propagated insertional activity: a model of positive sharp wave generation

ABSTRACT: In this study we utilized a dual monopolar needle recordingtechnique to assess propagated electromyographic insertional activity fromthe same single muscle fiber in order to characterize different categories ofinsertional activity. A total of six combinations of insertional activity wereidentified. Only two fundamental types of single muscle-fiber insertionaldischarge configurations were generated: biphasic initially-negative andmonophasic positive. The propagated waveforms corresponding to thesetwo insertional discharges were primarily triphasic initially-positive and, onlyrarely, monophasic positive. The monophasic positive insertional activitygenerated at the inserting electrode site is postulated to arise from a depo-larization zone adjacent to a needle-induced peri-electrode membranecrush. The monophasic positive discharge was utilized as a model forpositive sharp wave generation. It is postulated that the majority of positivesharp waves are initiated at the inserting electrode adjacent to a needle-induced zone of muscle membrane crush in contrast to the previous sup-position that positive sharp waves are blocked fibrillation potentials.

Muscle Nerve 34: 457–462, 2006

PROPAGATED INSERTIONAL ACTIVITY:A MODEL OF POSITIVE SHARPWAVE GENERATION

DANIEL DUMITRU, MD, PhD, and CARLOS T. J. MARTINEZ, DO

Department of Rehabilitation Medicine, University of Texas Health Science Center,7703 Floyd Curl Drive, San Antonio, Texas 78229-3900, USA

Accepted 30 May 2006

A complete understanding of positive sharp wave(PSW) generation continues to elude investigators.The most comprehensive appreciation of how thisclinically important waveform is generated supposesthat it is a blocked fibrillation potential.4–6 Specifi-cally, a fibrillation potential propagates toward therecording electrode and encounters a region of peri-electrode muscle membrane that has undergone aparticular type of distortion referred to as a “crushzone.” This peri-electrode region of crushed mem-brane is conceptualized to render transmembranesodium channels transiently nonfunctional, therebyproducing a so-called “crushed end effect” that re-sults in an extracellularly recorded waveform with aconfiguration reflective of the intracellular actionpotential (IAP). In innervated muscle, this configu-ration is a monophasic positive waveform, whereas in

denervated muscle it is a biphasic, initially-positivewaveform referred to as a PSW.4,5 Although thisparticular model is well founded in volume con-ductor theory and capable of explaining all thevarious waveform configurations detected in clin-ical neurophysiology, there remains a paucity ofexperimental evidence substantiating theoreticalPSW modeling.

Previous clinical and theoretical investigationshave documented a limited number of waveformconfigurations8,12 arising from needle insertional ac-tivity, with one detailed study defining two funda-mental waveforms (biphasic initially-negative andmonophasic positive) consistent with volume con-ductor theory.2 In this investigation a more quanti-tative assessment of needle-insertional configura-tion, propagation, and pattern distribution, utilizinga unique dual-channel recording montage, was em-ployed. These results were utilized to formulate arevised model of PSW production that is believed tobe more consistent with clinical observations. Addi-tionally, a patient with denervated muscle was exam-ined using the dual-channel montage documentinga PSW generated at, and propagating away from, theinserting electrode, consistent with the revised PSWmodel.

Abbreviations: IAP, intracellular action potential; PSW, positive sharp waveKey words: insertional activity; needle electromyography; positive sharpwave; single muscle fiber; volume conductionCorrespondence to: D. Dumitru; e-mail: [email protected]

© 2006 Wiley Periodicals, Inc.Published online 28 July 2006 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/mus.20615

Propagated Insertional Activity MUSCLE & NERVE October 2006 457

MATERIALS AND METHODS

Subjects. Ten healthy subjects (9 men and 1 wom-an; mean age, 35 years; range, 28–50 years), withouthistory or physical examination suggestive of periph-eral nerve disease, agreed to participate in this study.This investigation was approved by our institutionalreview board and subjects provided informed con-sent. In order to assure the absence of peripheralnerve disease, a peroneal and sural nerve conduc-tion study was performed in all subjects. Any personwith an abnormal history, physical examination, ornerve conduction study was precluded from partici-pating in the investigation.

Instrumentation. An electromyographic instrument(Synergy electromyograph; Viasys Healthcare, Mad-ison, Wisconsin) employing a two-channel montage(sweep, 10 ms/division; sensitivity, 100 �V/division;low-frequency filter, 20 Hz; high-frequency filter,10,000 Hz) was used to detect, electronically store,and analyze all electrical activity. Two disposablemonopolar needle electrodes (DMG 37; ViasysHealthcare, Old Woking, UK) were utilized to detectall of the insertional activity.

