Synaptic Connectivity: Nerve-Target Matching and Synaptic Integration
Introduction
If you have not already done so, read Appendix A, Crayfish Neuromuscular Preparation, for background. In this lab exercise, you will simultaneously record intracellularly from the superficial flexor (SF) muscle of the crayfish abdomen and extracellularly from ganglionic nerve 3, which innervates it. Your goals are to map the innervation pattern of motor neurons onto the muscle, describe excitatory postsynaptic potentials (EPSPs) in muscle fibers, matching EPSPs with the identifiable action potentials (APs) in the nerve that cause them, and document examples of synaptic integration. You may find it helpful to refer to your data from Lab 2, Nerve Recording, in which you determined the number of AP classes in nerve 3 and how nerve 3 activity changed with sensory stimulation.
You will see that individual muscle fibers are selectively innervated by some neurons, but not others, in that some action potentials in the nerve will not match with any EPSP in a given muscle fiber. You will also see evidence of polyneuronal innervation, in that most muscle fibers have EPSPs resulting from activity in more than one axon. Finally, you will examine some basic integrative features of the synapse, including temporal and spatial summation of EPSPs and IPSPs (Byrne, 2008; Nicholls et al., 2012; Purves, et al., 2012).
Dissection
The dissection is the same as for Lab 4, Resting Potential. Before starting, look at the methylene blue-stained specimen that was prepared in advance (it will resemble Figure A.2). This specimen shows nerve 3 leaving the ganglion, projecting to the superficial flexor muscle, and branching out over the surface of the muscle. At high magnification, you should be able to see single stained axons in nerve 3. Look closely at the nerve as it enters the muscle and note where it appears to terminate on the muscle. The fine branching ends of the nerves on the muscle are where synaptic contacts are made.
- Video 5.1, Nerve-Muscle Dissection and Recording, shows the entire dissection and recording procedure. You may want to watch this version during the lab after reading the descriptions below and watching the separate videos for each step of the dissection.
- Video A.1, Preparing Crayfish Abdomen. Place a crayfish in the freezer or in ice and leave it until it has stopped moving. Cut off and keep the tail; place the remainder in the freezer. Pin the tail, ventral surface up, in a dissecting dish and cover it with cold crayfish saline.
- Video A.2, Removing Swimmerets. Remove and discard the swimmerets.
- Choose any tail segment other than the first one (which is damaged from the initial cut) or the last one (which has an atypical organization and is relatively inactive). Many crayfish species have a blue stripe on the ventral midline. It lies right over the ventral nerve cord. The dissection requires opening a window in the thin cuticle over the nerve cord, followed by exposing the muscle to one or the other side of this window.
- Video 4.2, Exposing Superficial Flexor. Dissection to expose the muscle consists of three incisions. This crayfish, like many others, has a blue stripe on the ventral midline. It lies right over the ventral nerve cord. Before starting the dissection, find the muscle attachment point (the white line in Figure A.2). Take care not to cut through this line.
- Turn the dish so that the cut end of the tail faces away from you. Using a scalpel with a sharp (preferably new) blade, make an incision along the midline between the two sternites. This cut should go all the way through the cuticle. If your crayfish has a blue stripe, this cut will go along the center of the stripe.
- With forceps, lift the cuticle at the posterior end of the first incision and cut along the sternite toward the lateral edge. Although the video shows this dissection being done with a scalpel, you should use fine scissors if they are available. Hold the scissors so that the blades are flat and move parallel to the muscle during cutting. If the blades instead move up and down, they can damage the muscle. If using a scalpel, keep the blade shallow and parallel to the muscle, as shown in the video.
- Lift the flap of cuticle so that it stands up straight from the muscle insertion (the white line). Use scissors (preferred) or a scalpel to cut the flap away. Again, keep the blade flat and avoid touching the muscle.
- After the dissection, rinse all tools with fresh water and lay them aside where they will not be damaged.
Recording
Figure 5.1 shows the setup for dual intracellular and extracellular recording. Video 5.2, Nerve-Muscle Recording, shows the recording procedure. Before starting to record from the muscle, replace the saline in the dissecting dish with fresh cold saline. Repeat this every half hour or so, but do not interrupt a good recording to do so.
