents consistently revealed projections into a
single glomerulus located in the ipsilateral ventroposterior
antennal lobe (Figs 24). Its contralateral counterpart did not
contain labelled processes, except for a very few in one
specimen. These presumably belonged to receptor cells of the
contralateral maxillary palp, which could have been severed
during the operation at the closely neighbouring palp and
thereby been caused to degenerate. Preparations labelled for
varying periods, from 2.5 to 48 h, did not show significant
differences in the projection pattern and the terminal regions
of the axonal processes, indicating that the nerve had been
completely labelled. This was further supported by the finding
that all axons within the maxillary nerve appeared to be
labelled.
Earlier
morphological
and
fine-structure
investigations on the maxillary receptor cell types of the fourth
palpal segment had described a similar number of receptor
cells (McIver, 1982). The ventroposterior glomerulus
identified here is located in the same antennal lobe region as
the axon terminals found in the fluorescent dye labellings of

1876 P. G. DISTLER AND J. BOECKH

Fig. 3. Ultrathin section through

the ventroposterior glomerulus
innervated
by
HRP-labelled
maxillary afferents (same section
as in Fig. 2A). Stained processes
(arrows) are distributed throughout
the glomerulus. act, basal region of
the antenno-cerebral tract; AL,
antennal lobe neuropile; G,
ventroposterior glomerulus. Scale
bar, 10 m.

Anton (1996). A slight difference between the studies concerns

the number of innervated glomeruli. In the present study,
terminal ramifications of afferent fibres were found only in one
large glomerulus (Figs 24), and the fluorescence appeared to
be distributed over two smaller, very closely neighbouring
glomeruli.
In contrast to other cyclorrhaphic Diptera (Boeckh et al.
1970; Stocker et al. 1990; Stocker, 1994), the maxillary
afferents projected exclusively into the ipsilateral antennal
lobes. Only in the suboesophageal ganglion were a few fibres
found to cross the midline. The majority of the maxillary
afferents identified in Drosophila melanogaster bifurcate and
project into both antennal lobes. There, they terminate within
a small, mirror-symmetrical group of three (five)
ventroposterior glomeruli (Stocker et al. 1990; Singh and
Nayak, 1985). Morphologically, the maxillary afferents in D.
melanogaster and A. aegypti differ with regard to (a) the
projection site and (b) the number of antennal lobe glomeruli
innervated. Such differences might be due, for example, to
different numbers of chemoreceptor cells on the palps in the
two species (for a review, see Stocker, 1994). In
hemimetabolous insects (Locusta migratoria, Ernst et al. 1977;
Altman and Kien, 1986; Periplaneta americana, Boeckh and
Ernst, 1987), the maxillary nerve projects into both the ipsiand the contralateral brain hemisphere. There, the terminal
ramifications are located in the so-called lobus glomeratus.

The maxillary projection pattern in A. aegypti shows certain

parallels with the labial afferents in some lepidopteran species.
Bilateral axonal projections from each labial palp have been
shown to terminate mirror-symmetrically in a single
glomerulus in each antennal lobe in R. luteibarba (Bogner et

Fig. 4. HRP-labelled right maxillary nerve in the suboesophageal

ganglion (sog) (same brain as in Fig. 2A). The fibres (arrow) project
towards the centre of the neuropile, where small ramifications are
evident (arrowhead). Few processes cross the midline (none shown
here). 30 m thick horizontal section. og, optic ganglia. Scale bar,
100 m.

Maxillary and antennal nerve projections 1877

Fig. 5. Ultrathin section

through the maxillary nerve
in the suboesophageal
ganglion. (A) HRP-labelled
nerve. (B) Maxillary nerve
(unlabelled)
in
the
contralateral hemiganglion.
Arrows, axonal processes of
labelled (A) and unlabelled
(B) receptor neurones. Scale
bar, 1 m.

