motor cortex - bmj · katayama, tsubokawa, maejima, hirayama, yamamoto a motor cortex stim. 3: i8 0...

Journal of Neurology, Neurosurgery, and Psychiatry 1988;51:50-59

Corticospinal direct response in humans: identificationof the motor cortex during intracranial surgery undergeneral anaesthesiaYOICHI KATAYAMA, TAKASHI TSUBOKAWA, SADAHIRO MAEJIMA,TERUYASU HIRAYAMA, TAKAMITSU YAMAMOTO

From the Department ofNeurological Surgery, Nihon University School ofMedicine, Tokyo, Japan

SUMMARY The corticospinal direct (D) response to stimulation of the motor cortex exposed forintracranial surgery was recorded in 20 cases from wire electrodes inserted into the spinal epiduralspace. The D response was obtained from stimulation of restricted areas of the cerebral cortex, thatis, the hand, trunk and thigh areas of the motor cortex. The D response was resistant to anaesthesiaand unaffected by muscle relaxants. Thus, recordings of the D response are useful for identifying thelocation of the motor cortex during intracranial surgery under general anaesthesia.

In experimental animals, it has repeatedly beendemonstrated that a corticospinal direct (D) responseto stimulation of the motor cortex can be recordedfrom the lateral column of the spinal cord or the spi-nal epidural space.' The corticospinal D responseis recorded only when the motor cortex is stimu-lated.'`4 Furthermore, unlike muscle responses tomotor cortex stimulation, the corticospinal Dresponse is resistant to surgical doses ofanaesthetics' and is unaffected by muscle relax-ants. Thus, recordings of the corticospinal D responseduring intracranial surgery in humans would be ofvalue for identifying the location of the motor cortexand thereby reducing neurological complicationsresulting from unnecessary damage to the motor cor-tex. It has recently been reported that the corti-cospinal D response can be recorded in humans5 -7 totranscranial stimulation of the brain through theintact scalp.8- 16 We summarise here our experiencewith recordings of the corticospinal D response tostimulation of the exposed motor cortex in humansduring intracranial surgery.

Methods

The data analysed were obtained from 20 patients whoshowed no motor deficits before surgery. Recordings of the

Address for reprint requests: Yoichi Katayama, M.D., Ph.D.,Department of Neurological Surgery, Nihon University School ofMedicine, 30 Oyaguchi-Kamimachi, Itabashi-ku, Tokyo 173, Japan.

Received 31 March 1987 and in revised form 5 June 1987.Accepted 26 August 1987

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corticospinal D response were performed in these patientsfor the purpose of identifying the motor cortex and protec-ting it from possible surgical damage. All patients gaveinformed consent for intraoperative recording of the corti-cospinal D response. A pair of flexible, platinum wire elec-trodes insulated except at their tip (Medtronic Co. M-8483;fig 1) were inserted into the epidural space of the cervicaland/or upper thoracic vertebrae before surgery. The subjectswere placed in the lateral position and 18-gauge Touhyneedles were inserted into the epidural space at the upperthoracic level. Each electrode was inserted with a styletthrough the Touhy needles and advanced to the appropriateposition under X-ray control. The Touhy needles were thenremoved and the electrodes fixed with adhesive tape on theskin. The response was recorded monopolarly from the elec-trodes, with the reference electrodes placed at the para-vertebral muscles, in response to stimulation of the motorcortex exposed during surgery. The scalp of the foreheadwas grounded.

During intracranial surgery, the motor cortex and othercortical areas were directly stimulated with multicontactplate electrodes (Medtronic Co. M-3586). The location ofthe motor cortex, however, could not be precisely defined byany methods other than recordings of the corticospinal Dresponse under general anaesthesia. Thus, in the presentstudy, attention was focused on whether the D response waselicited from stimulation of clearly restricted areas of thecortex, as is the D response in experimental animals; whethersuch areas roughly corresponded to the location of themotor cortex estimated from bone landmarks by means of amethod usually employed for intracranial surgery; andwhether surgical damage to an area from which the Dresponse was obtained caused motor deficits. The four elec-trodes were 5 mm in diameter and spaced 5 mm apart. Theseelectrodes were designated 0, 1, 2 and 3, respectively, begin-ning arbitrarily from one end to the other. The response was

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Corticospinal direct response in humans

Fig I Radiographs showing electrode leads placed within the epidural space of the cervical spinal cord.

evoked by monopolar stimulation using one of these elec-trodes or bipolar stimulation with various pairs of elec-trodes. Thus, the interpolar distance for bipolar stimulationvaried from 10 to 30mm. Stimuli were applied as monopha-sic square wave pulses of 0 2-05 ms duration delivered at4 Hz. Delivery of the stimuli was triggered by electro-cardiograms. Signals from the electrodes were fed into an

amplifier with a bandpass range of 5 Hz to 5 kHz and aver-

aged for 32-128 sweeps with a signal processor. Electro-encephalograms were always monitored during recording ofthe responses, and were repeatedly recorded after thesurgery.

