Author: Silverstein, Justin
Date published: March 1, 2012
Localization of the sensory and motor cortices can be traced back to the late 19th century when surgeons, scientists, and neurologists such as Sir David Ferrier and Sir Victor Horsley were utilizing direct cortical stimulation (DCS) to begin to understand structural function of the pre and post Rolandic areas. In 1888, C.B. Nancrede mapped the motor cortex utilizing a battery operated bipolar probe that delineated function of the face, forearm, elbow, and shoulder, which in turn gave insight to the functional layout of the homunculus (Uematsu et al. 1992). The homunculus is an upside down representation of the body within the sensory and motor cortices (Figure 1). It starts deep within the longitudinal fissure where the genitals and lower extremities are represented and continues laterally to the border of the temporal lobe where face representation occurs. The motor representation follows the precentrai gyrus of the frontal lobe; the sensory representation of the homunculus is found on the postcentral gyrus of the parietal lobe. From medial to lateral, the sensory and motor cortices are represented as follows: lower extremities, trunk, arms, hands, and face. However, each person has individual variance and deviations in anatomical make-up (Brodai 2004, Carlson 2007, Marieb and Hoehn 2007).
Penfield and Boldrey (1937) noted that when the precentrai gyrus is stimulated, a muscle contraction is seen from the contralateral side of the body which specifically correlates to anatomy based on which part of the gyrus is stimulated. Also noted was a need for more stimulus intensity when stimulating anterior to the precentrai gyrus which elicited more complex muscle actions indicating sensitive but nonspecific muscle action generated from the premotor and supplementary motor areas of the cerebrum. Charles Sherrington in the early 190Os began to utilize monopolar stimulation to elicit motor responses and began the era of delineating the pre-Rolandic area (precentrai gyrus) as motor cortex and post-Rolandic area (postcentral gyrus) as sensory cortex in simians. Harvey Gushing, a neurosurgeon who studied with Sherrington, went on to perform DCS in anesthetized human patients with outcomes that paralleled Sherrington's primate mapping. Gushing was one of the first people to point out that the Rolandic fissure (central sulcus) was the definitive separation point between the sensory and motor cortices, demonstrating the ideas of narrow motor and sensory strips as opposed to the thought of broader motor and sensory areas (Uematsu et al. 1992). Initially bipolar stimulators were utilized to locate areas that showed distal motor function and were first employed to treat patients undergoing surgery for focal epilepsy (Goldring and Gregorie 1984, O'Leary and Goldring 1976). In the mid to late 20th century somatosensory evoked potentials produced by stimulating peripheral nerves to evoke responses recorded directly from the surface of the brain were reported. Robust sensory responses were noted with a drop in amplitude occurring at the central sulcus and a phase reversal of the response seen in the motor cortex (Lüders et al. 1986).
The case that follows shows how modern neurophysiological techniques are indebted to the pioneers of cortical mapping. Although these modern techniques are vastly more sophisticated, they are built on a foundation that began in the late 19th century.
A 22-year-old, 5 '8", 54 kg, male with no past medical history for medical or neurological problems presented with a new onset of status epilepticus consisting of left face and left upper extremity jerking that had been persistent during the past four weeks. Prior to the onset of status epilepticus, the patient demonstrated no symptoms with the exception of a headache the day before. The differential diagnosis was encephalitis due to an unknown viral infection.
The patient was anesthetized and monitored in the intensive care unit (ICU) prior to being brought to the operating room. A craniotomy was performed to localize the focal point of the status epilepticus. Electroneurophysiological modalities used to map the brain include sensorimotor localization (phase reversal) and direct cortical stimulation (DCS). Sensorimotor localization was used to differentiate the motor and sensory cortices by utilizing a somatosensory evoked potential. DCS was used to identify eloquent cortex and verify "safe zones" that could be potentially resected or sub-peeled without adverse neurological deficits post-operatively. DCS also allowed the surgeon to map out the functional anatomy of the precentrai gyrus. A 16-channel Protektor(TM) IOM (XLTEK, Natus Medical Inc., San Carlos, California, USA) was used for both phase reversal sensorimotor localization and direct cortical stimulation.
