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Modulation of tension production by proctolin in the dorsal longitudinal muscles of the cricket Teleogryllus oceanicus.

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Archives of Insect Biochemistry and Physiology 14:71-83 (1990)
Modulation of Tension Production by Proctolin
in the Dorsal Longitudinal Muscles of the
Cricket, Teleogryllus oceanicus
Bruce A. O'Gara
Department of Zoology, Iowa State University, Ames, Iowa
High-frequency electrical stimulation (-20 Hz) of the lateral nerve in abdominal segments of the cricket, Tileogryh oceanicus, caused an increase in tonus
of the abdominal dorsal longitudinal muscle (DLM). This effect persisted for
1-5 min following stimulation. Application of the pentapeptide proctolin
(threshold 1-10 nM) mimicked the increase in muscle tonus produced byelectrical stimulation. Individual twitches were unaffected or slightly reduced by
proctolin. Low-frequencyelectrical stimulation (<7 Hz) of the lateral nerve counteracted a previously induced increase in muscle tonus, apparently by activation of an inhibitory motoneuron. y-Aminobutyric acid (CABA) mimicked the
effect of low-frequency stimulation and reduced muscle tonus. Octopamine,
in concentrations of ~ 0 . mM,
was inactive on the abdominal DLM when stimulated at low frequencies (0.5-2 Hz). Application of proctolin to the rnetathoracic DLM caused an increase in twitch amplitude but had little effect on
basal tonus. In conjunction with the previously described responses of the
metathoracic DLM to octopamine, these results show that the serially homologous abdominal and metathoracic DLMs have dissimilar responses to the
modulators proctolin and octopamine.
Key words: octopamine, CABA, differentiation, insect
The abdominal dorsal longitudinal muscle of the cricket Teleogryllus oceanicus
is specialized for relatively slow movements and postural control of the abdomen [l-41.In contrast to the abdominal dorsal longitudinal muscle (DLM),"
*Abbreviations used: DLM = dorsal longitudinal muscle; DUM = dorsal unpaired median;
EJP = excitatory junctional potential; GABA = y aminobutyricacid; IJP = inhibitory junctional
Acknowledgments: I thank Dr. C.D. Drewes and Dr. W.O. Friesen for critical comments on
the manuscript. I also thank Dr. A.E. Kammer for a gift of proctolin.
Received December 4,1989; accepted March 6,1990.
Dr. Bruce O'Gara is now at Department of Biology, University of Virginia, Charlottesville, VA
22901. Address reprint requests there.
Q 1990 Wiley-liss, Inc.
the metathoracic DLM is specialized for the rapid contractions that power wing
movements [5,6]. The metathoracic DLM responds to octopamine by producing
increases in twitch amplitude, contraction rate, and relaxation rate. The receptor
mediating these responses has been shown to be an octopaminel receptor [ 6 ] .
Proctolin-responsive muscles show several distinct types of response to
proctolin. One type of response is characterized by a proctolin-induced increase
in basal tonus [7,8]. This maintained tension is also known as a lingering tension or “catchlikd’ contraction 191. In contrast, a second type of response to
proctolin is characterized by increased twitch amplitude but little change in
basal tonus [lo-121.
Another important neuromodulatory substance, octopamine, is active on
several arthropod neuromuscular systems (for review, see David and Coulon
[13]). Octopamine increased the amplitude and relaxation rate of twitches
induced by both slow [14] and fast motoneurons [6,15]. The apparent sources
of octopamine for these muscles are (DUM) neurons. Although DUM neurons occur in the abdominal ganglion [16], it is not known whether the abdominal DLM is innervated by one of these octopaminergic neurons or whether
tension production is modulated by octopamine.
The purposes of this study were (1)to study the neural modulation of evoked
twitches and basal tonus in the abdominal DLM; (2) to determine the effects
of octopamine, proctolin, and GABA on tension production in the abdominal
DLM; and (3) to examine the effects of proctolin on the metathoracic DLM. A
brief report of some of these results has been previously published [17].
The care and feeding of Teleogryllus oceanicus have been previously described [6].