Results

A response having a large negative wave (Ni) pre-ceded by a small positive wave (P1) (fig 2a)was invariably recorded from the spinal epiduralspace to stimulation of restricted areas of the cortex,which roughly corresponded to the location of themotor cortex estimated from bone landmarks (seebelow). Neither convulsive seizures nor epileptic dis-charges were induced on the electroencephalogramsby the stimulation of the motor cortex. The response

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Interval (ms)Fig 2 (a) Representative examples of responses recordedfrom the spinal epidural space (C2 and C5 levels) to stimulationof the exposed motor cortex. An upward deflection corresponds to negativity. Arrows indicate the Ni wave. Note that theamplitude of the P1-NJ response decreases and the duration increases as the recording site is moved caudally. Tworecording sites are also plotted with the stimulation-recording distance on the abscissa and the latency on the ordinate. (b)Effects of double pulse stimulation with various interstimulus intervals (200-667 Hz) on responses recordedfrom the spinalepidural space (C2 level) to stimulation of the motor cortex. Arrows indicate the NJ wave in response to test stimulation.CS, conditioning stimulation; TS, test stimulation. Changes in percent values for the amplitude as compared with theresponse to single pulse stimulation (an average of records from 4 cases) are also shown in relation to interstimulus interval.Changes within 10% cannot be evaluated with precision because ofsuperimposed baseline changes. Calibrations: 2ms IOuV.


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Table Peak latency and conduction velocity ofthe NJ response

Peak latency (ms)*

Patient rostral rec. site caudal rec. site Distance (mm) between 2 rec. sites Conduction velocity (mls)1 2-83 3-39 28 502 2-90 3 41 35 693 2-31 2-62 21 684 3-53 4-10 33 575 3-09 3-61 39 75

*Values to the NI response at maximum stimulation intensity.

was recorded regardless of whether the recording elec-trodes were placed dorsally or dorsolaterally to thespinal cord. These two waves could not be separatedfrom each other on the basis of threshold and refrac-tory period. As the recording site was moved cau-dally, the latency of the P1-Ni response increasedand the amplitude decreased (fig 2a). The responsealso became gradually dispersed at lower levels(fig 2a). The difference in peak latency of the N I waveover the known distance between two recording siteswas used to calculate the conduction velocity (fig 2a).The calculated conduction velocity was within therange 50 to 75 m/s (table)-. The P1-NI response fol-lowed double pulse stimulation with interstimulusintervals of more than 500 Hz (fig 2b). Slight facili-tation (5-15%) of the P1-NI response to submaximalstimulation (approximately 50% maximal response)occurred with an antecedent conditioning stimulationwith interstimulus intervals ranging from 100 to500 Hz (fig 2b).The lowest intensity for evoking the P1-NI

response was as low as 2 mA, if the stimulation elec-trodes were appropriately placed on the motor cortex(see below). As the stimulation intensity was raised,the amplitude increased and then became saturated atcertain levels of intensity (fig 3a and 3b). It was alsofound that, as the stimulation intensity was raised, thelatency decreased and then became constant with thestimulation intensity over certain levels (fig 3a and3b). With an interpolar distance of 30mm for bipolarstimulation, the maximal decrease in latency was0-28 ms (fig 3b). The conduction velocity calculatedfrom the latency differences between two recordingsites, however, revealed no change.

For delineating the extent of stimulation sites fromwhich the P1-NI response was obtained, monopolarstimulation naturally provided better spatial resolu-tion. The threshold of the P1-NI response to mono-polar stimulation with anodal currents was generallylower than that with cathodal currents. However, theresponse to monopolar stimulation during intra-cranial surgery was often unstable in amplitude andthreshold during the course of surgery and was some-times associated with uncontrollable artifacts, pre-sumably due to large changes in impedance of current

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Fig 3 (a) Representative examples of responses recordedfrom the spinal epidural space to stimulation of the exposedmotor cortex with various stimulation intensities (5-25 mA).Arrows indicate the Ni wave. Note the changes in amplitudeand latency. N2, N3 and N4 waves are also seen with a highstimulation intensity (10-25 mA). (b) Changes in amplitudeand latency are shown in relation to stimulation intensity.Interpolar distance of stimulation electrodes: 20mm.Calibrations: 2ms; IO1V.