Recording Montage. The monopolar needles wereutilized simultaneously and were connected to eachof the two noninverting amplifiers of the electrodi-agnostic instrument. A common surface referencelocated over the tendons of the ipsilateral ankle wasconnected to each of the amplifiers’ inverting ports.A single surface ground electrode was utilized inclose proximity to the needle insertion site.

Needle Recording and Data Collection and Analysis.

The two monopolar needle electrodes were firmlypressed together by the principal investigator attheir hubs to maintain a relatively constant verticaland horizontal interelectrode relationship, therebysustaining an interelectrode separation approximat-ing 1 cm. This technique did not stabilize the nee-dle’s tips and permitted some degree of movement,which resulted in difficulty in exactly aligning the elec-trodes on identical needle fibers. Both needle elec-trodes were simultaneously inserted into each subject’sleft tibialis anterior muscle at a site approximating thedemarcation between this muscle’s proximal one-thirdand distal two-thirds. This muscle was chosen becauseof its relatively parallel muscle-fiber configuration,which was necessary to simultaneously align the twoneedle electrodes along the same muscle fiber.10

Following dual needle insertion into the muscle,the amplifiers were activated and the more proximalof the two needle electrodes was arbitrarily desig-

nated as the inserting/recording electrode, whilethe more distal monopolar needle served as thepurely passive recording electrode. The inserting/recording electrode was gently withdrawn no morethan 1 cm and then slowly inserted in very smallincrements so as to activate only a few muscle fibersduring needle insertion as directed by the electricalactivity noted on the corresponding amplifier trace(designated channel 1).2 The electrical activity de-tected by the second channel was carefully moni-tored for a time-locked electrical disturbance corre-sponding to activity detected on channel 1. Unlessthe inserting/recording electrode transiently acti-vated identical fibers within the recording territoryof the second channel’s electrode, no electrical ac-tivity was detected. Time-locked electrical activity wasrelatively easy to detect, but it was extremely difficultand tedious to exactly align the two electrodes onidentical single muscle fibers. Further, after severalwithdrawals and reinsertions, a 1-cm interelectrodeseparation could not be assured, thereby precludingaccurate muscle velocity measurements between thetwo insertion sites.

The electromyographic instrument permitted 20seconds of data to be stored electronically, whichafforded the investigators an opportunity to assesseach insertional run for time-locked activity. Eachsubject was investigated in this manner for approxi-mately 1 hour with as many time-locked insertionalruns saved to disk as permitted by the time allotted.

All insertional activity within a 100-ms time-framewas designated as an insertional run for the purposeof data analysis. No insertional activity extended forlonger than 100 ms. The electrical activity was as-sessed from the perspective of waveform configura-tion detected at the inserting/recording electrode(channel 1) and that time-locked, but temporallydelayed, electrical activity on the second channel.

Patient. The dual-recording technique just dis-cussed was performed in the tibialis anterior of asingle person with a known lesion producing axonalloss in the left lower limb. Specifically, the individualassessed was a 38-year-old man who had undergoneresection of a pelvic chondrosarcoma with partialbut significant loss of fibers contributing to the sci-atic nerve.

RESULTS

Needle Insertional Activity. Perfect alignment of thetwo electrodes was extremely difficult and multipleinsertions were usually required of the proximallylocated inserting/recording electrode. It was also

458 Propagated Insertional Activity MUSCLE & NERVE October 2006

necessary to withdraw both electrodes and reinsertthem into several adjacent muscle locations to col-lect recordings effectively from different muscle fi-bers. Although an interelectrode separation of 1 cmwas approximated, no attempt was made to maintainthis exact separation because determining muscleconduction velocities was not the aim of this study.As a result, the time difference between the majordepolarization spikes are provided only as a roughapproximation to support the supposition of actionpotential propagation for the corresponding wave-forms (Fig. 1).

A total of 436 traces were collected. Only twoconfigurations of needle insertional activity were ob-served at the inserting/recording electrode, utilizingthe previously described technique.2 Specifically, abiphasic initially-negative waveform and a monopha-sic primarily positive waveform were documented.These two waveforms are consistent with previously

recorded mechanically proven single muscle-fiberdischarges and conform quite well to volume con-ductor theory.2 It is to be noted that the theoreticallypredicted monophasic positive waveform recordedin this study displayed a small-amplitude terminalnegative phase. This is to be expected given therelatively high low-frequency filter of 20 Hz requiredto maintain baseline stability during careful needleinsertion. Lowering the high-pass filter from 20 Hzto 1 Hz during a single insertion verified the theo-retically predicted monophasic nature of the antici-pated single muscle-fiber discharge, but this low-frequency cut-off was simply not practical forefficient large-scale waveform collection because ofbaseline instability during needle insertion (Fig.1G).

