Name: Electrode Fabrication and Implantation in Aplysia californica for Multi-channel Neural and Muscular Recordings in Intact, Freely Behaving Animals (Video) | JoVE Journal
Uploaded: 2010-06-04T17:00:00.000+00:00
Duration: 12 min 37 s
Description: Learn electrode fabrication and implantation in Aplysia californica for multi-channel neural and muscular recordings. This technique enables real-time monitoring of neuromuscular control during feeding behavior.

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5 minutes

We gratefully acknowledge support from the NIH (NS047073 to H.J.C.). We also are grateful to Catherine Kehl for her early experiments with Kwik-Sil, which encouraged us to use it for our application.

1. Electrode Fabrication
<ol>
<li>To create the electrode, use scissors to cut a piece of enamel-coated 0.001 inch diameter stainless steel wire about 2 feet long. Attach a small ball of putty to each end of the wire, fold the wire in half, and spin the ends to create a twisted pair, called a differential electrode.</li>
<li> Tape both ends of the wire to prevent unraveling. Make four differential electrodes, using a different color of tape for each differential electrode for identification purposes (Figure 1A).</li>
<li> Twist two of the differential electrodes together, leaving two inches untwisted on one end and 1 inch on the other end. Repeat with the remaining pair of differential electrodes (Figure 1B).</li>
<li> Twist both sets of two differential electrodes together, making sure that the ends remain untwisted. Hold up the electrode assembly and apply household silicone glue at the junction of the four differential electrodes, leaving the ends free. Hang and allow the glue to dry for at least 4 hours (Figure 1C).</li>
<li> To insulate the branches, lay the electrode assembly down on a flat, movable, surface such a piece of wood. Fan out the ends and secure them with tape. Use a small piece of plastic to elevate the electrode assembly just before it branches, and secure that with tape.</li>
<li> At a dissecting microscope, use forceps to coat the branches with silicone glue. The 1-inch long ends will be inside the animal, so they should have a very thin coat of glue. Allow the glue to dry for at least 3 hours.</li>
<li> Shorten the 1-inch long end of one differential electrode to two centimeters. On each wire, remove 1cm of silicone and enamel. Curl one bare wire into a hook for recording. Bend the other wire up and away from the hook; this will serve as the ground wire. Repeat for the remaining three electrodes.</li>
<li> Select one of the four electrodes on the 2 inch end. Use forceps to scrape silicone and enamel off, exposing 1cm of bare stainless steel wire on each of the 2 wires. Solder a gold connector to each of the two wires. Use a piece of lab tape to secure the end and maintain a separation between the ground and recording pins. Repeat for the remaining three electrodes.
</li>
<li> Attach a 1-2cm ball of the silicone glue to the cable, about 1.5 inches from the hook end to anchor the electrodes within the animal. Allow to dry for at least one hour (Figure 1D). <img src="/files/ftp_upload/1791/1791fig1.jpg" alt="Protein purification method diagram using chromatography system for multistep separation process." data-altupdatedat="1788235205000" data-alt="Figure 1"> Figure 1. Electrode Assembly Fabrication. (A) Single differential electrode consisting of a folded and twisted wire with its ends secured with tape. (B) Two differential electrodes twisted together, leaving untwisted space at the ends. Different colored tape or another marking should be used to identify the ends. (C) All four differential electrodes combined into a single electrode assembly forming a single cable with separate branches of the individual electrodes on each end, marked with distinct colors of tape. (D) Final form of electrode assembly. On the left, there are curled hooks for recordings and ground wires for each differential electrode. On the right, gold connector pins have been soldered to the wires for connection to the amplifier. An anchoring ball of silicone glue has also been placed towards the left side of the assembly.</li>
</ol>
2. Preparation of Animal For Implantation
<ol>
<li> Select a healthy animal that weighs about 350-450g. In response to small pieces of seaweed, the animal should generate bites at intervals of between 3 to 5 seconds. The complete surgery with electrode implantation should take about an hour.</li>
<li> To anesthetize the animal, inject it with 30% w/v isotonic MgCl2. To prevent the loss of hemolymph and MgCl2, the injection site can be coated in superglue before removing the needle. <img src="/files/ftp_upload/1791/1791fig2.jpg" alt="Kidney nephron diagram with loop of Henle indicating urine concentration process." data-altupdatedat="1788235205000" data-alt="Figure 2"> Figure 2. Schematic diagram showing how the animal is pinned for electrode implantation, and the location of the incision (indicated by a bar). </li>
<li> Lay the anesthetized animal out in a dissection tray with its foot down. Facing the animal head on, shift the gill area to your left such that the animal is partially on its side, leaning away. Pin down the anterior tentacles (Figure 2).</li>
<li> Place the tray on the stage of a dissecting microscope. Prop up the tray at about a 20 degree angle to elevate the head and collect the hemolymph in the tail, away from the incision.</li>
<li> Using dissection scissors, start an incision slightly to your right of the eyespot and extend it 1 to 1.5cm anteriorly. Use retractors attached to the edges of the tray to hold the incision open (Figure 2; note bar near eyespot indicating incision).</li>
<li> To expose the buccal mass, use forceps to lift the clear membrane underneath the skin and use scissors to cut an opening matching the main incision. Tuck the edges of the membrane into the retractors. </li>
</ol>
3. Electrode Implantation