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Fig 4 (a) Representative examples of responses recordedfrom the spinal epidural space to stimulation of the exposed

motor cortex with various interpolar distances of the stimulation electrodes (10-30mm). The arrow indicates the Nl wave.

Note the progressive increase in amplitude with a longer interpolar distance. Stimulation intensity: 5 pv. (b) Changes in

amplitude are shown in relation to interpolar distances of the stimulation electrodes. Calibrations: 2ms; JO1 V.

pathways induced by various surgical procedures.We, therefore, attempted to record the P1-NIresponse with bipolar stimulation as well. It was

difficult to obtain clear responses with interpolar dis-tances of less than 10mm for stimulation. In contrast,a longer interpolar distance of more than 10mm

clearly produced the P1-NI response (fig 4A). At thesame level of stimulation intensity, the longer inter-polar distance produced a larger P1-NI response.

When both poles were placed on the motor cortex, theamplitude remained approximately the same afterreversing the polarity of stimulation (fig 4b) and stim-ulation artifacts could be removed with a signal aver-

aging technique by applying anodal currents alter-nately to one and then the other pole of thestimulation electrodes (fig 5). Such a technique, how-ever, was rarely necessary when the patients were

appropriately grounded. When only one pole of thestimulation electrodes was placed on the motor cor-

tex, the amplitude was slightly larger with the anoderather than the cathode applied to the motor cortex.With an interpolar distance of 10mm, the P1-NI

response was obtained only from stimulation ofrestricted areas of the cortex even employing a highstimulation intensity (fig 6). The focus giving theresponse with an interpolar distance of 10mm

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Fig 5 Representative examples of records containing largestimulation artifacts. Since both poles of the stimulationelectrodes were placed appropriately on the motor cortex,

the amplitude of the recorded responses remainsapproximately the same after reversing the polarity forstimulation. In such a case, stimulation artifacts can beremoved by applying anodal currents alternately using a

signal averaging technique.

roughly corresponded to the motor cortex withinareas 0-8 cm lateral to the midline, that is, the hand,trunk and thigh areas, as estimated from bone land-marks (fig 6). Stimulation of the medial motor cortexwas not examined. When the hand area was stimu-lated with an interpolar distance of 1O mm, the P1-N

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response was recorded only from the cervical level.Even with an interpolar distance of 30 mm, theP1-NI response was recorded only when at least onepole was placed precisely on or very close to themotor strip defined with interpolar distance of 10mmfor stimulation (fig 6). In three patients in whomsurgical damage was caused to the areas delineated inthis way, apparent motor deficits resulted aftersurgery. In contrast, remaining patients in whom sur-gical damage to these areas was avoided did not showapparent motor deficits.The P1-NI response was recorded independently

of the depth of anaesthesia, and was relativelyresistant to the physical condition of the motor cor-tex. Several negative waves (N2, N3 and N4) weresometimes seen with a high stimulation intensity fol-lowing the initial P1-NI response (fig 3a), but theselater responses were vulnerable to changes in thephysical condition of the cortex and the depth ofanaesthesia. The later responses were dependent alsoon the modality of stimulation.

In three cases, the corticospinal responses to stimu-lation with electrodes placed in the cranial epiduralspace overlying the motor cortex were recorded aftersurgery without anaesthesia and muscle relaxants. Insuch recordings, the initial P1-N1 response followedby several negative waves and large muscle responsesoriginating from the reference electrode placed in theparavertebral muscles were observed (fig 7). Pro-gressive administration of thiopental (50-250 mg, IV)clearly attenuated the later waves (N2, N3 and N4),as well as the muscle responses (fig 7a and b). In con-trast, the initial Pl-N1 response showed only slightdepression in amplitude (fig 7a and b). In noinstances did we encounter unfavourable side effectssuch as convulsive seizures or epileptic discharges onthe electroencephalograms.

