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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
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Dual inhibition of the dactyl opener muscle in lobster

Mary Kate Worden* and Joseph A. Camacho

Department of Neuroscience, University of Virginia, PO 801392, Charlottesville, VA 22908, USA


Figure 1
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  		Fig. 1. Schematic illustrating the neural innervation of the dactyl opener and closer muscles of the propus and the stretcher muscle of the carpus of the lobster walking leg. Muscles are indicated by boxes; within the boxes are abbreviations for the names of the innervating motoneurons. Lines illustrate the innervation paths of the axons of each of the motoneurons. The opener muscle receives innervation from the common inhibitor (CI), the opener excitor (OE) and the specific opener inhibitor (OI). Placement of suction electrodes for stimulation of the axons of these motoneurons is illustrated by numbered arrows. (1) The axon of OE is stimulated by an electrode placed on the nerve running between the stretcher and opener muscle; this nerve contains the axon of OE (black line) as well as CI (see Results). (2) The axon of OI is stimulated via its axon (heavy black line) in the main nerve trunk in the carpus. (3) The axon of CI (broken lines) is stimulated by an electrode placed on a nerve branch that stretches between the opener and closer muscles. The innervation of the closer muscle and the stretcher muscle is also shown: the closer is innervated by fast and slow excitatory axons (FCE and SCE) as well as by CI, while the stretcher is innervated by CI as well as the stretcher excitor (SE). The stretcher excitor SE is another name for the opener excitor OE; both muscles are innervated by the same excitatory axon.

 

Figure 2
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  		Fig. 2. Synaptic responses recorded in a dactyl opener muscle fiber in response to stimulation of the opener excitor (OE), the specific opener inhibitor (OI) and the common inhibitor (CI) motoneurons. The relative timing of stimulation for each motoneuron is indicated schematically. Muscle potential was –70 mV. Scale bar, 1 mV, 250 ms.

 

Figure 3
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  		Fig. 3. Synaptic responses elicited by both the opener inhibitor (OI) and the common inhibitor (CI) can be detected in many regions of the dactyl opener muscle. Intracellular recordings from different areas of the muscle (labeled A–D) are shown. In each case, CI was stimulated before OI. Scale bars for electrophysiological recordings, 2.5 mV, 0.5 s. Scale bar for photo, 0.25 cm.

 

Figure 4
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  		Fig. 4. Synaptic responses elicited by the opener inhibitor (OI) and the common inhibitor (CI) reverse polarity at similar temperatures. The amplitudes of inhibitory junction potentials (IJPs) elicited by stimulation of OI and CI are plotted as a function of temperature. All measurements were made in a single muscle fiber; insets show synaptic responses at 2°C and 18°C. Note that IJPs are hyperpolarizing at colder temperatures (<10°C) and depolarizing at warm temperatures (>12°C). Scale bars, 0.5 mV, 0.2 s.

 

Figure 5
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  		Fig. 5. Methylene blue staining reveals three axons in the nerve innervating the dactyl opener. Left and right photos were obtained from sites located 25% and 75%, respectively, along the length of the entire proximal–distal axis of the dactyl opener muscle. Proximal is at the top of each photo. Arrows show a small-diameter axon that branches (as do two large diameter axons) distally to supply branches of the nerve. Scale bars, 50 µm.

 

Figure 6
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  		Fig. 6. Inhibitory synaptic responses and muscle relaxations triggered by the opener inhibitor (OI) and the common inhibitor (CI). (A) Upper trace shows inhibitory junction potentials (IJPs) elicited by single stimuli (indicated by arrows) to OI and to CI; lower trace shows the corresponding relaxation in muscle tension. Scale bar, 0.1 mV, 4 mg, 1 s. (B) Upper trace shows synaptic responses to identical 10 Hz trains of stimuli delivered to OI and CI; lower trace shows the corresponding relaxation of muscle tension. The timing of stimulus trains is indicated by horizontal black bars. Scale bar, 0.5 mV, 12.5 mg, 2 s.

 

Figure 7
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  		Fig. 7. Inhibition of excitatory junction potentials (EJPs) by the opener inhibitor (OI) depends on interstimulus interval. A series of recordings from a single muscle fiber is shown; each trace is the average of six trials. In each recording, OI is stimulated at the time indicated by the arrow, the opener excitor (OE) was stimulated at an interstimulus interval indicated to the left of each trace. Note that the delay is preceded by a negative sign if OE is stimulated before OI. Scale bar, 2.5 mV, 250 ms.

 

Figure 8
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  		Fig. 8. Inhibition of excitatory transmission by the opener inhibitor (OI) and the common inhibitor (CI). (A) Examples of synaptic responses of a single muscle fiber to stimulation of the opener excitor (OE) alone, CI and OE (interstimulus delay 8.9 ms) and OI and OE (interstimulus delay 15.1 ms). Scale bar, 2 mV, 200 ms. (B) EJP amplitude plotted as a function of interstimulus interval between OE and each of the two inhibitors. All measurements are from a single muscle fiber; excitatory junction potential (EJP) size is normalized to its size in control trials where only OE was stimulated. (C,D) EJP amplitude, normalized to control, plotted as a function of the interstimulus delay between OE and OI (C, N=14 fibers) and OE and CI (D, N=8 fibers). Symbols represent the mean values, vertical error bars represent standard deviations of the means, and horizontal error bars indicate the range of interstimulus intervals in each bin. *Data are significantly different (P<0.05) from controls where the excitatory axon was stimulated prior to the inhibitory axon.

 

Figure 9
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  		Fig. 9. The opener inhibitor (OI) can completely suppress the synaptic response to the opener excitor (OE). Three recordings are shown from the same muscle fiber; the top two show the result of stimulating OI 18.4 ms and 46.8 ms, respectively, before stimulation of OE. The bottom trace shows the control response to OE stimulation. Scale bar, 1 mV, 200 ms.

 

Figure 10
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  		Fig. 10. Excitatory junction potentials (EJPs) inhibited by the opener inhibitor (OI) (left: interstimulus interval 52 ms, OI precedes OE) and by the common inhibitor (CI) (right: CI and OE stimulated simultaneously) superimposed on the EJPs recorded in the absence of inhibitory stimuli (broken lines). In these examples, OI inhibited the area under the EJP by 75.9% and the amplitude of the EJP by 29.7%. CI inhibited the area under the EJP by 49.8% and the amplitude of the EJP by 16%. Scale bar on left, 2 mV, 200 ms; scale bar on right, 1 mV, 200 ms.

 

Figure 11
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  		Fig. 11. The opener inhibitor (OI) and the common inhibitor (CI) are similarly effective in inhibiting synaptic and contractile responses to stimulation of the excitor OE. (A) Intracellular recordings of synaptic responses to identical stimulus trains (10 Hz, 600 ms) delivered to OE alone, OI and OE (stimulated simultaneously), CI and OE (stimulated simultaneously) and OE alone. Both inhibitors inhibit excitatory junction potential (EJP) amplitude and hyperpolarize muscle slightly. The broken line illustrates resting membrane potential. (B) Tension recordings corresponding to stimulus trials above. Note that the muscle contracts in response to stimulation of OE alone but fails to contract if either inhibitor is stimulated. The broken line indicates resting level of muscle tension in the absence of stimulation. Scale bar, 2.5 mg, 100 mg, 500 ms.

 

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© The Company of Biologists Ltd 2006