The role of the frontal ganglion in locust feeding and moulting related behaviours
Department of Zoology, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel
* Author for correspondence (e-mail: ayali{at}post.tau.ac.il)
Accepted 14 June 2002
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Summary |
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Key words: frontal ganglion, central pattern generator, desert locust, Schistocerca gregaria, feeding, moulting, ventilation
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Introduction |
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The locust foregut consists of a pharynx that leads into a short narrow
oesophagus. The oesophagus is curved, running dorsally before turning
posteriorly to lie beneath the brain. In the prothorax it merges into a
muscular crop, which opens into the proventriculus. The muscles of the foregut
consist of intrinsic and extrinsic muscles. All dilator muscles are extrinsic,
arising from the head walls and tentorium, and attaching to the foregut
(Albrecht, 1953). The major
source of innervation to the foregut dilator muscles is the frontal ganglion
(FG; Aubele and Klemm, 1977
;
Allum, 1973
;
Ayali et al., 2002
). The FG
lies on the dorsal surface of the pharynx, anterior to the brain. A pair of
frontal connectives links the FG with the tritocerebrum, and a recurrent nerve
passes backward along the dorsal surface of the pharynx up to the
hypocereberal ganglion. Another three pairs of fine nerves arise from the FG
to innervate the foregut.
The role of the FG in feeding, growth and development has been the focus of
many studies for more than a century
(Faivre, 1863;
Marchal, 1911
). Most of the
studies examined the effects of ablating the FG on the subsequent behaviour
and development of the insect. Removal of the FG in adult S. gregaria
resulted in decreased feeding activity
(Highnam et al., 1966
;
Hill et al., 1966
).
Ganglionectomy in Locusta migratoria caused the abolition of crop
emptying (Bignell, 1973
).
Similar results were also reported in Lepidoptera, including adult
Heliothus zea (Bushman and
Nelson, 1990
). Manduca sexta larvae from which the FG was
removed were reported to exhibit slower growth
(Bell, 1986
) and deficiency in
food ingestion (Griss et al.,
1991
). In adult M. sexta, Miles and Booker
(1994
) found that the FG is
essential for the activity of the cibarial pump during feeding, and both
necessary and sufficient to produce the motor patterns of the foregut muscles
(Miles and Booker, 1994
,
1998
).
In addition to feeding, in several different insects the foregut and FG
play a critical role in at least one other aspect of insect life history: the
moult (Bounhiol, 1938;
Clarke and Langley, 1963
;
Penzlin, 1971
;
Hughes, 1980a
;
Carlson and O'gara, 1983
;
Bell, 1986
;
Bestman et al., 1997
;
Miles and Booker, 1998
). A
moulting insect displays a stereotypical set of behaviours that culminate in
the shedding of the old cuticle at ecdysis. There are two stages of ecdysis in
which the insect needs to exert pressure on the body wall: during rupture of
the old cuticle, and when expanding the new cuticle and wings after emergence
(Reynolds, 1980
). The
principal mechanism locusts employ for exerting this pressure is to fill the
gut with fluid or air. Jousset De Bellesme
(1877
) was the first to show
that the pronounced enlargement of freshly emerged dragonflies was
accomplished by internal air pressure built up in the digestive tract
(summarized by Allum, 1973
).
Since then, air swallowing during ecdysis has been reported in several insect
species (Cottrell, 1962
;
Carlson and O'gara, 1983
;
Miles and Booker, 1998
;
Hughes, 1980d
). Hughes
(1980d
) reported that the
success of the imaginal ecdysis of the desert locust depends on inflation of
the gut with air.
Bell (1986) suggested that
in M. sexta the FG plays a role in the ecdysis to the adult stage, or
eclosion. The FG was shown to be involved in swallowing air; frontal
ganglionectomy abolished air swallowing immediately and thereby caused defects
in eclosion and in expansion of the wings. Recent work has revealed that the
FG plays a critical role in the successful completion of both larval
(Bestman et al., 1997
) and
adult moults in M. sexta (Miles
and Booker, 1998
). At both stages, the FG controls a foregut motor
pattern that is used first to remove moulting fluids from the space between
the old and new cuticle prior to ecdysis, and second for air swallowing.