Six unique patterns of insertional and relatedpropagated electrical activity were documented (Ta-ble 1). The most common type of needle-insertional

FIGURE 1. (A)–(F) Six patterns of insertional and related propagated electrical activity (see text for descriptions). (G) The same positiveinsertional waveform recorded with a low-frequency filter of 1 HZ (upper trace) and 20 HZ (lower trace). Note the creation of a terminalnegative phase (lower trace) secondary to utilization of an elevated low-frequency filter to promote baseline stability during needleinsertion. The number in parentheses between the upper (induced) and lower (propagated) traces represents the time (in milliseconds)between the major depolarization spikes of each related waveform.


activity consisted of a series of all positive waveformson channel 1 and time-locked but slightly delayedcorresponding triphasic (initially-positive) wave-forms on channel 2 (positive/triphasic; Fig. 1A).This pattern of insertional and corresponding prop-agated waveforms comprised 39.4% of the total doc-umented insertional runs (Table 1). The secondmost common discharge pattern was a series of in-sertional biphasic negative/positive spikes totaling36% of observed waveform pairs, again generating apropagated triphasic waveform as detected by thesecond channel (negative/triphasic; Fig. 1B; Table1). A rarer, third pattern of waveforms, comprising15.6% of total observations, was documented to be amixture of negative and positive insertional spikes,again leading to a recorded series of associatedtriphasic waveforms on the second channel (Fig. 1Cand Table 1). A series of initially-negative insertionalspikes generating a series of positively recorded

waveforms occurred in 4.4% of recorded potentialgroups (Fig. 1D and Table 1). An equally rare occur-rence (4.4%) of waveform runs was observedwhereby the inserting potentials were all positive aswere the recorded waveforms from channel 2 (Fig.1E and Table 1). Finally, a single discharge pair(0.2%) of a series of insertional negative spikesyielded a mix of triphasic and positive spikes on thesecond channel (Fig. 1F and Table 1).

Patient. The technique just described was also per-formed in our patient with a peripheral nerve lesion.Physical examination revealed significant atrophy ofall muscles in the left lower limb innervated by thesciatic nerve, with only trace movements in a fewmuscles. The dual-recording technique indeed veri-fied multiple positive sharp waves and fibrillationpotentials in the patient’s tibialis anterior muscle,with only a single motor unit. The presence of floridmembrane instability resulted in considerable diffi-culty in identifying related discharges. Fortunately asingle location in the muscle revealed a clearly identi-fiable PSW recorded at the inserting/recording elec-trode and a distinct time-locked fibrillation potential atthe second (channel 2) recording electrode (Fig. 2).The examination was limited secondary to patient dis-comfort unrelated to the needle assessment.

DISCUSSION

Although the current explanation of PSW genera-tion is well founded in volume conductor theory,experimental evidence substantiating this theoreti-

Table 1. Insertional activity categories.

CategoryNumber of

runsPercent of

total

Positive/triphasic 172 39.4Negative/triphasic 157 36.0Mixture/triphasic 68 15.6Negative/positive 19 4.4Positive/positive 19 4.4Negative/mixture 1 0.2

Positive: a grouping of positive waveforms only; negative: a grouping ofbiphasic initially-negative waveforms only; mixture: a grouping of insertionalpositive and biphasic initially-negative (Fig. 1C) as well as a grouping ofpropagated positive and triphasic (Fig. 1F) waveforms.

FIGURE 2. The upper five waveform traces show a PSW recorded at the inserting electrode. The lower set of five traces documents thecorresponding time-locked propagated fibrillation potential arising from the PSW generated at the inserting electrode.


cal framework would provide additional support andfurther insight into one of the most fundamental ofall neurophysiologic waveforms.4,5 We hypothesizedthat exploring single muscle-fiber discharges as in-duced by mechanical depolarization associated withneedle insertion in normal muscle would providevaluable insights into the underlying mechanism ofPSW generation. Specifically, a previous experimentdocumented two fundamental types of insertionalactivity: biphasic initially-positive and monophasicpositive waveforms.2 Volume conductor theory pro-vided an explanation for the production of bothwaveforms and it was anticipated that further assess-ment of the monophasic positive insertional wave-form would yield additional insights into the PSW.

