Name: Surgical Training for the Implantation of Neocortical Microelectrode Arrays Using a Formaldehyde-fixed Human Cadaver Model (Video) | JoVE Journal
Uploaded: 2017-11-19T13:00:00.000+00:00
Duration: 8 min 11 s
Description: Learn surgical techniques for implanting neocortical microelectrode arrays using a formaldehyde-fixed human cadaver model. This training method prepares neurosurgeons for precise brain-computer interface procedures.

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5 minutes

The authors are grateful to Dr. Rob Franklin (Blackrock Microsystems), Prof. Margitta Seeck (Division of Neurology, Geneva University Hospitals, Geneva, Switzerland), Dr. Andrea Bartoli and Prof. Karl Schaller (Division of Neurosurgery, Geneva University Hospitals, Geneva, Switzerland), and Mr. Florent Burdin and Prof. John P. Donoghue (Wyss Center for Bio and Neuroengineering, Geneva, Switzerland) for their support in preparing the present work.

The human cadaver used in this work was provided under the framework of body donations for medical education. Informed consent for body donation was obtained in writing during the lifetime of the donor. In accordance with the federal and cantonal laws, no review by an ethics committee was necessary.
Note: This protocol assumes that the persons performing the practice surgery are neurosurgeons with training and expertise in standard neurosurgical procedures, including patient positioning and head fixation, craniotomy and durotomy, and suturing. In addition to the tools and equipment specific to the microelectrode array, standard neurosurgical tools and equipment are used.
1. Selection of the cadaver and setup of the operating room
<ol>
	<li>Select a specimen with no history of disease or injury to the head, skull and brain.
	<ol>
		<li>Optionally, perform a computed tomography (CT) scan of the cadaver&#39;s head to ensure that there is no significant intracranial lesion (Figure 1A), e.g. chronic subdural hematoma or an intra-axial expansive lesion. Using the CT scan, identify a target cortical area for the implantation of the microelectrode array (such as the &#34;hand knob&#34; area of the precentral gyrus, corresponding to the representation of the hand in the primary motor cortex27, in the case of training for the implantation of a BCI).</li>
	</ol>
	</li>
	<li>Position cadaver in lateral decubitus on an operating table. Use an operating table rather than a dissection table in order to add to the realism of the OR-like environment and facilitates the fixation of the skull clamp and pneumatic impactor. Position the cadaver in lateral decubitus in order to allow the fronto-temporal approach in a formaldehyde-fixed cadaver, in whom neck rotation is limited.</li>
	<li>Fix the head in the skull clamp (Figure 1B). Cover with surgical drapes (Figure 1C). 
	Note: In our case, the posterior pins of skull clamp are unusually positioned in the sagittal plane of the head (see Figure 1B), because we used a skull clamp that had been modified for surgical training purposes to hold a cadaveric head separated from the rest of the body.
	<ol>
		<li>When using a standard skull clamp on an operating table, place the posterior pins securing the head perpendicular to the sagittal plane.</li>
	</ol>
	</li>
</ol>
2. Exposure of the neocortical surface
<ol>
	<li>Incise the scalp using a scalpel, following a question-mark incision to expose the temporal and frontal bones. Dissect the temporalis muscle along the posterior edge of the incision. Recline the scalp and temporalis muscle by blunt dissection (Figure 1D).</li>
	<li>Perform a large square fronto-temporal craniotomy, e.g. 5 x 5 cm (Figure 2A). For that purpose, drill four burr holes at the corners of the intended craniotomy. Then, use the craniotome to connect the burr holes. Remove the bone flap using a spatula, exposing the dura mater. Store the bone flap in saline solution.</li>
	<li>Open the dura mater on three sides of the craniotomy using dura scissors (Figure 2B). Recline it and expose the arachnoid membrane and the surface of the cerebral neocortex (Figure 2C).</li>
</ol>
3. Fixation of the electrode pedestal
<ol>
	<li>Select a cortical gyrus where the microelectrode array will be implanted. Select a gyral surface that is approximately flat so that the microelectrode array will lie flush with it when inserted. Ensure that there is no visible blood vessel coursing on the cortical surface where the microelectrode array will be inserted.</li>
	<li>Select a site for the fixation of the electrode pedestal on the superior edge of the craniotomy, close to the skin incision, and allowing sufficient slack for the wire bundle so that the microelectrode array can reach the target gyrus. Screw the pedestal onto the external table of the skull bone next to the craniotomy (Figure 2D). Use 6 to 8 self-tapping cortical bone screws (6 mm length, 2 mm diameter) to ensure appropriate fixation.
	<ol>
		<li>When manipulating the pedestal, always ensure that the microelectrode array does not touch anything (it may be damaged or could lacerate the neocortical surface) by holding the wire bundle close to the microelectrode array with tweezers with plastic- or rubber-coated tips (Figure 2E).</li>
	</ol>
	</li>
</ol>
4. Positioning and insertion of the microelectrode array
<ol>
	<li>Position the microelectrode array parallel with the surface of the target gyrus. Bend the wire bundle as necessary for that purpose (Figure 3A). 
	Note: The stiff wire bundle does not easily conform to the surgeon&#39;s wishes. Care and patience are required to obtain good alignment of the microelectrode array and cortical surface.
	<ol>
		<li>Optionally, use &#34;dog-bone&#34; titanium straps to secure the wire bundle to the skull and control its course toward the target gyrus. Do not screw the strap too tightly to avoid damaging the wire bundle.</li>
	</ol>
	</li>
	<li>Bring the pneumatic impactor into approximate alignment with the back of the microelectrode array (Figure 3B). Control the connections of the pneumatic impactor to its control box, and then turn on the control box. 
	Note: Make sure that the pneumatic impactor is at least 5 mm away from the array before turning the control box on, as the pneumatic impactor might be triggered when first turned on.</li>
	<li>Use the millimetric screws of the pneumatic impactor holder to refine the impactor&#39;s alignment with the back of the microelectrode array (Figure 3B, inset). Using the impactor, apply an excursion distance- and pressure-controlled tap to the back of the microelectrode array and insert it into the cortical surface, pushing it through the arachnoid membrane. 
	Note: Check that the microelectrode array is flush with the cortical surface.</li>
</ol>
5. Positioning of the subdural ECOG grid
Note: This step is optional.
<ol>
	<li>Position a subdural ECOG grid over the exposed cortical surface (Figure 3D). If necessary, remove electrodes by cutting through the grid so that the overall shape of the ECOG grid fits the craniotomy.</li>
	<li>Orient the ECOG grid so that its wires will exit the dura mater and skull superiorly or posteriorly.</li>
	<li>Irrigate the ECOG grid with saline before placing it into contact with the cortical surface.</li>
	<li>Secure the ECOG grid by suturing it to the dura mater at the edges of the durotomy.</li>
</ol>
6. Repositioning and closure of the dura mater, bone flap, and skin flap
<ol>
	<li>Reflect the dura mater back over the exposed cortical surface and suture it to the edges of the durotomy.</li>
	<li>Screw &#34;dog-bone&#34; titanium straps onto the edges of the bone flap using self-tapping cortical bone screws. Reposition the bone flap within the craniotomy. Secure the bone flap to neighboring skull bones with the &#34;dog-bone&#34; titanium straps and self-tapping cortical bone screws. Take care not to crush the wire bundle of the microelectrode array (and those of the optional ECOG grid) between bone edges.</li>
	<li>Reflect and suture the skin flap. Close the skin incision around the neck of the electrode pedestal (Figure 3E).
	<ol>
		<li>Alternatively, allow the pedestal to egress the scalp through a separate stab incision made into the scalp flap.</li>
	</ol>
	</li>
</ol>