The patient was placed in a supine position with the head turned to the left at 90 degrees. The head was fixated with pins in a Mayfield head holder. A bump was placed under the patient's right shoulder to help in rotation. A craniotomy was performed, a skin flap was made, and a bone plate was removed over the right lateral section of the skull. The dura mater was peeled back and a 1 ? 6 subdurai strip electrode was placed for acquisition of somatosensory evoked responses for sensorimotor localization. Each contact of the subdural electrode was referenced to Fz of the International 10-20 System. Stimulation electrodes were placed over the left median nerve at the wrist (between the palmaris longus and flexor carpi radialis tendons) which was contralateral to the site of the lesion. Stimulation was delivered transcutaneously at 25 mA with a sweep of 1000 trials, a duration of 0.20 msec, and a repetition rate of 4.7 Hz. Total intravenous anesthesia (TIVA) of propofol, sufentanil, and ketamine was utilized with no muscle relaxant. The anesthesiologist placed a soft bite block for protection of the tongue and endotracheal tube. Ice-cold saline was available on the sterile field in case a seizure was induced due to direct cortical stimulation. Afterdischarges were not monitored; however, electrocorticography was utilized by a staff neurologist after the functional brain mapping occurred, using two subdural grid electrodes (8x8 and 2x8) (Figure 2) to locate and follow the driver for the status epilepticus.
A baseline phase reversal was obtained with sensory cortex being represented from contacts 1 and 2 and motor cortex being represented by contacts 3 through 6 (Figures 3A and 3B). The phase reversal indicated a posterior to anterior placement of the strip electrode with contact 1 being most posterior. Once the baseline was established, the surgeon proceeded to move the strip posteriorly where the phase reversal was found between contacts 3 and 4 (Figures 4A and 4B). The strip was moved laterally which kept the phase reversal between contacts 3 and 4 (Figures 5A and 5B). Next, the electrode was moved anteriorly and the phase reversal was seen between contacts 2 and 3 (Figure 6A and 6B). The surgeon lifted the strip and reversed how it sat on the cortex (now anterior to posterior). This change obtained sensory responses from contacts 1 and 2, with no response from contacts 3 through 6; no phase reversal was obtained (Figures 7A and 7B). The surgeon placed the electrode in its initial direction (posterior to anterior) and moved the strip anteriorly. A phase reversal was identified between contacts 4 and 5 (Figures 8A and 8B).
Direct cortical stimulation utilized the same 1 ? 6 subdural strip electrode. Each contact of the strip electrode acted as a monopolar anodal (+) stimulator referenced to a non-cephalic cathode (-) placed outside the field inferior to the right ear at the base of the skull. A pulse trained stimulus was delivered at 15 mA with a 500 Hz repetition rate and a 0.5 msec duration. Needle electrodes were placed in various musculature contralateral to the site of the lesion. These muscles included the left oris (face), left biceps (upper arm), left flexor carpi radialis (forearm), left abductor pollicus brevis (hand), left vastus lateralis (upper leg), and left tibialis anterior (lower leg). Due to limited channels, the oris electrode was not plugged in until the surgeon believed he was in an area which would elicit a face response.
With the final phase reversal indicating the motor cortex being represented under contact 5, DCS began with contact 5. Upon initial stimulation, the flexor carpi radialis was saturated with noise and had to be essentially turned off by decreasing the screen gain. Contact 5 elicited an upper arm and hand response (Figure 9). The surgeon moved the strip posteriorly but within the same plane and no response was obtained from any musculature (Figure 10). Next, the strip was moved laterally and only an upper arm response was obtained (Figure 11). Moving the strip laterally again, the surgeon requested the face be monitored. Contact 4 was stimulated and a face response was obtained (Figure 12). Again, the strip was moved laterally and a face response was elicited from contact 4 (Figure 13). The surgeon requested stimulation from contact 6, where a response from the face was subsequently elicited (Figure 14). The electrode was moved medially next, where responses from the upper arm and face were obtained from contact 2 (Figure 15).
