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First published online March 30, 2006
Journal of Experimental Biology 209, 1385-1394 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02114
Dual inhibition of the dactyl opener muscle in lobster
Department of Neuroscience, University of Virginia, PO 801392, Charlottesville, VA 22908, USA
* Author for correspondence (e-mail: mkw3k{at}virginia.edu)
Accepted 19 January 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: inhibition, dactyl opener, lobster, crustacean, CI, common inhibitor, Homarus americanus
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Bykhovskaia et al., 2004;
Dudel and Kuffler, 1961;
Parnas et al., 2000;
Vyshedskiy et al., 1998;
Vyshedskiy and Lin, 2000;
Worden et al., 1995;
Worden et al., 1997;
Zucker, 1973). In part, the
popularity of this neuromuscular system among physiologists arises from the
simplicity of its neural innervation. In astacuran species (lobsters and
crayfish), neural innervation is supplied both by a specific opener excitor
axon (OE) and a specific opener inhibitor axon (OI) as well as a common
inhibitor axon (CI) that also supplies inhibition to all the other limb
muscles (reviewed in Wiens,
1989). It has been well established that the innervation patterns
of OI and OE motoneurons are coextensive; the muscle fibers of the opener are
100% tonic (Mearow and Govind,
1986), and OI and OE supply all of them
(Govind, 1995;
Marmont and Wiersma, 1938;
Van Harreveld, 1939).
However, the extent to which CI innervates the fibers of the dactyl opener
is not clear. In the dactyl opener of the crayfish Procambarus
clarkii, CI elicits synaptic responses only in a small number of the most
proximal muscle fibers and exerts a weaker physiological effect than does OI,
suggesting that CI does not innervate the bulk of the opener muscle
(Wiens, 1985;
Wiens, 1989). This type of
restricted innervation pattern contrasts sharply with the arrangement in the
brachyuran crab species Eriphia, where CI innervates all the fibers
of the dactyl opener muscle (Wiens et al.,
1988). In the lobster Homarus americanus, Wiens confirmed
dual inhibitory innervation of the dactyl opener by both OI and CI for a small
number of fibers in the proximal region
(Wiens, 1990). However, that
study did not examine whether CI, like OI, makes synaptic contacts along the
entire proximal–distal extent of the muscle.
The issue of whether CI does, in fact, supply only a small region of the
muscle is an important consideration for understanding its functional role in
astacurans. The physiological role of the specific inhibitor OI has always
been considered in the context of the excitor OE, with which it is closely
associated anatomically and with which it shares all innervation targets. OI
exerts both postsynaptic and presynaptic inhibition in the dactyl opener
system (reviewed in MacDermott et al.,
1999). Since OE supplies the dactyl opener as well as the
stretcher muscle, it seems likely that OI serves to moderate OE signaling to
the opener and enable independent function by the stretcher, as first
suggested by Marmont and Wiersma (Marmont
and Wiersma, 1938). By contrast, the physiological role of CI is
less clear. Its physiological effects are reported to be weak compared with
those of OI (Wiens, 1985;
Wiens, 1993), however as it
supplies all limb muscles it is thought to facilitate alternating contractions
of antagonistic muscle pairs (Ballantyne
and Rathmayer, 1981; Wiens,
1989).
In the present study, we examine the innervation pattern of CI in the lobster dactyl opener and compare the physiological effectiveness of CI and OI in inhibiting the dactyl opener neuromuscular system. In contrast with previous studies on decapod crustaceans, we find that CI innervates fibers along the entire length of the dactyl opener. Further, we find the physiological impact of CI and OI to be strikingly similar: both relax muscle to a comparable extent, and each inhibits synaptic responses and muscle contractions stimulated by the excitatory motoneuron OE.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Methods for intracellular recording of synaptic potentials are as described
previously (Worden et al.,
1995). Each of the three axons innervating the dactyl opener was
drawn into a separate suction electrode and stimulated (stimulator model S88;
Grass-Telefactor, West Warwick, RI, USA) with brief (1–3 ms) stimuli
sufficient to elicit synaptic responses in the dactyl opener muscle. In the
carpus, the axon of the opener motoneuron OE was stimulated via the
nerve that innervates the stretcher muscle (arrow 1,
Fig. 1), and the axon of the
inhibitor OI was stimulated by dissecting the OI axon from the main nerve
trunk (arrow 2, Fig. 1). The
axon of the inhibitor CI was stimulated in the propus via a nerve
branch that innervates the dactyl closer muscle (arrow 3,
Fig. 1)
(Wiens, 1990). Intracellular
recordings of synaptic potentials in the muscle fibers of the dactyl opener
were made using glass microelectrodes filled with 3 mol l–1
potassium acetate and a Neuroprobe (A-M Systems, Carlsborg, WA, USA) amplifier
and filtered at 100 Hz. At 2°C, synaptic responses to OE were
depolarizing, while responses to OI and CI were hyperpolarizing. In every
recording we verified that stimulation of OI and CI generated synaptic
responses that could be distinguished by their shape and/or size. In this
manner, we confirmed that both axons innervated the muscle fiber and ruled out
the possibility that we inadvertently stimulated release from one of the
inhibitors twice. Muscle resting potentials at 2°C were in the range of
–51 to –89 mV. Muscle tension was measured by tying 6.0 silk
surgical thread to the distal end of the apodeme of the dactyl opener and
attaching the thread to a Grass FT03 force transducer (Grass-Telefactor).