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<li>Yiasemidou, M., Roberts, D., Glassman, D., Tomlinson, J., Biyani, S., Miskovic, D. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((A+Multispecialty+Evaluation+of+Thiel+Cadavers+for+Surgical+Training%5BTitle%5D)+AND+%22World+J.+Surg%22%5BJournal%5D)">A Multispecialty Evaluation of Thiel Cadavers for Surgical Training.</a> World J. Surg. , (2017).</li>
<li>Ploch, C. C., Mansi, C. S. S. A., Jayamohan, J., Kuhl, E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Using+3D+Printing+to+Create+Personalized+Brain+Models+for+Neurosurgical+Training+and+Preoperative+Planning%5BTitle%5D)+AND+%22World+Neurosurg%22%5BJournal%5D)">Using 3D Printing to Create Personalized Brain Models for Neurosurgical Training and Preoperative Planning.</a> World Neurosurg. 90, 668-674 (2016).</li>
<li>Del Castillo-Calcáneo, J., Donoghue, J. A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((A+Novel+Method+for+3-Dimensional+Printing+a+Brain+That+Feels+and+Looks+Like+One%3A+The+Next+Step+in+the+Search+of+the+Perfect+Neurosurgical+Simulator%5BTitle%5D)+AND+%22World+Neurosurg%22%5BJournal%5D)">A Novel Method for 3-Dimensional Printing a Brain That Feels and Looks Like One: The Next Step in the Search of the Perfect Neurosurgical Simulator.</a> World Neurosurg. 91, 620-622 (2016).</li>
<li>Martin, S., Millán, J. D. R., Knight, R. T., Pasley, B. N. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((The+use+of+intracranial+recordings+to+decode+human+language%3A+Challenges+and+opportunities%5BTitle%5D)+AND+%22Brain+Lang%22%5BJournal%5D)">The use of intracranial recordings to decode human language: Challenges and opportunities.</a> Brain Lang. , (2016).</li>
</ol>