Somatosensory evoked potentials (SSEPs) are utilized for an array of diagnostic and prognostic evaluations, as well as a means to monitor spinal cord and brain function during surgery (Chiappa 1990, Legati 1995). The SSEP is perceived as a neuronal relay elicited by an electrical stimulus starting at the peripheral nerve as the primary IA afferent sensory neuron. The primary neuron travels up the peripheral nerve where it enters the dorsal column-medial lemniscus tract of the spinal cord on the same side in which it enters. The dorsal column is specific to touch, vibration, and proprioception and the axons of the dorsal column are usually heavily myelinated, making for saltatory or fast conduction with propagation of action potentials from one Node of Ranvier to the next. If the neuron enters the dorsal column below the spinal cord level of T6, it travels the fasciculis gracilis tract (Figures 16 and 17). If the primary neuron enters at or above T6, then it travels up the fasciculis cuneatus tract (Figures 16 and 17). Depending on which route the neuron takes (cuneatus or gracilis), when the primary neuron reaches the brainstem it synapses with a secondary neuron in one of the respective nuclei (cuneatus or gracilis). Here the secondary neuron decussates at the medial lemniscus and travels to the ventral posterolateral nucleus of the thalamus where it synapses with the tertiary neuron. The tertiary neuron ascends via the posterior limb of the internal capsule to the primary sensory cortex (Figure 17). Stimulus of an SSEP usually occurs over large mixed nerve trunks such as the median or ulnar nerves in the upper extremities and the posterior tibial or peroneal nerves in the lower extremities (Brodai 2004).
The evoked potential seen from the sensory cortex following median nerve stimulation is a negative deflection with a peak latency at about 20 msec (N20) followed by a positive deflection at 30 msec (P30). However, when the subdural electrode is placed over the motor cortex, a mirror image of the N20 occurs. The reason for the phase reversal is still not fully understood; however, it is postulated that sensory impulses from the thalamus are being sent to the posterior wall of the central sulcus and that neurons within the pre-Rolandic area are generators for the P22 response. Association fibers from Brodmann's area 3B may influence the generation of the P22; however, it is most likely direct projections from the thalamus to the motor cortex eliciting the response (Moore and Newell 2005). Phase reversal is a common modality used to differentiate the primary motor cortex from the primary sensory cortex using a somatosensory evoked potential.
DCS is considered the "gold standard" for mapping the eloquent areas of the brain and is utilized during awake and anesthetized craniotomies for tumor resection or epilepsy (Picht et al. 201 1, González-Darder et al. 201 1). Bipolar DCS is the most common form of cortical stimulation especially in awake patients. However, anodal monopolar stimulation based on the teachings of Hern and Gorman, show better excitability in the neurons of anesthetized patients (Kombos and Suss 2009). Monopolar stimulation hyperpolarizes motor dendrites activating corticospinal volleys much easier and faster in anesthetized patients, where bipolar stimulation will often require more current and more time (2 to 4 seconds) to elicit a response (Kombos and Suss 2009). DCS is used as a tool to map the motor cortex and differentiate functional areas of the motor cortex. In principle, it is much like a transcranial motor evoked potential (TCMEP); however, the stimulus is delivered directly to the brain's surface. Like a TCMEP, a compound muscle action potential (CMAP) is elicited from different musculature where EMG electrodes have been placed.
Electrophysiological mapping of the sensory and motor cortices is a vital aspect to the safety of brain surgery. This is especially important as incision sites become smaller, surgeries become more complex, and landmarks are not as easily recognizable (Duffau 2007). The cortical mapping provided in this case allowed the surgeon to differentiate the motor cortex from the sensory cortex, as well as create a topographic map of the motor cortex while the patient was under general anesthesia (Figure 1 8). Multi-modality mapping should be conducted when loss of motor function is a co-morbidity associated with brain surgery. For over one hundred years this has been a proven method to help guide surgeons in the mapping of anatomical and functional landmarks.
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Justin Silverstein, CNIM, R.NCS.T., CNCT, MS
Director of Clinical Neurophysiology
Spine Medical Services, PLLC
Commack, New York