Start with an extracellular recording of nerve 3 on one side (see Lab 2, Nerve Recording, for recording methods). If nerve 3 is not visible, apply Janus green for 15 s and then wash with saline. Be sure that the suction electrode placement will not prevent access to the muscle with the intracellular electrode. It is usually best to have the manipulator for the intracellular electrode on the same side as the muscle and the manipulator for the nerve on the opposite side. Rotate the preparation dish to get a good orientation. Next, record intracellularly from a muscle fiber on the same side as the nerve you are recording (see Lab 4, Resting Potential, for recording methods). If there are EPSPs in the fiber you are recording, they will appear as small (1 to 10 mV) deflections in the oscilloscope trace, as seen at the end of Video 5.2, Nerve-Muscle Recording.
Not every location from which you record on the superficial flexor will show EPSP activity. To see EPSPs, you must record near a synapse. Although each crayfish and abdominal segment is a little different, you may be able to direct your search by looking at a methylene blue-stained muscle and noting the location of fine nerve branches on the muscle. Generally, EPSPs can best be recorded in the middle of the muscle.
When starting muscle recording, set the oscilloscope channel with the intracellular recording to DC coupling with a fairly fast time scale (2 ms/div) and vertical scale of 0.1 V/div (your amplifier increases the signal 10×, so this corresponds to 10 mV/div of real voltage). Once you have a good muscle resting potential with obvious small depolarizing deflections on the oscilloscope, set this channel to AC coupling, slow the time scale (5 to 20 ms/div), and increase the vertical scale to 20 to 50 mV/div (corresponding to 2 to 5 mV in reality). Now the trace should appear more like that shown in Video 5.3, PSP Recording.
Experiments
EPSP Characteristics
Measure the waveform characteristics of some single EPSPs, including amplitude, rise time (from the initial positive deflection to the peak), and duration (measure at half the amplitude). Note the variation in amplitudes of the extracellular APs. Each extracellular action potential size class corresponds to a different axon in the nerve because each is caused by an axon of a different diameter. Larger diameter axons produce larger extracellular AP current densities than smaller diameter axons. Find an AP size class that always closely precedes a particular EPSP size. Does more than one size of AP correspond to EPSPs in this fiber? Measure the delay between several different AP size classes and the onset of the EPSPs that regularly follow them. Note that not every AP in the nerve can be matched to an EPSP in the muscle fiber. This is because not every axon in nerve 3 innervates every muscle fiber (selective innervation). If there is an obvious large AP that you cannot match with an EPSP, it may be from the inhibitory axon. Look for inhibitory postsynaptic potentials (IPSPs) or changes in the shapes of EPSPs after this axon fires. Are there any EPSPs that do not have an AP immediately preceding them? What does this mean?
Mapping Innervation
Draw a diagram of the muscle from which you are recording. Record from a variety of locations, marking them on your map. At each location, note the resting potential of the muscle fiber and which sizes of APs match EPSPs in the fiber. From this set of data, map the innervation of the muscle.
Reflex Activity
Changes in PSP activity in muscles due to sensory input are important because they lead to the behavioral response to sensory stimulation. While recording, gently prod the telson with a nonmetallic object (be careful not to disturb your muscle recording). The reflex activity evoked by this prodding will cause more AP activity in the nerve. Does it also activate a new size of AP in the nerve and a new EPSP in the muscle? Repeat this while recording from several different muscle fibers. Look for IPSPs during this reflex-evoked activity.
While eliciting reflex activity in the nerve and muscle, or when you have a spontaneously very active nerve and muscle, gather examples of temporal and spatial summation of EPSPs.
Further Exploration
You can follow up on questions raised by the above experiments in several ways:
- Use methylene blue to stain the preparation on which you mapped innervation and then compare the pattern of innervation revealed by the stain with your physiological mapping. Do the locations of fine nerve branches correlate with your physiological mapping?
- You have focused on EPSPs in this lab, but you may also see IPSPs. These are difficult to record at the normal muscle resting potential. Depolarize muscle fibers with current injection or high K+ saline to make IPSPs more easily visible.
- Picrotoxin blocks Cl− channels, thus reducing the effect of inhibitory neurotransmitters. This toxin may change the size or shape of EPSPs, thus revealing the effects of inhibition in the untreated preparation.
- Examine the muscle response to reflex activation by pushing swimmeret stumps of various segments and noting the effect this has on nerve 3 APs and muscle EPSPs.
- Examine the spontaneous release of transmitter packets from the presynaptic terminal by cutting the nerve near the ganglion, recording from the muscle, and looking for very small EPSPs. These are miniature endplate potentials (MEPPs). You are more likely to see them if you use a small crayfish. Why might that be?
- Examine the ionic basis of synaptic transmission by ion substitution. Replace Ca2+ with Ba2+ or Mg2+.