The authors have nothing to disclose.

The formaldehyde-fixed human cadaver model and the surgical protocol described here replicate the surgical procedure of implanting microelectrode arrays into the human cerebral neocortex. Each step of the procedure, including the positioning of the microelectrode array and its insertion with the pneumatic inserter, proceed in almost the same fashion as in a real-life patient, with the exception that cerebral pulsation and circulation are absent. The critical steps in the protocol are the alignment of the microelectrode a...

Recent years have seen the development of technological solutions to the challenge of recording the activity of multiple individual neurons in the living brain1,2,3. Silicon-based microelectrode arrays perform similarly to conventional wire microelectrodes in terms of signal properties, and they can record from dozens to hundreds of neurons in a small patch of cerebral tissue4,5,6,7. Microelectrode arrays have allowed scientists to establish the correspondence between neural activity in the primary motor cortex of monkeys and arm movements8, which in turn has provided a boost to the development of brain-computer interfaces (BCIs)9.
Microelectrode arrays have been used in humans in two situations: as chronic implants to control BCIs and as semi-chronic implants to study the activity of individual neurons in patients suffering from epilepsy. Chronic implants, targeting the functional representation of the hand in primary motor cortex, have allowed patients suffering from tetraplegia to control the motion of a robotic arm or of computer cursors10,11,12,13. Semi-chronic implants, inserted together with subdural electrocorticography (ECOG) electrodes in patients with drug-resistant epilepsy who are candidates for epilepsy surgery14, allow single-unit recordings before, during and after seizures, and have begun to shed light on the activity of single neurons during and in between epileptic seizures15,16,17,18,19. Microelectrode arrays have the potential to significantly improve our understanding of how the brain functions by establishing a link between the activity of neurons, on the one hand, and the perceptions, movements and thoughts of human beings, both in health and in disease, on the other20,21.
Silicon-based microelectrode arrays are now available commercially and their use in humans has been approved by regulatory authorities in the USA in the semi-chronic epilepsy indication. However, these devices are invasive and must be inserted into the brain. The negative consequences of improper insertion technique, beyond the failure of the device to record neuronal activity, include cerebral hemorrhage and infection, with the potential for long-lasting or permanent neurological dysfunction. Although the complication rate of microelectrode array implantation is currently unknown, the rate of potentially serious complications during the implantation of intracranial electroencephalography (EEG) macroelectrodes is 1-5%22,23. Therefore, the proper implantation of microelectrode arrays requires both extensive neurosurgical skills and procedure-specific training.
The approaches available for surgeons to hone their skills with microelectrode arrays in a safe environment include non-human mammals and human cadavers. The ideal training model would faithfully reproduce the size and thickness of the human skull; the toughness and vascular ramification of the dura; the gyrification pattern, consistency and pulsation of the human brain; the presence of circulating blood and cerebrospinal fluid; and the overall positioning of the subject in an operating room (OR)-like environment. Thus, animal models need to be of a sufficient size to provide a meaningful experience to the surgeons. Large non-human primates come closest, but their use for surgical training is unsustainable both from an ethical perspective and because they are expensive. Rodents do not enter consideration because of their small size; using even cats or rabbits implies diverging significantly from an OR-like environment.
Human cadavers represent an attractive alternative. Their advantages include the life-like size and shape of the head and brain and the possibility of setting up surgical training in an OR-like environment. The most obvious departures from a realistic situation are the absence of cerebral pulsations and bleeding and the modifications in the aspect and consistence of body tissues that are specific to the technique employed for cadaver preservation24. Fresh-frozen cadavers preserve the consistency and flexibility of many organs and tissues to some extent, but they have several drawbacks: they start degrading as soon as thawing begins, so that the brain becomes too degraded for the insertion of a microelectrode array to be performed realistically, and they are a relatively rare and expensive resource. Formaldehyde-fixed cadavers, on the other hand, are more affordable and available and much more durable, at the expense of hardened tissue consistency.
Here, we establish a procedure using a formaldehyde-fixed human cadaver model to provide neurosurgical training for the implantation of a neocortical microelectrode array. Our approach allows realistic, OR-like positioning and instrumentation; performing craniotomy and durotomy and exposing the neocortical surface; attaching the electrode pedestal to the skull bone neighboring the craniotomy; and inserting the microelectrode array into the neocortex with a pneumatic impactor25. Critically, it enables surgeons to practice the precise alignment of the microelectrode array (which is connected to the electrode pedestal by a bundle of individually insulated gold wires) parallel to the neocortical surface26. Our protocol faithfully replicates the indication of microelectrode array implantation together with ECOG implantation in patients who are candidates for epilepsy surgery. The particulars of the implantation surgery are influenced significantly by the exact type of microelectrode array; here, we describe the procedure for an array that recently received regulatory approval for use in humans in the USA. The so-called Utah array comprises a 4x4 mm, 100 microelectrode grid; a transcutaneous pedestal that is attached to the external table of the skull; and a wire bundle connecting the two.