al. 1986), P. rapae (Lee and Altner, 1986) and M. sexta (Kent
et al. 1986). In Rhodogastria, furthermore, it has been
demonstrated that the respective receptor cells in the distal
labial pits are very sensitive to CO2 and only slightly sensitive
to other odorants (Bogner, 1990). The CO2-sensitive receptor
neurones constitute the majority of labial afferents in
Rhodogastria.
Anterograde tracing of the antennal nerve in A. aegypti
revealed projections only into the ipsilateral antennal lobe. All
the glomeruli, with the exception of the maxillary
glomerulus, were innervated (Fig. 6). These findings are in
accordance with data reported in a previous fluorescence
labelling study (Anton, 1996). Ipsilateral projections of
antennal chemoreceptor cells are typical of many insect species
(for reviews, see Boeckh and Tolbert, 1993; Hildebrand, 1996).
In cyclorrhaphic Diptera such as Musca and Drosophila,
however, the majority of antennal chemoreceptors have axon
projections into both the ipsi- and the contralateral antennal
lobe (Boeckh et al. 1970; Stocker 1994). In D. melanogaster,
it has been reported that glomeruli innervated by the maxillary
afferents receive no other antennal afferents (Singh and Nayak,
1985; Stocker et al. 1990). These findings are consistent with
the situation in A. aegypti, where no antennal axons terminated
in the ventroposterior glomerulus. Studies on the central
Fig. 6. Antennal nerve afferents. (A) 30 m thick horizontal section
(overview) through a brain with HRP-labelled antennal afferents
(right antennal nerve stained, 5 h). (B) All glomeruli of the ipsilateral
antennal lobe, with the exception of the ventroposterior glomerulus,
are innervated. (C) Induced degeneration (24 h) of the right antennal
nerve reveals a similar innervation pattern. (B,C) 3 m thick
horizontal sections counterstained with Richardson Blue. Arrows,
innervated glomeruli; asterisks, ventroposterior glomeruli. act,
antenno-cerebral tract; AL, antennal lobe; cb, central body; PC,
protocerebrum. Scale bars, A, 100 m; B,C, 50 m.

1878 P. G. DISTLER AND J. BOECKH

projections of the antennal nerve in Lepidoptera (M. sexta,
Kent et al. 1986; P. rapae, Lee and Altner, 1986;
Rhodogastria, Bogner et al. 1986) also revealed innervation of
all antennal lobe glomeruli with the exception of the one
receiving the labial afferents.
Functional considerations
In the present study, all the labelled maxillary afferents
terminated within a single glomerulus, suggesting that the
latter might be a distinct region of the antennal lobe specialized
for the primary processing of CO2. The hypothesis of a CO2specific glomerulus is supported by the observation that in A.
aegypti no other appendages (for example, the antenna) are
known to have CO2-sensitive receptor cells that could form an
additional afferent pathway. However, this glomerulus, in
addition to the CO2-sensitive axonal projections, also receives
input from other palpal receptor neurones, which are sensitive
to a variety of chemical vapours, such as n-heptane, acetone
and amyl acetate (Kellogg, 1970). Since the latter are colocalized with the CO2-sensitive receptor neurones in the same
type of basiconic sensillum (McIver, 1982), the labelled axons
could not be identified as being sensitive to either CO2 or
odorants. Therefore, the identified glomerulus is presumed to
be a sensory neuropile in which signals from both CO2sensitive and other maxillary receptor cells (see above) are
processed.
Further insect antennal lobe glomeruli have been identified
as specific target neuropiles of certain chemo- and
thermosensitive receptor neurones (for reviews, see Boeckh et
al. 1990; Stocker, 1994; Hildebrand, 1996). In cockroaches
and moths, for example, pheromone-specific chemoreceptor
cells project exclusively into a single large glomerulus, the socalled macroglomerulus. A small set of glomeruli in the
antennal lobe of Periplaneta americana receives axonal
projections from cold receptor neurones, and other glomeruli
are the target neuropile of afferents from hygroreceptor
neurones on the antenna (Nishikawa et al. 1995). In D.
melanogaster, 23 identified glomeruli are thought to form the
sensory neuropile in which the axons of certain
thermosensitive neurones from aristal sensilla terminate
(Stocker, 1994). However, it still remains unclear in all these
cases whether a particular glomerulus receives input
exclusively from a single receptor type or also from other, so
far unidentified, receptor cell types.
The present findings show that the glomerulus described
here in A. aegypti represents probably the only and specific
target area for CO2-sensitive afferents, which is analogous to
the situation in R. luteibarba. However, there is combined
anatomical and physiological evidence for other
chemoreceptor afferents in this glomerulus, suggesting that, in
contrast to the situation in R. luteibarba, further odorants are
probably processed in this neuropile in A. aegypti.
We thank Mrs E. v. Ciriacy for expert technical assistance
and Mrs H. Hallmer for photographic assistance.

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