Discussion

Since the initial P1 and Nl waves recorded in thepresent study could not be separated from each otheron the basis of threshold and refractory period, thesetwo waves are considered more likely to represent asingle synchronous impulse approaching and arrivingat the recording site, respectively. The large and syn-chronous shape of the response suggested that theP1-NI response is a volley mediated by a simple fibretract without intervening synapses. Several lines ofevidence supported such an interpretation. First, itwas demonstrated that the P1-N I response is capableof following double pulse stimulation with inter-stimulus intervals of more than 500 Hz. Second, onlyslight facilitatory effects of double pulse stimulationwere observed (see below). Finally the P1-NIresponse, in contrast to the later N2, N3 and N4


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Fig 6 Focus of stimulation giving responses in the spinal epidural space. (a) Stimulation with an interpolar distance of30mm. A pair of solid dots indicates a stimulation site giving responses. A pair of open circles indicates stimulation sitesgiving no response. (b) Small circles indicate foci giving responses even with an interpolar distance of 10mm for stimulationLarge circles indicate foci giving responses with an interpolar distance of20mm or more for stimulation. Areas encircledwith dots indicate the extent of craniotomy. cent = central sulcus; prc = precentral sulcus; syl = Sylvian sulcus. Scale:lOmm.

responses, was found to be clearly resistant to surgicaldoses of anaesthetics. These observations are all con-

sistent with the interpretation that the P1-N1response is not a synaptically mediated potential.The P1-NI response is limited to stimulation of

restricted areas which roughly correspond to thelocation of the motor cortex estimated from bonelandmarks. Furthermore, apparent motor deficits are

seen only when surgical damage is caused to theseareas. These findings indicate that a fibre tract medi-ating this response originates in the motor cortex. Nofibre tract other than the corticospinal tract is knownto have such a direct projection from the motor cortexto the spinal cord. There are many similaritiesbetween the P1-N1 response recorded in the presentstudy and the corticospinal D response reported forexperimental animals.'`4 The conduction velocity of

the P1-NI response, 50-75m/s, is similar to thatobtained for the corticospinal D response-or cortico-spinal neurons of the cat and monkey.'-4 17-20Because of the dispersion of the response at lowerlevels of the spinal cord, the conduction velocity esti-mated in the present study from peak latency must belittle lower than the maximal conduction velocity esti-mated from the onset latency of the response. How-ever, this difference appears to be minimal at the cer-vical level as compared with possible variabilities dueto unavoidable inaccuracies in roentgenographicmeasurements of conduction distance. This range ofconduction velocity is consistent with the conductionvelocity for fast corticospinal neurons.2' 23 The N2,N3 and N4 responses seen following the P1-N Iresponse in the present study resemble the indirect (I)responses reported for experimental animals.' 4 The

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Fig 7 Representative responses recorded from the spinal epidural space to stinmulation with electrodes placed in the cranialepidural space overlving the motor cortex without anaesthesia and muscle relaxants. The arrow indicates the Ni wave.

Thiopental w1as progressively administered (50-250mg, IV.). Note that large muscle responses are also recorded from thereference electrodc placed in the paravertebral muscles following the NI wave and several negative (N2, N3 and N4) waves.

In contrast to the N2, N3 and N4 waves and muscle responses, the NI wave is clearly, resistant to thiopental. Calibrations:2 ms; 10OpV.

present results thus directly demonstrate that a

corticospinal response equivalent to the D response

described originally by Patton and Amassian' forexperimental animals can be recorded in humans as

well. It has recently been reported that the cortico-spinal D response can be recorded in humans5`7 totranscranial stimulation of the motor cortex throughthe intact scalp.8 16 The data presented here are in

agreement with the observation in these previous

studies,` especially that reported by Boyd et al,7regarding the morphology, conduction velocity andother physiological features of the response.

The corticospinal D response has been consideredto result from activation of the cell bodies and/oraxons of corticospinal neurons rather than apicaldendrite arborising in the superficial layer.1 4 Thepresent study has demonstrated, in agreement withearlier studies on experimental animals,1 4 that slightfacilitation of the corticospinal D response can occur

with an antecedent conditioning stimulation. Theoccurrence of facilitation suggests that the cortico-spinal D response results at least in part fromexcitation of the cell bodies or initial segments ofcorticospinal neurons. However, it does appear that

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the corticospinal D response results largely fromdirect excitation of cortical or subcortical axons ofcorticospinal neurons, especially when higher levels ofstimulation intensity are used. The present resultsshowed that, as the stimulation intensity was raised,the latency of the corticospinal D response decreased.Since the conduction velocity calculated from thedifference in latency between two recording sites didnot change, the decrease in latency may have been dueto spread of the stimulation currents to more distalparts of axons (see fig 3b). Similar observation hasbeen reported in humans with transcranial brainstimulation.7The finding that the corticospinal D response in