<ol>
<li>Place the electrode assembly on a micromanipulator and move it over the animal's incision.</li>
<li> The radular nerve is most difficult to access, and should be approached first. There are two options for accessing the radular nerve.</li>
<li> The first option, which is preferable, is to look under the buccal ganglion between BN1 and BN2. If a branch of the radular nerve is visible, use fine-tipped forceps bent into a hook to lift out the branch (Figure 3, loop of RN under ganglion labeled 1).</li>
<li> If a branch of the radular nerve is not accessible above the muscle, a second option is to access it via a small incision in I2 next to the connective tissue at the base of the buccal ganglion (Figure 3, RN beneath muscle labeled 2). The incision in I2 must go through two layers of the I2 muscle. Hold onto the edge of the muscle incision with straight forceps and use the hooked forceps to pull out an RN branch.</li>
<li> While holding the nerve with the hooked forceps, use a different set of forceps to manipulate the electrode hook onto the nerve.</li>
<li> Use the micromanipulator to raise the hook so that the nerve is lifted up away from the buccal mass and clear of any other nerves or tissue. Do not overstretch the nerve.</li>
<li> Dry the electrode using a Kim-Wipe or suction off the excess fluid with a syringe. Water tension can cause the nerve to collapse on itself, or a water seal to form under the nerve. In either case, the area should be completely dried before glue is applied.</li>
<li> Apply a small dab of superglue where the base of the hook is in contact with the bottom of the nerve. Apply a drop of Aplysia saline or hemolymph to set the superglue. When the glue is wet nothing should be moved as getting glue between the wire and nerve would block the electrical connection.</li>
<li> Dry the hook again. Mix Kwik-Sil glue on an ice pack.</li>
<li> Use the tip of a pin to apply a small amount of the Kwik-Sil glue, completely covering any exposed wire of the hook, but not the ground wire.</li>
<li> Allow the glue to set for about 5 minutes, readjusting the glue if it pulls away from sections of the hook. The glue is set when it no longer sticks when touched with the pin (Figure 4 shows the final configuration).</li>
<li> Once the radular nerve electrode is set, the I2 muscle can be accessed. In the area between BN1 and BN2, use the hooked forceps to hook and to separate 2 bands of the I2 muscle from the rest of the muscle by gently pulling the bands upwards. Attach the electrode using the same procedure.</li>
<li> Buccal nerves 2 and 3 are easily accessed and electrodes are attached with the same procedure.</li>
<li> Once all the electrodes are attached, slide the electrode assembly into the animal up to the silicone anchor. </li>
<li> Suture the incision closed around the protruding electrode cable, keeping the anchor inside the animal. Superglue the stitches to ensure a good seal.</li>
<li> Insert the gold connector tips at the other end of the electrode into a small block of Styrofoam. Return the animal to the main tank in an aerated isolation container for recovery overnight.</li>
</ol>
<img src="/files/ftp_upload/1791/1791fig3.jpg" alt="Anatomy diagram of mollusk buccal ganglion; nerve pathways labeled, electrode positions marked." data-altupdatedat="1788235205000" data-alt="Figure 3"> Figure 3. A diagram of the Aplysia feeding apparatus known as the buccal mass. Shown are the buccal nerves (BN1, BN2, BN3), the radular nerve (RN) that exits the bottom of the buccal ganglion, then plunges beneath the muscle, and the location on the I2 muscle where the electrode is attached.
<img src="/files/ftp_upload/1791/1791fig4.jpg" alt="Neurosurgery diagram with Kwik-Sil application and superglue technique for nerve repair." data-altupdatedat="1788235205000" data-alt="Figure 4"> Figure 4. Schematic diagram of single electrode attached to a nerve (or muscle) and glued in place. Note that the de-insulated region of the curled hook is in direct contact with the nerve (or muscle), anchored in place with superglue, and electrically insulated from the fluid medium using Kwik-Sil. Note also that the deinsulated tip of the ground electrode is exposed to the fluid medium.
4. Recording
<ol>
<li> Acclimate the animal in an aerated container while attached to the recording equipment for at least 1.5 hours. Monitor the signal while the animal is acclimating to verify that all electrodes are working and that noise levels are low.</li>
<li> Use a video camera to record feeding behavior while using the computer to record signals from the neural and muscular electrodes. Synchronize the video and electrode recordings using a square wave signal that controls a digital counter in the camera view while it is simultaneously recorded as an additional channel on the computer in Axoscope.</li>
<li> Feeding behaviors are elicited by the techniques described in Morton and Chiel 1993.</li>
</ol>
Although invertebrate animals do not require formal approval by an institutional animal use and care committee, we have ensured that all treatments of Aplysia minimize harm and suffering to the animal, and that all surgical techniques are done while the animal is fully anesthetized.
Representative Results
<img src="/files/ftp_upload/1791/1791fig5.jpg" alt="Electrophysiology data with nerve activity graphs and an experimental recording setup." data-altupdatedat="1788235205000" data-alt="Figure 5"> 
Figure 5. (A) Simultaneous four channel recordings from a muscle (the protractor muscle I2), and from three buccal nerves (the radular nerve, RN, buccal nerve 2, BN2, and buccal nerve 3, BN3) during a swallowing response. (B) A still frame from the simultaneous video recording of the freely behaving animal as it swallows a precut seaweed strip (0.5 cm in width), which has been marked at 0.5 cm intervals with white bands so that its movements can be readily visualized as the animal feeds.