Abdominal DLM Dissection and Experimental Procedures
For experiments involving the abdominal DLM, the cricket was decapitated
and the thoracic segments discarded. The abdomen was opened with a middorsal incision, and the gut was removed. To reduce spontaneous movements,
the nerve cord was removed in most experiments. The fat and air sacs overlying
the abdominal DLM were carefully removed (see Carlson [3] for a description of
the abdominal musculature of T. oceunicus). The exoskeletal attachment of the
anterior end of the abdominal DLM was pinned to the bottom of the dissecting
dish. To monitor muscle tension, a minutien pin, attached to a tension transducer (Narco Biosysterns F50, Houston, TX), was positioned to contact the
posterior exoskeletal attachment of the abdominal DLM. The force transducer
was positioned for optimally recording twitch amplitude. This method, involving semi-isometricmonitoring of tension, was found superior to attaching the
transducer to the isolated posterior attachment of the DLM because the required
isolation procedure greatly reduced the viability of the preparation. Experiments were performed using all abdominal segments except the first and the
highly modified, fused posterior segments. No differences were noted in the
responses of the abdominal DLM in any of the segments used.
Modulationof Tension in the DLM
To study neurally evoked responses of the abdominal DLM, the lateral nerve
was electrically stimulated with a suction electrode. Tension records were monitored on an oscilloscope or chart recorder (Brush RD 1684-00 or Gould 2200S,
Cleveland, OH). Saline or drugs were usually superfused over the preparation
at 0.75 mumin, a rate that exchanged the fluid volume covering the preparation every few seconds. During experiments using GABA (see Figs. 5 , 78),the
perfusion system was not used, and drugs or saline changes were applied
from a pipette. This method permitted more exact control of the timing of
drug application.
Metathoracic DLM Experimental Procedures
The procedures used during experiments on the metathoracic DLM have
been previously described [6]. Briefly, the posterior muscle attachment was
isolated from the exoskeleton and attached to the transducer, which measured
isometric tension. Muscle twitches were evoked by stimulation of the four DLM
motoneurons in mesothoracic nerve 6 [18] with a suction electrode.
Electrophysiology, Saline, and Drugs
Intracellular electrical activity from the muscle was recorded using borosilicate glass microelectrodes filled with 1M K acetate (15-40 M a resistance). The
composition of the saline was identical to that of OGara and Drewes [6]. Drugs
were purchased from Sigma (St. Louis, MO). The experimentswere conducted
at room temperature (21-25°C).
Innervation of the Abdominal DLM
Electrical stimuli applied to the lateral nerve evoked a large, overshooting
response in DLM muscle fibers (Fig. 1A). The response was recruited in an
all-or-none fashion and was accompanied by an observable twitch. In the
absence of stimulation when the nerve cord was present, several smaller
spontaneous EJP (Fig. 1B,C) and an inhibitory junctional potential (IJP)
were also observed (Fig. 1D). The small EJPs often occurred during respiratory
movements of the abdomen. When the lateral nerve was transected all spontaneous activity ceased (not shown). The pattern of innervation by the neurons producing these small junctional potentials was not studied in detail.
However, the size and number of junctional potentials appeared similar to
those in the grasshopper abdominal DLM 1191.
Effects of Octopamine on the Abdominal DLM
Application of octopamine at concentrations of 0.1-100 pM (n = 5) caused
no detectable effect on twitches evoked by 0.5-2 Hz neural stimulation or on
basal tonus at stimulation rates of 0-2 Hz (not shown). Aside from the absence
of octopamine receptors, another explanation for this result is that octopaminergic neurons (presumably in the lateral nerve) may have been inadvertently stimulated. Thus, the abdominal DLM may have already been maximally
facilitated before exogenous octopamine was applied. To test this idea, the
octopamine antagonist metoclopramide 16,201 was applied to the preparation
Fig. 1. Synaptic potentials in the abdominal DLM. (A) A single stimulus delivered to the
lateral nerve elicited a fast muscle spike. Spontaneous excitatory responses (B,C) and IJPs (D)
were also recorded. The largest spikes in B were apparently evoked by the same motor
neuron activated in A. Voltage scale: (A), (B), (D) 10 mV; (C) 5 mV. Time scale: (A) 5 ms; (B),
(D)100 ms; (C)50 ms.
at a concentration of 0.1 mM for periods of 630 min. Metoclopramide produced no reduction of neurally induced twitches (n = 6), suggesting that no
inadvertent octopaminergic modulation of the abdominal DLM had occurred.