In the accompanying paper (Ayali et al.,
2002) we began the characterization of the spontaneous FG motor
pattern in an in vitro preparation isolated from all descending and
sensory inputs. The present study continues this work, and investigates the
generation and characteristics of FG motor outputs in the intact locust in two
distinct and fundamental behaviours, feeding and moulting.
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Materials and methods |
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Locusts were briefly anaesthetized in CO2, and their wings and legs removed. The FG and the nerves leaving it were easily accessible by cutting out a window in the head cuticle (frons), and clearing fat tissue and air sacs as required. Movements of the gut were observed and recorded using a force transducer attached to the oesophagus wall. Extracellular recordings of FG nerves and the activity of a specific foregut dilator (muscle 37) were made with fine (125-175 µm) insulated silver wire and hook electrodes that were electrically insulated with petroleum jelly. Muscles of the abdominal wall (mostly lateral muscle 176) were recorded in order to monitor the ventilation pattern, using bipolar stainless-steel pin electrodes. Data were recorded using a 4-channel differential AC amplifier (Model 1700 A-M Systems), played back in real time and stored on the computer using an A-D board (Digidata 1320A, Axon instruments) and Axoscope software (Axon instruments).
Locust saline consisted of 147 mmoll-1 NaCl, 10
mmoll-1 KCl, 4 mmoll-1 CaCl2, 3
mmoll-1 NaOH, (Frutarom, Haifa, Israel), 10 mmoll-1
Hepes (Biological industries, Bet Haemek, Israel), pH 7.2
(Abrams and Pearson, 1982;
Penzlin, 1985
).
The significance of results was tested using a one-way ANOVA test, followed by Bonferroni test (Instat, GraphPad software inc, San Diego, CA, USA).
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Results |
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The FG motor output varied greatly between preparations. Rhythmic activity, as above, was not always observable, and when present, displayed variations in cycle period as well as in the phase relations between bursts of action potentials recorded from the different nerves.
Effect of the state of the gut on the FG rhythm
When testing for different physiological states of the animal that would
account for the observed variability in the FG motor patterns, we found that
differences in cycle period or burst frequency depended on the amount of food
present in the gut (Fig. 2).
Fig. 2A demonstrates that the
FG burst frequency was significantly higher in animals with food present in
their crop, compared to those with empty crops (0.30±0.04 Hz
versus 0.11±0.04 Hz, respectively, N=12). However, in
cases where the gut was replete with food throughout its length, no FG
bursting activity was recorded. We noted that the slow rhythmic pattern
recorded in locusts with an empty gut was similar to the spontaneous intrinsic
frequency of totally isolated in vitro preparations (0.07±0.03
Hz, N=48) (Ayali et al.,
2002). To further confirm the dependence of cycle frequency on the
state of the gut, we artificially manipulated the crop's fullness state.
Fig. 2B shows an example of
extracellular recording from a FG nerve in a locust with an empty gut, before
(Bi), and after (Bii) injecting petroleum jelly into the crop. It clearly
shows that filling the crop with petroleum jelly increased the burst frequency
(0.36 Hz before versus 0.14 Hz after). These results corroborate the
reported effect of food and the state of the gut on the FG rhythm burst
frequency (Fig. 2A).
|
Interaction of the foregut and the FG with the ventilation
patterns
In our ongoing investigation of the sources of variations in the FG motor
patterns we tested for interactions with another known and important central
pattern generator in the locust. Simultaneous recordings of the locust
ventilation rhythm (monitored by EMG recordings from abdomen wall muscles) and
foregut dilation (monitored by a force transducer attached to the oesophagus)
revealed that the foregut could be active in synchrony with the ventilation
pattern (Fig. 3A), whereas at
other times it showed no rhythmic movements
(Fig. 3B), or a totally
independent motor pattern (Fig.