<ol><li>Lu, H., Chestek, C. A., Shaw, K. M., Chiel, H. J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Selective+extracellular+stimulation+of+individual+neurons+in+ganglia%5BTitle%5D)+AND+%22J.+Neural+Eng%22%5BJournal%5D)">Selective extracellular stimulation of individual neurons in ganglia.</a> J. Neural Eng. 5, 287-309 (2008).</li>
<li>Morton, D. W., Chiel, H. J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((In+vivo+buccal+nerve+activity+that+distinguishes+ingestion+from+rejection+can+be+used+to+predict+behavioral+transitions+in+Aplysia%5BTitle%5D)+AND+%22J+Comp.+Physiol.+A%22%5BJournal%5D)">In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia.</a> J Comp. Physiol. A. 172, 17-32 (1993).</li>
<li>Warman, E. N., Chiel, H. J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((A+new+technique+for+chronic+single+extracellular+recording+in+freely+behaving+animals+using+pipette+electrodes%5BTitle%5D)+AND+%22J.+Neurosci.+Methods%22%5BJournal%5D)">A new technique for chronic single extracellular recording in freely behaving animals using pipette electrodes.</a> J. Neurosci. Methods. 57, 161-169 (1995).</li>
<li>Ye, H., Morton, D. W., Chiel, H. J., J, H. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((nbsp%3BNeuromechanics+of+multifunctionality+during+rejection+in+Aplysia+californica%5BTitle%5D)+AND+%22J.+Neurosci%22%5BJournal%5D)">nbsp;Neuromechanics of multifunctionality during rejection in Aplysia californica.</a> J. Neurosci. 26, 10743-10755 (2006).</li>
</ol>

A key innovation that has made these recordings successful is combining the electrodes into one cable. Two electrode recordings have been used before, but expanding to four individual electrodes resulted in the formation of surgical adhesions that often prevented the animal from making normal feeding movements. Combining the electrodes into one cable reduces the bulk of the electrodes inside the animal, which in turn reduces the immune response and allows the animal to move more freely.
The o...