Neural Modulation of Basal Tonus
The possibility that basal tonus could be predictably modulated by neural
stimulation was examined by repetitive stirnulation of the lateral nerve at various frequencies. As shown in Figure 2, stimulation at 20 Hz for 3 s caused an
increase in basal tonus which outlasted the neural stimulation for up to 5 min.
As shown in Figure 2B, the increase in tonus was dependent upon stimulus
frequency. In most preparations, the lowest stimulation frequency which
increased tonus was -7 Hz, corresponding approximately to the frequency
that just caused incomplete tetanus (ix., the frequency of stimulation at which
the muscle did not return to resting tension between twitches). Lower stimulus frequencies (i.e., those producing no fusion of individual twitches) caused
a reduction of tonus (Fig. 2). Muscle membrane potential during neurally
induced increases in basal tonus was usually unchanged, but occasionally a
slight depolarization of <5 mV occurred (several fibers from each of six preparations were sampled) (Fig. 3). Since these small depolarizationswere unusual,
they may be the result of movement artifacts.
In a few preparations, distinct stimulus voltage thresholds were found for
increasing or decreasing tonus (Fig. 4). In these preparations, low-frequency
(2-Hz)stimulation produced substantialincreases or decreases in tonus depending on stimulation voltage (Fig. 4B). The intracellular electrical correlate for
the decrease in tonus was a threshold-dependent hyperpolarizing potential
that followed the fast spike (Fig. 4C). The amplitude and duration of this potential appeared similar to those of the spontaneously occurring IJPs (Fig. 1D).
This hyperpolarizing potential can also be seen in Figure 3 (trace i) as a small
deflection below baseline during the stimulation-induced reduction in tonus.
Modulation of Tension in the DLM
2 0 Hz
2 Hz
Fig. 2. Modulation of tonus by stimulation of the lateral nerve. (A) Stimulation at 20 H t for 3 s
(bar) produced a large phasic contraction. After termination of stimulation, muscle tonus was
elevated. Near the end of the record, stimulation at 2 Hz evoked twitches and a decrease of
tonus. (B)At the beginning of the record the lateral nerve was stimulated at 20 Hz for 3 s (bar).
Tonus was then reduced by2-Hz stimulation. Stimulation at 30 Hz for 3 s evoked a larger increase
of tonus compared to 20-Hz stimulation. The increase of tonus was then counteracted by 3-Hz
stimulation of the lateral nerve. The variation in the width of the trace was caused by vibration. Time scale: 15 s . Tension scale: 75 mg.
Fig. 3. Membrane potential during neurally induced changes of tonus. The bottom trace (t)
shows tension of the abdominal DLM. Muscle tonus was increased by 20-Hz stimulation for 3 s
(bar) and counteracted by 2-Hz stimulation. The top trace (i)shows muscle membrane potential during changes of tonus. A series of fast muscle spikes (peaks clipped by amplification),
evoked during 20-Hz stimulation, was followed by -5 mV depolarization that accompanied the
increase of tonus. This was the largest sustained shift of membrane potential in any preparation. Voltage scale: 10 mV. Time scale: 5 s. Tension scale: 75 rng.
Fig. 4. Thresholds for changing tonus. (A) The first and third twitches were elicited by a single pulse and were followed by a reduction of tonus. The second twitch, elicited by a slightly
lower stimulus voltage, was followed by an increase of basal tonus. (B) Large increases or
decreases of tonus were produced during 2-HZ stimulation by alternating between the stirnulusvoltages in A. (C) The intracellular correlate (i)for the decrease of tonus was a hyperpolarizing
potential that follows the fast muscle spike. Threshold for the hyperpolarization was identical
to the threshold that produced a decrease of tonus in A and B. In the tension record (t) a
slightly faster muscle relaxation occurred following the hyperpolarizingpotential. Voltage scale:
10 mV. Time scale: (A) I s; (B)2 s; (C) 50 ms. Tension scale: 150 mg.