3C).
|
We further tested the interaction between the foregut and FG pattern with
the ventilation pattern. Fig.
4A shows an example when no independent feeding-related pattern
was observed; the FG rhythmic output was strongly coordinated with the
ventilation rhythm. Cutting the ventral nerve cord between the pro- and
mesothoracic ganglion (where the connectives are relatively long and easy to
reach) resulted in uncoupling of the FG and ventilation rhythms. Disconnecting
the metathoracic ganglion, which is the site of the ventilation central
pattern generator (Bustami and Hustert,
2000) from the FG caused an immediate inhibition of the rhythmic
activity (Fig. 4Bi) followed by
the emergence of a new independent FG pattern within 15 min
(Fig. 4Bii).
|
Moulting-related FG patterns
At the onset of the moult the fifth instar larval abdomen acts as a
ventilatory pump (Hughes,
1980b). Simultaneous extracellular recordings from the abdominal
muscles and MPN show that the ventilation pattern recorded at this stage was
rapid (0.44±0.04 Hz, N=13) and continuous. It was correlated
with the FG efferent nerve output (MPN,
Fig. 5A). When disconnecting
the ventilation central pattern generator (CPG) from the FG (by tightening a
pre-implanted ligature on the connectives between the mesothoracic and the
prothoracic ganglion) the synchronized activity recorded from the FG was
instantly lost (data not present). In order to identify possible neural
pathways in which the ventilation CPG interacts with the FG CPG, we
consecutively disconnected the FG nerves
(Fig. 5). In the control, the
FG rhythmic output was strongly coordinated with the ventilation rhythm
(Fig. 5A). Cutting the
recurrent nerve (RN) resulted in the appearance of new rhythmic bursts of
action potentials that seemed to be independent of the ventilation-coupled
activity (Fig. 5B). Further
cutting of the two frontal connectives (practically isolating the ganglion
in situ) and subsequent repeated superfusion with saline, caused
uncoupling of the two CPGs and emergence of an FG rhythmic pattern that
resembled the output of the FG efferent nerves in the in vitro
preparation (Fig. 5C).
|
When locusts were collected at a very precise time point, after the animal
had found a perch for moulting and moved to an upright position, simultaneous
FG and ventilation recordings revealed that the very consistent
ventilation-synchronized pattern had changed. The totally synchronized pattern
gave rise to alternation between rapid bursts of FG activity (0.74±0.06
Hz, as recorded from muscle 37, N=3) and bouts of ventilation
(Fig. 6). At this point the
locust has switched to air swallowing behaviour (our observations;
Hughes, 1980a). The time
window in which air swallowing behaviour is exhibited is very limited, so it
was practically impossible to record the nervous activity during this
behaviour.
|
In the different preparations studied (N=19) the ventilation burst
frequencies ranged from 0.4 Hz before the onset of air swallowing behaviour,
to 0.7 Hz at the time the old cuticle split. As the old cuticle ruptured and
the thorax started to emerge, a unique pattern of activity appeared in which
the abdomen periodically contracted in long squeeze-like bouts that exerted
pressure on the old cuticle (recorded as long periods of tonic, high frequency
firing; Fig. 7A). Following the
emergence of the pro- and mesothoracic legs and the proceeding of the moult,
the described squeezing pattern increased in duration and a variable number of
fast ventilatory strokes occurred at the end of each tonic compression
(Fig. 7B,C).