<table><tbody><tr><td>Mayfield skull clamp</td><td>Integra LifeSciences, Cincinnati, OH</td><td>A1059</td><td></td></tr><tr><td>Midas Rex MR7 system for craniotomy</td><td>Medtronic, Minneapolis, MN</td><td>EC300</td><td></td></tr><tr><td>Dura scissors</td><td>Sklar Surgical Instruments, West Chester, PA</td><td>22-2742</td><td></td></tr><tr><td>Self-tapping bone screws</td><td>OrthoMed Inc., Tigard, OR</td><td>OM SYN211806</td><td></td></tr><tr><td>Microelectrode array and pedestal</td><td>Blackrock Microsystems, Salt Lake City, UT</td><td>LB-0612</td><td>Mock-up arrays are available from the manufacturer upon request</td></tr><tr><td>Pneumatic impacter</td><td>Blackrock Microsystems, Salt Lake City, UT</td><td>LB-0088</td><td></td></tr><tr><td>64-channel electrocorticography grid</td><td>Ad-Tech Medical Instrument Corporation, Racine, WI</td><td>FG64C-SP10X-0C6</td><td>Optional</td></tr></tbody></table>

surgical training for the implantation of neocortical microelectrode arrays using a formaldehyde-fixed human cadaver model

Surgical Training for the Implantation of Neocortical Microelectrode Arrays Using a Formaldehyde-fixed Human Cadaver Model

This protocol describes a procedure to assist surgeons in training for the implantation of microelectrode arrays into the neocortex of the human brain. Recent technological progress has enabled the fabrication of microelectrode arrays that allow recording the activity of multiple individual neurons in the neocortex of the human brain. These arrays have the potential to bring unique insight onto the neuronal correlates of cerebral function in health and disease. Furthermore, the identification and decoding of volitional neuronal activity opens the possibility to establish brain-computer interfaces, and thus might help restore lost neurological functions. The implantation of neocortical microelectrode arrays is an invasive procedure requiring a supra-centimetric craniotomy and the exposure of the cortical surface; thus, the procedure must be performed by an adequately trained neurosurgeon. In order to provide an opportunity for surgical training, we designed a procedure based on a human cadaver model. The use of a formaldehyde-fixed human cadaver bypasses the practical, ethical and financial difficulties of surgical practice on animals (especially non-human primates) while preserving the macroscopic structure of the head, skull, meninges and cerebral surface and allowing realistic, operating room-like positioning and instrumentation. Furthermore, the use of a human cadaver is closer to clinical daily practice than any non-human model. The major drawbacks of the cadaveric simulation are the absence of cerebral pulsation and of blood and cerebrospinal fluid circulation. We suggest that a formaldehyde-fixed human cadaver model is an adequate, practical and cost-effective approach to ensure proper surgical training before implanting microelectrode arrays in the living human neocortex.

Our protocol uses a formaldehyde-fixated human cadaver model to allow surgeons to practice the surgical procedure of implanting a microelectrode array into the cerebral neocortex in a realistic, OR-like environment. The option of performing post-mortem neuroimaging, such as head CT, will confirm the absence of any significant intracranial lesion (Figure 1A) and can help with the selection of the implantation site. Working with an entire specimen and setting up for surgery on an operating tab...