Role of GABA in Regulating Tonus
If the hyperpolarization that accompanied the decrease in tonus was caused
by the inhibitory neurotransmitter GABA, application of GABA should cause
a similar decrease in tonus. In each of eight preparations, GABA application
caused marked reductions of tonus (Fig. 5A).
Further evidence that neurally induced reductions of tonus were mediated
by GABA was obtained by application of the GABA antagonist picrotoxin. Exposure of the abdominal DLM to 1mM picrotoxin for 10 min blocked the reduction of basal tonus normally produced by 2-Hz stimulation of the lateral nerve
(n = 10) (Fig. 58). Taken together, these results suggest that the reductions of
tonus in the abdominal DLM are mediated by the release of GAM from an
inhibitory motoneuron.
Proctolin applied to the abdominal DLM caused increased tonus (Fig. 6),
thus mimicking the increase of tonus produced by repetitive neural stimulation
(see Fig. 2). The effects of proctolin were dose dependent at concentrations
between 1nMand 1pM (n = 6) (Fig. 6). Concentrations >1pM were not used.
Proctolin-inducedincreases of tonus were also antagonized by lateral nerve
stimulation at 2 Hz (n = 3) (Fig. 7A). However, 2-Hz lateral nerve stimulation
did not cause relaxation of the abdominal DLM to baseline tension. Application of 1mM GABA completely antagonized the effect of 1 pM proctolin (n =
5 ) (Fig. 7B). Following GABA application, tonus remained reduced for at least
5 min, even though proctolin was still present in the bath.
Modulation of Tension in the DLM
i - 24H 1
Fig. 5. Effects of GABA in modulating tonus. (A) Muscle tonus was increased by stimulating
the lateral nerve at 20 Hz for 5 s (bar). Addition of 0.3 ml saline had no effect, but 0.3 ml of
1 mM GABA produced a reduction of tonus. (B) Neurally induced changes of tonus were
blocked by picrotoxin. During a control period (1)an increase of tonus was produced by stirnulation at 20 Hz for 5 s (bar) and a reduction of tonus was induced by 2 Hz stimulation. Ten
minutes after picrotoxin (1 mM) treatment (2), an increase in tonus was produced by 20-Hz
stimulation (bar) but the normal reduction of tonus by 2-Hz stimulation was blocked. Time
scale: 30 s. Tension scale: 100 mg.
Fig. 6. Effects of proctolin on tonus of the abdominal DLM. Proaolin was applied at the first arrow
and was washed off at the second arrow. A dose-dependent increase of tonus was evident. Bars
on each panel indicate equivalent amounts of tension. Time scale: 5 rnin. Tension scale 150 mg.
2 Hz
Fig. 7. Termination of proctolin-induced increases of tonus. (A) An increase of tonus was
produced by addition of 0.3 rnl of 1 FM proctolin. Muscle tonus was then reduced by 2-Hz
stimulation of the lateral nerve. (6)The proctolin-induced (1 FM) increase of tonus was
reversed by GABA (0.3 rnl of 1 rnM) but was unaffected by saline (0.3 rnl). Time scale: 2 min.
Tension scale: 200 mg.
Effect of Proctolin on Neurally Induced Twitches
To examine the effects of proctolin on twitches of the abdominal DLM, the
lateral nerve was stimulated at 0.5 Hz, a frequency that normally caused no
change of basal tonus. When proctolin was applied to the preparation, tonus
increased and twitches were superimposed on this increase of tonus (Fig. 8C).
Comparison of twitches, before and after proctolin application, showed either
no effect (2 of 5 preparations) (Fig. $A) or a slight reduction in amplitude (3 of
5 preparations) (Fig. 8B). The maximal effect of proctolin in any preparation
was a 23%reduction in twitch amplitude (Fig. 8B,C).