<table><tbody><tr><td>Enamel coated stainless steel wire</td><td>California Fine Wire Company</td><td></td><td>0.001D, coating h</td></tr><tr><td>Household Silicone II Glue</td><td>GE Healthcare</td><td></td><td></td></tr><tr><td>Kwik-Sil Adhesive</td><td>World Precision Instruments, Inc.</td><td></td><td></td></tr><tr><td>Duro Qwik-Gel superglue</td><td>Henkel Corp</td><td></td><td></td></tr><tr><td>A-M Systems model 1700 amplifier</td><td>A-M Systems</td><td></td><td>Filter settings:100-1000Hz nerves,10-1000Hz I2 muscle</td></tr><tr><td>Axoscope 10.1</td><td>Molecular Devices</td><td></td><td></td></tr><tr><td>Gold Connector Pins</td><td>Bulgin</td><td>SA3148/1</td><td></td></tr><tr><td>Gold Connector Sockets</td><td>Bulgin</td><td>SA3149/1</td><td></td></tr></tbody></table>

electrode fabrication and implantation in aplysia californica for multi-channel neural and muscular recordings in intact, freely behaving animals

Electrode Fabrication and Implantation in Aplysia californica for Multi-channel Neural and Muscular Recordings in Intact, Freely Behaving Animals

Recording from key nerves and muscles of Aplysia during feeding behavior allows us to study the patterns of neural control in an intact animal. Simultaneously recording from multiple nerves and muscles gives us precise information about the timing of neural activity. Previous recording methods have worked for two electrodes, but the study of additional nerves or muscles required combining and averaging the recordings of multiple animals, which made it difficult to determine fine details of timing and phasing, because of variability from response to response, and from animal to animal. Implanting four individual electrodes has a very low success rate due to the formation of adhesions that prevent animals from performing normal feeding movements. We developed a new method of electrode fabrication that reduces the bulk of the electrodes inside the animal allowing for normal feeding movements. Using a combination of glues to attach the electrodes results in a more reliable insulation of the electrode which lasts longer, making it possible to record for periods as long as a week. The fabrication technique that we describe could be extended to incorporate several additional electrodes, and would be applicable to vertebrate animals.

A technique is described for implanting four in vivo electrodes to monitor the neuromuscular control of feeding behavior in Aplysia californica.

Recording from key nerves and muscles of Aplysia during feeding behavior allows us to study the patterns of neural control in an intact animal.  ...