Tension recordings were filtered at 10 Hz and amplified by a Cyberamp (Axon
Instruments–Molecular Devices, Union City CA, USA) and calibrated in
units of grams. All data were recorded on a VCR, digitized by an
analog-to-digital converter and analyzed using pClamp software (Digidata1200
A-D converter and pClamp software from Axon Instruments–Molecular
Devices). Means of measurements are reported ± s.e.m., unless otherwise
indicated.
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To compare the effectiveness of each of the inhibitors in inhibiting synaptic transmission by the excitor OE, one of the inhibitory motoneurons (either OI or CI) was fired with a delay (–150 ms<x<800 ms) relative to stimulation of the OE. The size of the excitatory junction potential (EJP) elicited by OE was then measured with respect to the muscle resting potential prior to both stimuli. Experimental trials where the inhibitor was stimulated were alternated with control trials in which the inhibitor was not stimulated. In cases where presynaptic inhibition was measured by analysis of area, the area under the EJP was found by integrating the area under the curve described by the EJP with respect to the baseline determined as the level of the resting membrane potential prior to stimulation.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), we tested
whether synaptic responses to both CI and OI would have the same reversal
potential, as would be predicted if they release the same neurotransmitter.
Warming the preparation from 2 to 22°C produces hyperpolarization of the
muscle fibers and reverses the sign of the inhibitory synaptic responses from
hyperpolarizing to depolarizing (Fig.
4). Table 1 shows
the results from experiments on multiple fibers. Synaptic responses triggered
by each inhibitor reversed polarity at similar membrane potentials and bath
temperatures, consistent with the idea that both inhibitors release the same
neurotransmitter.
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To test the possibility that CI reaches the dactyl opener via the nerve that carries the axon of the stretcher/opener excitor to the stretcher and opener muscles, a series of stimulation experiments were performed. Stimulation of the nerve supplying both the stretcher and the opener muscles (arrow 1, Fig. 1) elicited EJPs at low stimulus voltages by recruiting OE (see Materials and methods). However, higher stimulus voltage recruited a combination of IJPs and EJPs (data not shown), consistent with the possibility that the axon of CI travels with the axon of OE to reach both the stretcher and the opener before branching to reach the closer (path illustrated by broken line in Fig. 1).
Finally, to obtain histological confirmation that three axons innervate muscle fibers throughout dactyl opener preparation, we stained preparations with methylene blue. While it was rare to find regions where all three axons were apparent, Fig. 5 shows two examples where three axons could be identified within the nerve innervating the dactyl opener. In both cases, a small-diameter axon could be seen running with two larger-diameter axons and branching alongside them.
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CI and OI are equally effective at hyperpolarizing the muscle fibers and relaxing the muscle
To compare the physiological impact of the inhibitory neurotransmission
from the CI motoneuron with that of the OI motoneuron, we measured the sizes
of IJPs elicited by both in single muscle fibers. Overall, IJPs elicited by OI
were significantly larger than those elicited by CI [0.80±0.09 mV (mean
± s.e.m.) compared with 0.64±0.07 mV; P<0.05; paired
sample t-test; N=34]. However, the magnitude of this
difference is not large, on the order of 20–25%. Calculated in each of
the 34 fibers as a ratio (CI:OI), the mean ratio was 0.90. In 11 of the 34
fibers tested, the IJPs resulting from stimulation of CI were larger in size
than those resulting from OI. Measurements of IJP size were internally
consistent among the fibers within a single neuromuscular preparation: IJPs
from OI were larger than those from CI in each of multiple muscle fibers
(N=11) from three preparations, while in a fourth preparation CI
elicited larger IJPs than did OI in all fibers tested (N=9).