Effect of Proctolin on the Metathoracic DLM
In contrast to the metathoracic DLM [6], the abdominal DLM was insensitive
to octopamine. Thus it was of interest to determine if the two muscles also
differed in their responses to proctolin. Within 1min of application of proctolin
to the metathoracic DLM, a clearly observable increase in twitch tension
occurred (Fig. 9). Twitch amplitude continued to increase for as long as proctolin
was applied (S10 min).The threshold concentrationwhich produced an increase
in twitch amplitude was -0.1 pM. At 0.1 pM, twitch amplitude was increased
by8.9 k 3.5%(mean k SEM) (n = 3) while contractionand relaxationrates were
unchanged. At 1FM twitch amplitude was increased by92.3 2 18.6%,contraction rate by 50.6 k 13.3%,and relaxation rate by 31.2 21.1% (n = 3). These
effects persisted for at least 2 h after exposure to 1pM proctolin.
The pharmacological responses of the abdominal DLM contrast markedIy
with those of the metathoracic DLM. While proctolin application to the abdom-
Modulationof Tension in the DLM
Fig. 8. Effect of proctolin on twitches of the abdominal DLM.(A$) Two superimposed twitches
are shown, one prior to proctolin application and the other near the end of 7-to 8-min proctolin
exposure. Baselines were adjusted to nullify the proctolin effect on muscle tonus. (C) The effects
of 0.1 pM proctolin on both basal tonus and twitches are shown. Proctolin was applied at the
first arrow and washed off at the second arrow. The deflection at the second arrow i s an artifact of saline change. In some preparations, proctolin either had little or no effect on twitches
(A) or in other preparations produced a decrease of twitch amplitude (6,C). (C)Time scale: 50
ms (A$), 2.5 min (C). Tension scale: 15 mg (A$), 45 mg (0.
inal DLM produced an increase of tonus (Fig. 6),it did not greatly affect twitch
amplitude. However, in contrast to the abdominal DLM, proctolin application
to the metathoracic DLM caused an increase of twitch amplitude (Fig. 9). The
concentrations of proctolin necessary to produce measurable effects on the
metathoracic DLM were relatively high for a peptide neuromodulator. However, the physiological relevance of the proctolin response is suggested by the
finding that the proctolin-induced facilitation of twitch amplitude (at 1 pM)
was similar to the maximal amount of facilitation produced by octopamine or
its agonists [6].
High-frequency stimulation of the lateral nerve produced a "catchlike" tension in the abdominal DLM (see Fig. 2). Unfortunately, the use of the term
"catch' has become imprecise in the literature [21-241. Such increases of tonus
may not be called catch contractions but may be termed only "catchlike"
because these contractures have not met the criteria fordefining catch [9]. Catch
Fig. 9. The effect of proctolin on the metathoracic DLM. (A) Traces I show twitch tension
(lower) and differentiated twitches (upper) prior to proctolin application. Contraction rate is
indicated by downward deflections and relaxation rate is indicated by upward deflections. Traces
2 show these parameters after application of 1 IJ.Mproctolin. (B)The response of the same preparation to 1 M proctolin was recorded at a slow paper speed. Due to the slow paper speed
individual contractions are not evident in either the tension (t) or differentiated (d) records.
Note that the differentiated signal is inverted compared with A. Contraction rate is indicated
by deflections above the white line, and relaxation rate is indicated by deflections below the
line. In this preparation, twitch amplitude was increased by 105.9% and contraction rate by
52.4%, but relaxation rate was not facilitated. Time scale : (A) 20 ms; (6)2 rnin. Tension scale:
0.4 g. Differentiated traces: (A) 2 8.s-I; (6) 1 g.s-l.
is characterized by an extremely strong resistance to stretch during and after
initial shortening. Once the muscle is in catch no further shortening occurs. It
is unknown whether the abdominal DLM exhibits these properties of catch.
Until a preparation (e.&.,the abdominal DLM) has satisfied the formal critiera
of catch, alterations of maintained tension would be more productively referred
to as alterations of basal tonus.
Low-frequency stimulation caused decreases of muscle tonus (see Fig. 2).