Fig. 7D summarizes squeeze
duration (the duration of the first and longest tonic episode in each cycle)
and cycle period during these different behaviours. As in the onset of the
moult, the FG pattern closely followed all the changes in the ventilation
pattern, from the vigorous abdominal contractions to the later tonic
compression pattern with the changes in duration of tonic compression,
throughout the expansion phase of the new adult, as described by Hughes
(1980c).
|
Next we wanted to test whether the reason for the transient uncoupling of the FG and ventilation patterns described above is indeed the emergence of the air-swallowing behaviour. In the example shown in Fig. 8A the adult locust has fully emerged, and is occupied in expanding its wings (as in Fig. 7C). At this stage, we punctured the inflated gut by simply inserting a syringe needle through the cuticle and the wall of the crop. As can be seen in Fig. 8B, this caused a marked change in the interaction between the FG and ventilation patterns. The FG rhythm switched from full synchrony between the activity recorded from the different nerves and the ventilation pattern, to a new and different rhythmic pattern. This new pattern resembled the air-swallowing burst frequency (0.60±0.09 Hz for 10 consecutive bursts, compared to 0.74±0.06 Hz, respectively), as well as the described feeding-related behaviour (i.e. a rostral-to-caudal phase relation; Fig. 1), although the latter was much slower. The independent FG rhythm was interrupted at every squeeze-like contraction of the abdomen. The new air-swallowing pattern developed rather progressively and the number of bursts within a bout gradually increased (Fig. 9). The pattern went through fluctuations, probably reflecting fluctuations in air pressure in the punctured gut, as the locust refilled it with air and lost the air again through the punctured crop.
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Discussion |
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In this work we gained a first insight into the role that the multifunctional FG CPG plays in two distinct and fundamental behaviours, feeding and moulting. We have begun to investigate the different rhythmic patterns demonstrated by the FG in these different behavioural contexts.
We have shown that the amount of food present in the gut modulates the
frequency of the FG rhythm. In a feeding locust the motor patterns of the
foregut work to push food backwards to the crop and empty the crop toward the
midgut. In cases when the entire gut seemed to be replete with food, these
feeding-related patterns were inhibited altogether and no corresponding
rhythmic activity could be recorded from the FG nerves. Volumetric feedback
from the gut has been reported elsewhere: in the fly, sensory information
mediated via stretch receptors from the gut-wall has been shown to be
instrumental in the control of feeding (summarized by
Möhl, 1972). Simpson
(1983
) showed in locusts a
system in which volumetric feedback from the crop and hindgut interacts in the
regulation of meal size. Clarke and Langley
(1963
) concluded that in
L. migratoria the FG forms a link in the passage of nervous impulses
originating from the stretch receptors of the pharynx and passing via
the posterior pharyngeal nerve, FG and frontal connectives to the brain. In
M. sexta the pattern of foregut activity has also been shown to vary
with the amount of food present in the foregut and crop
(Miles and Booker, 1994
).
Ascending signals of sense organs (e.g. stretch receptors) could either
produce inhibition directly or generate central inhibition
(Griss et al., 1991
).
FG pattern alteration could also work via neuromodulators or
humoral factors. Release of humoral factors that have a role in the cessation
of locust feeding and involvement of chemoreceptors of the foregut have
already been suggested by Bernays and Chapman
(1973). In the adjacent paper
we have shown that application of haemolymph (taken from animals with a very
full gut or from animals just before the moult) to the FG in vitro
abolished the rhythm completely. In contrast, haemolymph from feeding locusts
had no inhibitory effect. We also showed that the rate of appearance of the FG
rhythm in an in vitro preparation is dependent on the physiological
state of the donor locust, suggesting washout of some modulatory humoral
factors. Various neuromodulators have been traced to FG neurons, some of which
are known to modulate gut activity (Duve et al.,
1995
,
1999
,
2000
;
Miyoshi and Endo, 1998
;
Maestro et al., 1998
). These
factors could in turn have an effect upon the FG circuits themselves.
When no feeding-related foregut pattern was observed, the FG motor output
was strongly correlated with the locust's ventilation pattern. Other workers
have showed that in locusts, as in other insects, ventilation interacts with
other motor systems (Miller and Mills,
1976; Paripovic et al.,
1996
; Ramirez,
1998
). Our experiments reveal that the full synchrony between the
FG and ventilation rhythms can be switched off, which suggests a hierarchical
relationship between the ventilation and foregut motor patterns. Gut movements
can be recruited to participate in ventilation, probably as a means of helping
with haemolymph circulation. Recent work on the neural pathways of cardiac
reflexes in lepidopterous insects shows that the heartbeat can be triggered by
stimulation of axons in the visceral nerve arising from the FG
(Kuwasawa et al., 1999
). We
still lack evidence for such a direct interaction between the FG and
ventilation. We hope to gain more information by focusing on the FG and
ventilation CPGs during the moult.