To compare the effectiveness of each motoneuron in influencing muscle tonus, we stimulated OI and CI and monitored the resulting changes in muscle tension. Fig. 6A shows an example of a preparation in which single IJPs triggered muscle relaxations; both OI and CI were equally effective in relaxing muscle. In addition, IJPs evoked by each of the inhibitors firing in high-frequency stimulus trains relaxed muscle to a comparable extent (Fig. 6B). Similar results were observed in two other preparations.
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CI and OI are equally effective at inhibiting excitatory neurotransmission
In a series of classic experiments in the crayfish opener muscle, Dudel and
Kuffler showed that stimulating the OI motoneuron within a few milliseconds of
the excitor OE depressed the EJPs and that this phenomenon is due in part to
presynaptic inhibition (Dudel and Kuffler,
1961). Repeating these experiments in the lobster demonstrates
similar results: EJPs are reduced in size when OI is stimulated shortly before
OE (Fig. 7). To test whether CI
also inhibits excitatory neurotransmission, identical stimulation protocols
were used to stimulate OE in sequence with either OI or CI, and the magnitude
of the inhibition of the EJP was measured as a function of the interstimulus
delay.
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If stimulated within a short time before OE, both OI and CI inhibit
synaptic transmission by the excitatory motoneuron OE by depressing the
amplitude of the EJP (Fig. 8A).
OI and CI are equally powerful in inhibiting excitatory neurotransmission,
suppressing the size of the EJP by >60%, on average, at the shortest
interstimulus intervals (Fig.
8B–D). Maximum inhibition by both inhibitory motoneurons
occurs at interstimulus intervals of <60 ms, and recovery from inhibition
is observed when the interstimulus intervals approach 300–400 ms. [Note
that the duration of inhibition lasted much longer in these experiments at
2°C than the time course of 8–10 ms reported for the earlier
crayfish experiments at 15°C (Dudel and
Kuffler, 1961).] The prolonged nature of inhibition in the lobster
experiments is probably the result of the long time course of synaptic
responses at cold temperatures.
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Whereas the preceding analysis of EJP amplitudes clearly demonstrates inhibition by both OI and CI, a more sensitive indicator of the degree of inhibition might be to analyze the change in shape of the EJP, rather than simply its amplitude. Fig. 10 shows examples of inhibition of the EJP by both OI and CI at 2°C. In both cases, analysis of the area under the curve of the EJP reveals a higher degree of inhibition than does the analysis of the amplitude of the EJP. To compare these two methods of analysis, we measured both the area under the EJP as well as EJP amplitude in multiple recordings where the delay between the EJP and the IJP was in the range 0–100 ms and compared these measurements to those for the respective control EJPs (Table 2). In 21 examples of presynaptic inhibition by OI, the inhibition measured as the change in area under the EJP was nearly twice that measured as inhibition of EJP amplitude (ratio inhibited/control=1.91). Similar results were obtained in 12 examples of recordings showing presynaptic inhibition by CI (ratio inhibited/control=2.01). Since depolarization directly gates calcium influx in crustacean muscle, changes in the overall shape of the EJP are likely to be critical for excitation–contraction coupling.
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OI and CI are equally effective in inhibiting contractions by OE
To compare the effectiveness of both inhibitors in reducing muscle
contractions triggered by OE, short stimulus trains were delivered to the axon
of OE in the presence and absence of identical trains simultaneously delivered
to one of the inhibitors. Fig.
11 is representative of three experiments in which we observed
that contractions evoked by OE can be completely abolished by simultaneous
firing of either OI or CI. Although the intracellular record reflects
physiological activity in a single muscle fiber while the contraction is
measured from many fibers, two aspects of these recordings are notable.
Inhibition of muscle contraction is profound, being 100% effective for
relatively few inhibitory stimuli in either inhibitor (provided they are
optimally timed with respect to the excitatory stimuli). In addition, the
contractions failed to develop even though neither inhibitor completely
abolished the EJPs. Assuming the intracellular record from this single muscle
fiber is representative of the majority of muscle fibers, the records suggest
that the inhibited EJPs are not large enough or do not facilitate sufficiently
to generate the contraction.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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These results are surprising, given that previous work in the crayfish
dactyl opener failed to find synaptic responses to CI in any but the most
medial of the longitudinally oriented fibers of the most proximal end of the
muscle (Wiens, 1985). In
addition, in the crayfish, the physiological consequences of CI stimulation
are weak compared with those of OI: CI innervates fewer fibers, the IJPs
elicited by CI are smaller, and CI is considerably less effective at
abolishing contractions elicited by the excitor OE
(Wiens, 1985;
Wiens, 1993). A previous study
in the lobster reported similar results; IJPs resulting from OI stimulation
were stronger initially and maintained or increased their effectiveness more
effectively than those evoked by CI
(Wiens, 1990). However, only
muscle fibers located in the proximal third of the lobster opener were sampled
for CI innervation, and synaptic responses to stimulus trains were reported
for only two muscle fibers.