We designed a procedure in which a formaldehyde-fixed human cadaver is used to assist neurosurgeons in training for the implantation of microelectrode arrays into the neocortex of the human brain.

This protocol describes a procedure to assist surgeons in training for the implantation of microelectrode arrays into the neocortex of the human brain. ...

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Research

JoVE Journal

Medicine

We provide useful information for surgeons who are learning the process of implanting chronic neural recording electrodes.  Techniques for both penetrating and surface electrode systems are described in a rodent animal model.

Surgical Implantation of Chronic Neural Electrodes for Recording Single Unit Activity and Electrocorticographic Signals

The video demonstrates a procedure for implanting a wireless bidirectional multichannel electrode unit into a rat brain to record and stimulate multichannel neural networks.

Implanting a Wireless Bidirectional Microelectrode System in a Rat Brain

This video demonstrates a technique for implanting an electrode assembly into a mouse brain. The assembly contains bipolar electrodes to record activity from the hippocampus and a reference electrode to obtain baseline activity from the cerebellum. An anesthetized mouse is placed on a stereotaxic frame, and the electrode assembly is implanted in the target brain region. The animal is then allowed to recover before performing electrophysiological recording.

Implantation of an Electrode Assembly in a Mouse Brain for Electrophysiological Recording

Shuttle-box avoidance learning is well-established in behavioral neuroscience. This protocol describes how shuttle-box learning in rodents can be combined with site-specific electrical intracortical microstimulation (ICMS) and simultaneous chronical in vivo recordings as a tool to study multiple aspects of learning and perception.

Combined Shuttle-Box Training with Electrophysiological Cortex Recording and Stimulation as a Tool to Study Perception and Learning

We have developed a whole-cortical electrocorticographic array for the common marmoset that continuously covers almost the entire lateral surface of cortex, from the occipital pole to the temporal and frontal poles. This protocol describes a chronic implantation procedure of the array in the epidural space of the marmoset brain.

Chronic Implantation of Whole-cortical Electrocorticographic Array in the Common Marmoset

This work presents a protocol to perform a stereotaxic, neurosurgical implantation of microelectrode arrays in the common marmoset. This method specifically enables electrophysiological recordings in freely behaving animals but can be easily adapted to any other similar neurosurgical intervention in this species (e.g., cannula for drug administration or electrodes for brain stimulation).

Stereotaxic Surgery for Implantation of Microelectrode Arrays in the Common Marmoset (Callithrix jacchus)

This report describes the methods to generate a model of temporal lobe epilepsy based on the electrical kindling of transgenic VGAT-Cre mice. Kindled VGAT-Cre mice may be useful in determining what causes epilepsy and for screening novel therapies.

Preparation and Implantation of Electrodes for Electrically Kindling VGAT-Cre Mice to Generate a Model for Temporal Lobe Epilepsy

Here, we introduce a lightweight, cost-effective probe implant system for chronic electrophysiology in rodents optimized for ease of use, probe recovery, experimental versatility, and compatibility with behavior.

The DREAM Implant: A Lightweight, Modular, and Cost-Effective Implant System for Chronic Electrophysiology in Head-Fixed and Freely Behaving Mice

This protocol presents a microcontroller-based behavioral box to assess prepulse inhibition (PPI) by collecting acceleration data from a sensor beneath the box. This data evaluates sensory gating deficits in socially isolated rats, with an added method for synchronizing data with neuronal activity to advance neurophysiology studies on behavioral disorders.

Developing a Behavioral Box for Assessing Prepulse Inhibition and Neural Activity in Psychiatric Animal Models

Here, we present a structured protocol for cochlear implant electrode insertion training using a novel simulation system, enabling hands-on practice across normal and malformed inner ear anatomies.

Testing a Cochlear Implant Electrode Insertion Training System for Optimal Electrode Array Placement in Different Inner Ear Anatomies

This protocol describes a two-phase surgical method to create a large, resealable, dura-sparing cranial window in mice. This technique enables chronic, multi-modal electrophysiological recordings from distributed, deep-brain networks, such as the Default Mode Network, over several weeks.

Surgical Protocol for a Large, Resealable Cranial Window Enabling Longitudinal, Multi-Modal Electrophysiology Recordings of Mouse Default Mode Network

Learn surgical techniques for implanting neocortical microelectrode arrays using a formaldehyde-fixed human cadaver model. This training method prepares neurosurgeons for precise brain-computer interface procedures.

Surgical Training for the Implantation of Neocortical Microelectrode Arrays Using a Formaldehyde-fixed Human Cadaver Model

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