Modulation of Tension in the DLM
The intracellular event that correlated with reductions of abdominal DLM tonus
was a hyperpolarizing potential (Fig. 4C), similar in size and duration to spontaneous inhibitory junctional potentials. GABA mimicked the effects of low
frequency stimulation and reduced muscle tone, regardless of whether the
increase of tonus was induced by proctolin or lateral nerve stimulation
(Figs. 5A, 7B). Likewise, GABA antagonizes proctolin-induced increases of
tonus in lobster skeletal muscle [25]. These results suggest that decreases of
tonus in the abdominal DLM were produced by an inhibitory motoneuron.
Similar actions of inhibitory motoneurons have been described in other
arthropod muscles [8,21-22,241.
Increases of tonus in the cricket abdominal DLM were induced by highfrequency stimulation, but with little change in muscle membrane potential.
Similar effects of high-frequency stimulation have been seen in the cockroach
coxal depressor muscle [21] and locus extensor tibiae 1221. More recent evidence indicates that both muscles are innervated by motoneurons that use
1-glutamateand proctolin as co-transmitters, with 1-glutamateinitiating twitches
and proctolin causing increased tonus [7,8,26]. A similar situation may exist
in the abdominal DLM.
Proctolin usually had no effect or slightly reduced the amplitude of abdominal DLM twitches without affecting twitch duration (Fig. 8). This contrasts
with the prolongation of the relaxation phase of twitches in the cockroach
coxal depressor treated with proctolin [7]. This apparent difference between
the abdominal DLM and the cockroach coxal depressor may be an artifact.
Inhibitory motoneurons are known to shorten the relaxation phase of muscle
contractions [27-291. In most abdominal DLM preparations, an inhibitory
motoneuron was unavoidably stimulated along with the unit(s) that produced
the twitches and increases of tonus, since both units had similar thresholds
(see Fig. 4). In those abdominal DLM preparations in which activation of the
inhibitor could be avoided (see Fig. 4), twitch duration was increased as
compared to when inhibitory motoneurons were activated.
Although it is unknown whether the abdominal DLM motoneurons contain proctolin, several neurons in the same general location as the abdominal
DLM motoneurons [30]exhibit proctolin-like immunoreactivity in the cockroach [31]. An additional indication that proctolin is involved in abdominal
muscle function is the localization of a proctolin-like peptide in abdominal
muscles of the Colorado potato beetle [32], cockroach [33],and Drosophila [34].
Further work is needed to determine if the T. oceanicus abdominal DLM
motoneurons contain and release proctolin.
The abdominal DLM was unresponsive to octopamine at concentrations of
CO.1 mM when stimulated at frequencies that do not produce tetanus. This
contrasts with the high sensitivity of the serially homologous metathoracic
DLM to octopamine [6]. The absence of octopamine sensitivity in the abdominal DLM may be explained in several ways. First, octopaminergic innervation
of the abdominal DLM may not exist. Although octopaminergic DUM neurons exist in the abdominal ganglia, the peripheral sites of innervation by these
DUM neurons are unknown [16]. Second, octopaminergic inputs onto the
abdominal DLM may exist but may have been stimulated during capture and
dissection [ZO], or by electrical stimulation. Since the octopamine antagonist
metoclopramide did not reduce twitch amplitude, this suggests twitch amplitude potentiation had not occurred prior to octopamine application. However,
since the antagonistic effect of metoclopramide is only due to competition for
binding sites, it would not antagonize a long-lasting process induced by endogenous octopamine before the application of metoclopramide. It remains possible that if the abdominal DLM were activated by stimulation of single identified
motoneurons rather than by stimulation of the whole lateral nerve, specific
octopamine effects may be revealed.
The results presented in this paper as well as those of OGara and Drewes
[6] show that these two serially homologous muscles have differential pharmacological sensitivities to octopamine and proctolin. Since both DLMs are
innervated by serially homologous motoneurons, it is possible that the expression of neurotransmitter types by these neurons may also be different. The
different responses of the two DLMs to proctolin suggest that the differential
modulation of tension production occurs through distinct intracellular mechanisms. The developmental factors responsible for phenotypic differences in
the quantitative or qualitative properties of these two serially homologous neuromuscular systems are unknown but probably represent an important general mechanism by which segmental specializations are produced.
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