Our results demonstrate that in the lobster dactyl opener, the generality that OI is a stronger inhibitor than CI does not hold. While overall the IJPs triggered by CI are smaller, in one third of fibers (11 out of 34) CI's IJPs were in fact larger than those of OI. Further, although we did not systematically examine the facilitation properties of the two inhibitors, it is clear that IJPs elicited by CI can show more facilitation than those elicited by OI (for example, see Fig. 6B). The two inhibitors are similarly powerful in inhibiting the EJPs stimulated by OE (Fig. 8), and both inhibitors, firing at relatively low frequency, can abolish muscle contractions stimulated by OE (Fig. 11). Finally, both OI and CI, firing either once or in trains, can relax the dactyl opener muscle to approximately the same extent (Fig. 6).
The reasons for the discrepancies between our findings and those of others are unclear, however we note that the low temperature used in our experiments favors large IJPs because the resting potentials of the muscle fibers at 2°C are depolarized relative to their values at 10–11°C, where the IJPs reverse polarity (see Table 1). At 2°C, our ability to detect hyperpolarizing synaptic responses is relatively enhanced because the driving force for the IJPs is relatively large at cold temperatures. Previous crayfish studies have been done at room temperature, where the resting membrane potential is close to the equilibrium potential for the chloride ions and inhibitory synaptic signals can be relatively small or at their reversal potential. Under these conditions, it is possible that inhibitory synaptic responses may not be detectable in the background noise of the recording.
It is important to note that temperatures as cold as 2°C are in fact
physiologically normal for lobsters living in the wild. By affixing
temperature loggers to Homarus living in the Gulf of Maine, Cowan and
co-workers demonstrated that this species lives in extremely cold
(0–6°C) water temperatures throughout the six months of winter and
early spring (Cowan et al., in
press).
Because we performed our experiments in the cold (2°C), two particular physiological issues deserve mention. First, the resting muscle tension relieved by CI and OI (see Fig. 6) appears to be relatively strong in the cold (M.K.W., unpublished observations), possibly because the muscle fibers are sufficiently depolarized to mediate a resting calcium influx. However, little is known about the generation of resting muscle tension in this or any other crustacean muscle, and the mechanisms by which inhibitors relax muscle tension remain to be elucidated. Second, it is possible that cold temperatures compromise the safety factor for action potential conduction by slowing the kinetics of ion channel activity in axonal membranes. At 2°C, we observe that the effectiveness of presynaptic inhibition is >60% for each of the inhibitors (Fig. 8), however presynaptic inhibition might be even stronger at warmer temperatures. Future experiments will address whether the strength of presynaptic inhibition in the lobster might be temperature dependent.
Finally, our observation that one of the three axons innervating the dactyl
opener muscle is of much smaller diameter than the others
(Fig. 5) may explain why the
triple innervation of this muscle in lobster has been largely overlooked.
Previous authors described two major axons in cross-sections of fixed dactyl
opener nerve and assumed that the smaller axon profiles were branches of the
two main axons OI and OE (Kravitz et al.,
1963). In our hands, most methylene blue preparations of dactyl
opener muscle show two large axons over most of the extent of the muscle,
however evidence for three can be observed with close examination (see
Fig. 5). The technical problem
of underestimating the number of methylene blue-stained axons if two axons run
in close proximity or one lies over another has been noted previously in a
discussion of the triple innervation of the crayfish extensor muscle
(Van Harreveld and Wiersma,
1937).
What distinctive physiological roles are served by each of the inhibitors?
Our finding that CI can be as powerful as OI in several physiological
assays at a physiologically relevant temperature is important in understanding
the functional roles of these two inhibitors. Previously, it was thought that
the physiological roles of the common and specific inhibitors may be distinct,
in that the inhibition by CI is more general in scope (reaching multiple
muscles) and weaker in nature. By contrast, the physiological roles of
specific inhibitors (such as OI) have been strongly associated with inhibiting
the output of the specific excitors, which they powerfully inhibit and with
which they share all innervation targets. In a review, Wiens summarized the
distinction between the specific and common inhibitors in decapod crustaceans
by noting that, in contrast to the common inhibitor, specific inhibitors
`innervate all fibers in their target muscles powerfully and can totally
eliminate any contraction in these muscles'
(Wiens, 1989). However, our
data would suggest that such a view requires revision, as the common inhibitor
CI fits this description as well as the specific inhibitor OI in the lobster
dactyl opener neuromuscular system.