- Examine the contribution of K+ channels to the shape of the EPSP by adding 4-aminopyridine or tetraethylammonium (TEA) to the saline. These block K+ currents that repolarize the presynaptic membrane after an AP and should thus cause more transmitter release.
- Apply agonists and antagonists of the excitatory and inhibitory neurotransmitters (glutamate and GABA, respectively) to the saline and observe the effects on PSPs.
- Apply different concentrations of glutamate or GABA locally near your recording site to elicit PSPs directly. (These transmitters to the bath will also change membrane potential.) Determine a dose-response curve for the PSP-like response or membrane potential change. Nerve 3 should be cut before these experiments.
- Estimate the time constants of the falling phases of PSPs from several spike classes and in two or more muscle fibers. Are they more consistent within a muscle fiber or more consistent within a spike class?
Lab Cleanup
During the lab, be sure to immediately discard used glass electrodes in the appropriate container. After the lab, remove your last electrode from its holder and discard it as well. Clean up any spilled saline and rinse the ground electrode with distilled water. Expel saline from the suction electrode and rinse it with distilled water. Put the crayfish tail in the freezer along with the frozen heads and rinse the dissecting dish with fresh water.
Questions
- Why must the electrode be near a synaptic junction for PSPs to be recorded?
- Show your measurements of the waveforms of some EPSPs, including amplitude, rise time, and duration. Why do different AP classes often cause EPSPs of different amplitudes? Would you expect one AP class to elicit the same size PSP in different muscle fibers? Does the size of an AP correlate with the size of the PSP it causes? What would PSPs with different rise times tell you? Explain why you might see a PSP without an AP associated with it.
- Present your measurements of some intervals between APs in the nerve and the PSPs they cause in the muscle. Are the intervals shorter when the APs are larger? What physiological processes account for this interval?
- Present a map of the innervation of the superficial flexor muscle, marking all the sites from which you recorded and which AP size classes caused PSPs at each site. Are there medial-to-lateral differences in innervation of the muscle? What does selective innervation of particular muscle fibers by particular motor neurons suggest about the development of these synaptic connections?
- Show examples of what happened to nerve and PSP activity when you stimulated the tail.
- Present examples of the synaptic integration you observed.
- It is easy to find EPSPs in your recordings, but much harder to see evidence of inhibition. Why is this? Consider the ion conductances activated by excitatory and inhibitory innervation and explain why EPSPs are easier to record than IPSPs. How could the inhibitory axon affect EPSPs without producing a distinct hyperpolarizing IPSP? How could you enhance the amplitude of IPSPs to make them more visible in a recording?
- Briefly explain why the crayfish neuromuscular junction is a good model for human brain synapses while the mammalian neuromuscular junction is not.
References
- Atwood HL (1982). Synapses and neurotransmitters. In: Atwood HL, Sandeman DC (eds.), The Biology of Crustacea, Vol 3, Neurobiology: Structure and Function (Academic Press, New York), ch. 3.
- Atwood HL (2008). Parallel ‘phasic’ and ‘tonic’ motor systems of the crayfish abdomen. J Exp Biol 211:2193-2195. [doi]
- Byrne JH (2009). Postsynaptic potentials and synaptic integration. In: Byrne JH, Roberts JL (eds.), From Molecules to Networks: An Introduction to Cellular and Molecular Neuroscience (Academic Press, San Diego), ch. 16.
- Clement JF, Taylor AK, Velez SJ (1983). Effect of a limited target area on regeneration of specific neuromuscular connections in the crayfish. J Neurophysiol 49:216-226. [pdf]
- Krause KM, Vélez SJ (1995). Regeneration of neuromuscular connections in crayfish allotransplanted neurons. J Neurobiol 27:154-171. [doi]
- Nicholls JG, Martin AR, Fuchs PA, Brown PA, Diamond ME, Weisblat DA (2012). From Neuron to Brain (Sinauer Associates, Sunderland MA), ch. 16.
- Purves D, Augustine GJ, Fitzpatrick D, Hall WC, LaMantia A-S, McNamara JO, White LE (2012). Neuroscience (Sinauer Associates, Sunderland MA), ch. 5.
- Vélez SJ, Wyman RJ (1978a). Synaptic connectivity in a crayfish neuromuscular system: 1. Gradient of innervation and synaptic strength. J Neurophysiol 41:75-84. [pdf]
- Vélez SJ, Wyman RJ (1978b). Synaptic connectivity in a crayfish neuromuscular system: 2. Nerve-muscle matching and nerve branching patterns. J Neurophysiol 41:85-96. [pdf]