humans is limited to the motor cortex provides ameans of identifying the motor cortex during intra-cranial surgery under general anaesthesia. The tradi-tional concept of the motor cortex has been developedon the basis of studies which employed stimulation ofthe cortical surface to evoke muscle movements.24 -26It has been shown by Asanuma et al26 in experi-mental animals that intracortical microstimulationcan permit more discrete mapping than that obtainedwith surface stimulation.23 26 However, mapping ofthe motor cortex with evoked muscle movements isnot easy under general anaesthesia with the use ofmuscle relaxants. In contrast, the corticospinal Dresponse is resistant to the usual doses of anaestheticsand is unaffected by muscle relaxants. This is clearlyone advantage of identifying the motor cortex fromthe corticospinal D response under generalanaesthesia. While corticospinal neurons as detectedby retrograde axonal transport of horseradish peroxi-dase are also seen in other areas of the cortex in themonkey, the most dense labelling with horseradishperoxidase occurs in the motor cortex27 and fastcorticospinal neurons are substantially restricted tothe motor cortex. The corticospinal D responserecorded from the spinal epidural space may be attri-butable to synchronous activation of such densecorticospinal projections originating in the motorcortex.

In order to identify the location of the motor cortexwith the D response, monopolar stimulation withanodal current is apparently preferable. A large num-ber of investigations in experimental animals haveindicated that anodal current, rather than cathodalcurrent, more easily activates deeply located initialsegments or axons of corticospinal neurons fromwhich the D response initiates.4 However, monopolarstimulation during intracranial surgery appears to beassociated with considerable changes in impedance ofcurrent pathways related to various surgical pro-cedures, which result in unstable recordings andsometimes uncontrollable artifacts. In contrast,bipolar stimulation provides constant responses with-

out large artifacts. It is very difficult to obtain clearresponses with bipolar stimulation with interpolardistance of less than 10mm in humans. Similar obser-vation has been made in experimental animals. It hasbeen argued that bipolar stimulation with such ashort interpolar distance produces a current whichspreads tangentially, and preferentially activatessuperficially located neural elements.4 In contrast,responses obtained with bioplar stimulation withinterpolar distance of more than 1Omm may be con-sidered to be the sum of responses to monopolar stim-ulation with anodal and cathodal currents.4 Further-more, the present study did show that the focus givingthe corticospinal D response with an interpolardistance of 10mm for stimulation is restricted to thehand, trunk and thigh areas of the motor cortex (seefig 6b).2425 Even with an interpolar distance of30mm for stimulation, the corticospinal D response isrecorded only when at least one pole is placed pre-cisely on or very close to these areas. Thus, an inter-polar distance of 10-30mm for stimulation appearsto provide practically useful information concerningthe location of the motor cortex.The motor cortex may be displaced in cases with

intracranial space-taking lesions. The functioningmotor cortex may be displaced also in cases witharteriovenous malformations which involve themotor cortex. Use of this technique during intra-cranial surgery should, therefore, help to reduce neu-rological complications resulting from unnecessarydamage to the motor cortex in such cases.

References

I Patton HD, Amassian VE. Single- and multiple-unit analysis ofcortical stage of pyramidal tract activation. J Neurophysiol1 954;17:345-63.

2 Levy WJ, McCaffrey M, York D, Tanzer F. Motor evoked poten-tials from transcranial stimulations of the motor cortex in cats.Neurosurgery 1984;15:214-27.

3 Katayama Y, Tsubokawa T, Sugitani M, Maejima S,Hirayama T. Assessment of spinal cord injury withmultimodality evoked spinal cord potentials. Part 1.Localization of lesions in experimental spinal cord injury.Neuro-Orthopedics 1986;1:1 30-41.

4 Amassian VE, Stewart M, Quirk GJ, Rosenthal JL. Physiologicalbasis of motor effects of transient stimulus to cerebral cortex.Neurosurgery 1987;20:74-93.

5 Levy WJ, York DH, McCaffrey M, Tanzer F. Motor evokedpotentials from transcranial stimulation of the motor cortex inhumans. Neurosurgery 1984;15:287-302.

6 Tsubokawa T, Yamamoto T, Hirayama T, Maejima S,Katayama Y. Clinical application of corticospinal evokedpotentials as a monitor of pyramidal function. Nihon UnivJ Med 1986;28:27-37.

7 Boyd S, Rothwell JC, Cowan JMA, et al. A method of mon-itoring function in corticospinal pathways during scoliosissurgery with a note on motor conduction velocities. J NeurolNeurosurg Psychiatry 1986;49:251-7.

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Corticospinal direct response in humans8 Marsden CD, Merton PA, Morton HB. Maximal twitches from

stimulation of the motor cortex in man. Proc Physiol Soc1980;312:5.

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23 Humphrey DR. Corticospinal systems and their control by pre-motor cortex, basal ganglia, and cerebellum. In: RosenbergRN, Willis WD, eds. Clinical Neurosciences Vol 5: Neuro-biology. New York: Churchill Livingstone 1983:547-87.

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