Other neuromuscular systems where the physiological ramifications of dual
inhibitory innervation have been extensively studied include those of the
brachyuran crab Eriphia. In the crab, where the dactyl opener is
composed of both tonic and phasic fibers, CI inhibits the tonic fibers
strongly and the phasic fibers weakly, and this pattern is common to each of
the seven limb muscles in the crab (Wiens
et al., 1988). By comparison with the specific inhibitors to the
crab muscles, CI is usually reported to have weaker physiological effects. For
example, in the crab, CI exerts little presynaptic inhibition on the excitor
innervating the stretcher muscle whereas the specific inhibitor to the
stretcher exhibits both presynaptic and postsynaptic inhibition
(Atwood and Bittner, 1971); in
this system at firing frequencies below 70 Hz CI is considerably less
effective than the specific inhibitor at reducing EJP size. In addition, in
electromyograms of the crab, OI nearly completely suppressed the electrical
response of the muscle to OE, but CI rarely did so
(Ballantyne and Rathmayer,
1981). Interestingly, in the crab flexor, as in the lobster opener
(see Fig. 6), short bursts of
firing activity in CI in isolation can effectively relax muscle tension (see
fig. 4 in Wiens and Rathmayer,
1985).
Given that the peripheral effects of OI and CI are very similar in the
lobster dactyl opener, one speculation is that any distinctions between their
physiological functions in vivo must be due to differential firing
activity at the level of the CNS. A previous examination of central control of
dactyl movement evaluated efferent neural activity to both the dactyl opener
and the closer in the crayfish claw during reflex activity. The findings
suggested that OI and CI may have mutually inhibitory connections, ensuring
they will not fire simultaneously (Wiens
and Gerein, 1975). Interestingly, the data also indicated that CI
might inhibit OE centrally, whereas we have demonstrated that CI powerfully
inhibits OE peripherally. However, it was not clear from the earlier study
under what conditions firing of one inhibitor might be favored over that of
the other, nor was it known that CI, in fact, makes synapses on the opener
muscle as well as the closer. Thus, a definitive comparison between the roles
of CI and OI in moving the dactyl is lacking. The most comprehensive
examination of the central activity of CI has been in a chronic recording of
CI efferent activity during locomotion in the crab
(Ballantyne and Rathmayer,
1981). Firing tonically at low frequencies, CI shaped muscle
contractions stimulated by bursts of activity in OE such that contractions
became more phasic in nature, relaxing more quickly.
Under the stimulus conditions we tested (using single inhibitory stimuli
and short stimulus trains) we did not observe differences in the physiological
impact of OI as compared with CI in the lobster dactyl opener neuromuscular
system. However, we cannot exclude the possibility that differences exist
under other stimulus paradigms, such as when the inhibitors fire in prolonged
or high-frequency stimulus trains. In addition, there may be differences in
the membrane composition of the presynaptic terminals of each of the
inhibitors that could be important physiologically. For example, in the
crayfish dactyl opener it has been shown that different classes of GABA
receptors mediate presynaptic inhibition by OI depending on the frequency of
firing (Fischer and Parnas,
1996). It is unknown whether the terminals of CI operate
similarly. Inhibitory terminals on crayfish dactyl opener stain with
antibodies to GABA (Msghina and Atwood,
1997) as well as antibodies to mammalian GABAA
receptors (Feinstein et al.,
2003), however the authors assumed that staining corresponded
exclusively to terminals of OI rather than CI. We would predict that terminals
from both inhibitors would stain for GABA and GABA receptors in the lobster
opener, consistent with our observation that synaptic responses to both
inhibitors reverse at the same membrane potential.
In summary, CI and OI share innervation targets in the lobster dactyl opener and are comparable in terms of their physiological effects in relaxing muscle, inhibiting excitatory synaptic responses, and reducing neurally evoked muscle contractions. Future studies should elucidate whether and how these two inhibitors are differentially activated by the CNS. As CI also provides the only source of inhibition to the opposing dactyl closer muscle, understanding the relative roles of OI and CI motoneurons will be important for understanding the neural control of both of the muscles that move the dactyl.
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Acknowledgments |
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J. L. Hamilton, C. R. Edwards, S. R. Holt, and M. K. Worden Temperature dependent modulation of lobster neuromuscular properties by serotonin J. Exp. Biol., March 15, 2007; 210(6): 1025 - 1035. [Abstract] [Full Text] [PDF]
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