As the moult approaches, the last larval instar locust ceases to feed
(approximately 24h prior to shedding of the old cuticle)
(Hughes, 1980a). The abdomen
acts as a ventilatory pump, performing characteristic movements that may help
to loosen the old cuticle. We have shown that the FG ventilation-CPG
interaction is dominant all through the different stages of the moult. The
full synchrony between the FG and ventilation rhythms is only momentarily
switched off at the specific stage of air swallowing. By filling the gut with
air, the larval locust can generate enough internal pressure to split open the
old cuticle (Bernays, 1972
). As
the gut fully inflates, the FG pattern returns to demonstrate synchrony with
the ventilation rhythm. This lasts all through the `expansional motor program'
(Hughes, 1980c
) that serves to
expand the new cuticle into its final form and to expand the wings.
The gut remains inflated until the end of the moult
(Hughes, 1980d). Deflating it
induces uncoupling between the FG and the ventilation patterns. The locust
senses that the gut is loosened and switches its behaviour from full
synchronization to a new pattern that correlates to air swallowing activity.
Very much like the feeding-related pattern (only faster), the air-swallowing
pattern is characterized by a rostral-to-caudal phase delay between bursts of
activity recorded on the different FG nerves, which generate a wave of
anterior-to-posterior peristalsis in the foregut. Hence, our results support
Hughes's (1980d
) suggestion
that the air-swallowing motor program is regulated by the degree of foregut
distension. Its frequency is correlated with the degree of gut inflation, and
may be controlled, at least in part, by receptors located on the foregut.
Miles and Booker (1998)
reported that in adult M. sexta, the FG is activated about 6 h before
the adult emerges from the pupal case. The crop initially fills with moulting
fluids, then with air. After eclosion, as the moth hangs in a position to
expand its wings, the FG is again activated, producing a distinct
air-swallowing motor pattern that lasts about 1.5 min. During this period, the
wings visibly expand. The motor pattern recorded from the FG at air swallowing
was similar to that displayed during feeding
(Miles and Booker, 1998
). As
mentioned above, we have also observed many similarities between the FG
rhythms recorded during locust feeding and air swallowing.
The elaborate and complex nervous connectivity pattern of the locust
stomatogastric nervous system offers many alternative routes between the
foregut or the thoracic ventilation CPG to major neuroendocrine centers (e.g.
corpora cardiaca) on the one hand, and the central nervous system on the other
(Allum, 1973). Thus, at present
we do not know the sources of the neuromodulators and the routes of modulation
of the FG rhythmic motor patterns.
To summarize, the locust FG can generate two major types of motor patterns, which can be defined with relation to the ventilation pattern: the first, synchronized and the other, uncoupled (Fig. 10). In feeding adults or mid-instar larvae the `feeding related pattern', uncoupled to or independent of the ventilation pattern (Fig. 10Aii), is generated whenever food needs to be passed through the foregut. At other times the synchronized pattern is demonstrated (Fig. 10Ai). In moulting animals, the synchronized pattern is dominant throughout the different stages of the moult (Fig. 10Bi). The uncoupled pattern can transiently take over for specific, brief periods when the animal switches to the air-swallowing behaviour (Fig. 10Bii). Both types of motor patterns can probably be centrally modulated. The uncoupled pattern is volumetrically controlled by the foregut. Interestingly, we were able experimentally to induce a switch from the synchronized pattern to the uncoupled one, but not vice versa.
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Further identification and characterization of the locust FG central pattern generator network is required in order to conclusively determine whether the two uncoupled patterns (feeding and air swallowing) are comparable, and whether they are generated in a similar way. This work is currently in progress.
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Acknowledgments |
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