To make the electrode assembly for multichannel in vivo recordings, four differential electrodes are created and spun together with the individual differential electrodes branching apart. At the ends, the anesthetized animal is pinned out and an incision is made to the side of the eye spot. The target nerves and muscles are located and electrodes are attached to the drop of superglue at the base of the hook, and then insulated with quick seal sealant.Hi, I'm Miranda Collins from the laboratory of Dr.Halal Thiel from the biology department at Kiss Western Reserve University. Today I'll show you a procedure for assembling and implanting electrodes for in vivo recordings in SIA, California. We use this procedure in our laboratory to study the neuromuscular control of feeding and sia.Let's get started. To create the electrode use scissors to cut a piece of enamel coated 0.001 inch diameter stainless steel wire about two feet long. Attach a small ball of putty to each end of the wire.Fold the wire in half and spin the ends to create a twisted pair called a differential electrode. Tape both ends of the wire to prevent unraveling. Make four differential electrodes using a different color of tape for each differential electrode.For identification purposes, twist two of the differential electrodes together, leaving two inches untwisted on one end and one inch on the other end. Repeat with the remaining pair of differential jodes. Twist both sets of two differential electrodes together, making sure that the ends remain untwisted.Hold up the electrode assembly and apply household silicone glue at the junction of the four differential electrodes, leaving the ends free. Hang and allow the glue to dry for at least four hours. To insulate the branches, lay the electrode assembly down on a flat movable surface such as a piece of wood.Use a small piece of plastic to elevate the electrode assembly just before it branches, and secure that with tape. Fan out the ends and secure them with tape. At the dissecting microscope, use forceps to coat the branches with silicone glue.The one inch long ends will be inside the animal, so they should have a very thin coat of glue. Allow the glue to dry for at least three hours. Shorten the one inch long end of one differential electrode to two centimeters on each end of the electrode.Use forceps to scrape silicone and enamel away from both wires. To reveal one centimeter of bare wire curl one bare wire into a hook for recording. Then the other wire up and away from the hook to serve as the ground wire on the two inch long end solder a gold connector pin to each wire.Use a piece of tape to secure the end and keep space between the ground and recording pins. Repeat these steps so that there are hooks and gold connectors on all four differential electrodes. Attach a one to two centimeter ball of the silicone glue to the cable about 1.5 inches from the hook end.To anchor the electrodes within the animal allowed to dry for at least one hour, select a healthy animal that weighs about 350 to 450 grams in response to small pieces of seaweed. The animal should generate bites at intervals of between three to five seconds. The complete surgery with electrode implantation should take about an hour.Lay the anesthetized animal out in a dissection tray with its foot down facing the animal head on. Shift the gill area to your left such that the animal is partially on its side leaning away, pinned down the anterior tentacles. Place the tray on the stage of a dissecting microscope.Prop up the tray at about a 20 degree angle to elevate the head and collect the hemolymph in the tail away from the incision using dissection scissors, start an incision slightly to your right of the eye spot and extend it one to 1.5 centimeters towards the head. Use your tractors. Attach to the edges of the tray to hold the incision open.To expose the buccal mass. Use forceps to lift the clear membrane underneath the skin and use scissors to cut an opening, matching the main incision. Tuck the edges of the membrane into the retractors.Place the electrode assembly on a micro manipulator and move it over the animal's incision. Each of the four electrodes will take about 10 to 15 minutes to attach access to the nerves will be shown first followed by attachment to the electrode to the final nerve. However, in practice, each nerve should be attached to an electrode before the next nerve is exposed.The ular nerve is most difficult to access and should be approached first. There are two options for accessing the ular nerve. The first option, which is preferable, is to look under the buccal ganglion between BN one and VN two.If a branch of the ular nerve is visible, use fine tipped forceps bent into a hook to lift out the branch. If a branch of the ular nerve is not accessible above the muscle, a second option is to access it via a small incision in I two next to the connective tissue at the base of the buccal ganglion. The incision in I two must go through two layers of the I two muscle to attach an electrode to I two.Use the hooked forceps to lift and separate two bands of the I two muscle access buccal nerve two here. Buccal nerve three is here and will be used to demonstrate electrode attachment. All the electrodes are attached in the same way as demonstrated now on buccal nerve three.Once the nerve is hooked on the forceps, use another set of forceps to manipulate one electrode hook onto the nerve using the micro manipulator. Raise the hook so that the nerve lifted up and away from the buccal mass. Clear of any other nerves or tissue lifted as little as possible, half a centimeter or less.To avoid overstretching the nerve, use a kim wipe to dry off the electrode and adjacent area of the nerve. An insect pin is used to apply the glue, secure the electrode with a small dab of superglue where the base of the hook is in contact with the bottom of the nerve. Apply a drop of alysia saline or hemo lymph to set the super glue.Then red dry the hook on an ice pack mix. Quick seal glue. This keeps the glue workable for about 30 minutes.Additional mixings may be necessary over the course of the surgery. Use the insect pin to completely cover any exposed wire of the hook with a small amount of quick seal. Avoiding the ground wire.Allow the glue to set for five minutes. Readjusting the glue. If it pulls away from the hook, wait until the glue is dry before accessing the next nerve.Once all the electrodes are attached, slide the electrode assembly into the animal up to the silicone anchor. Suture the incision closed around the protruding electrode cable. Keeping the anchor inside the animal super glue the stitches to ensure a good seal.Insert the gold connector tips at the other end of the electrode into a small block of styrofoam. Return the animal to the main tank in an aerated isolation container for recovery overnight. Acclimate the animal in an aerated container while attached to the recording equipment for at least 1.5 hours.Monitor the signal while the animal is acclimating to verify that all electrodes are working and that noise levels are low. Use a video camera to record feeding behavior while using the computer to record signals from the neural and muscular electrodes. Synchronize the video and electrode recordings using a square wave signal that controls a digital counter in the camera view while it is simultaneously recorded as an additional channel on the computer.In aScope when the animal is feeding, there will be bursts of activity on the nerves and muscle. Here's an example of a swallowing pattern with EMG activity from I two and ENG from RN BN two and BN three. We've just shown you how to fabricate and implant multichannel electrodes to record the neural and muscular activity during feeding behavior in freely behaving sia.When doing this procedure, make sure to handle the nerve carefully and make sure to completely seal the recording hooks such that none of the wire is exposed. Thanks for watching and good luck with your experiments.

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Learn electrode fabrication and implantation in Aplysia californica for multi-channel neural and muscular recordings. This technique enables real-time monitoring of neuromuscular control during feeding behavior.

Electrode Fabrication and Implantation in Aplysia californica for Multi-channel Neural and Muscular Recordings in Intact, Freely Behaving Animals (Video) | JoVE Journal

Electrode Fabrication and Implantation in Aplysia californica for Multi-channel Neural and Muscular Recordings in Intact, Freely Behaving Animals

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