Our findings substantiate previous findings thatneedle insertional activity arises in two fundamentalconfigurations.2 The biphasic waveform appears es-sentially identical to that of an end-plate spike. It iswell accepted that end-plate spikes displaying thebiphasic initially negative configuration do so be-cause the initiation of single muscle-fiber depolariza-tion is coincident with the needle electrode’s record-ing tip.1 In this investigation, we found that at least40% (Table 1) of insertional waveform groupingsconsist of biphasic initially-negative waveforms. Fur-ther, these same insertional waveforms were suprath-reshold single muscle-fiber discharges because theygenerated propagated triphasic waveforms recordedby a second electrode located more distally on thesame muscle fiber (Fig. 1). Hence, these biphasicinitially-negative insertional spikes are generated co-incident with the inserting electrode as it plowsthrough muscle tissue.

The aforementioned findings of insertional activ-ity as arising from suprathreshold membrane depo-larizations that subsequently propagate along themuscle fiber, although certainly anticipated, haveuntil now not been documented to our knowledge.An even more interesting finding, however, is theobservation of the slightly more common (approxi-mately 44%) monophasic positive insertional spikeform (Table 1). The findings in this study stronglysuggest that this waveform is also generated in closeproximity to the recording electrode’s tip, whichgenerates a suprathreshold propagated single mus-cle-fiber discharge because it also gives rise to asecondarily recorded triphasic waveform. The onlycurrently viable volume conductor explanation ofhow a monophasic positive discharge can arise frominnervated single muscle fibers coincident with theinitiating site of depolarization involves the peri-electrode crush membrane effect.4 One of theunique characteristics of the crush membrane effect

is that it reflects extracellularly the configuration ofthe intracellular action potential (IAP; �80 mV ris-ing to approximately �40 mV and repolarizing to�80 mV); that is, both the IAP and its associatedextracellularly recorded waveform in innervatedmuscle are monophasic positive. Therefore, this in-vestigation yielded the unanticipated finding of theinserting electrode having the ability to generate twotypes of waveforms in association with its insertingleading edge. If the electrode produces little mem-brane deformation a waveform is generated exactlycoincident with the advancing needle tip—that is, abiphasic initially-negative potential similar to an end-plate spike (Fig. 1B). However, if the membrane isdeformed so as to produce a region of peri-electrodecrush, an action potential is also generated circum-ferential to this crush zone surrounding the elec-trode, which then propagates along the fiber as asuprathreshold single muscle-fiber discharge (Fig.1A). To our knowledge, the suggestion that a regionof depolarization can be initiated adjacent to a crushzone and propagate away from the crush region,instead of terminating there, has not previously beenrecognized.

Previous explanations of PSW generation as-sumed that the PSW was related to a fibrillationpotential that started at some location other than theelectrode, and upon encountering the recordingelectrode failed to propagate past it; that is, therewas action potential blockade at the recording elec-trode.4 This explanation proposed that the particu-lar type of blockade was consistent with a crush zoneinduced by the recording electrode’s mass effect.3 Asnoted earlier, the crush zone thereby permitted anextracellularly located electrode to, in effect, recorda waveform reflective of the IAP, which in dener-vated muscle tissue is biphasic initially positive with along terminal negative phase identical in configura-tion and time course to that of a PSW.4,11 The find-ings in innervated tissue from this study demonstratethat the inserting electrode commonly generates aperi-electrode crush zone and simultaneously in-duces a peri-electrode suprathreshold depolariza-tion (Fig. 1A, C, and E). Thus, it is logical to hypoth-esize that an inserting electrode can induce the sameeffect in muscle tissue with an associated unstableresting membrane potential, such as denervatedmuscle.

Employing this investigation’s methodology in apatient with clinically documented denervated mus-cle revealed that, as predicted, an inserting electrodedid indeed induce a PSW that was associated with apropagated time-locked fibrillation potential (Fig.2). Hence, this work shows that a PSW originates, as


opposed to terminates, at the recording electrode—that is, an induced PSW rather than a blocked fibril-lation potential. Additionally, it is now clear thatPSWs and fibrillation potentials are one and thesame, as one manifests as the other (Fig. 2). Specif-ically, they both represent a single muscle-fiber dis-charge with different configurations simply depend-ing upon the manner in which the recordingelectrode interacts with the muscle membrane, andthey do not represent significantly different poten-tials with separate clinical implications.7 We suggestthat in those patients in whom PSWs are observedprior to, or exclusive of, fibrillation potentials, thefiber’s resting membrane potential is unstable (de-nervation in progress or a channelopathy) and hasnot yet achieved an ability to cycle spontaneously,but does repetitively fire in response to the elec-trode’s mechanical depolarizing effect during inser-tion.

If we then consider all of the insertional activitydocumented in innervated tissue from this study, wefind that the vast majority of monophasic positivespikes arise at the initiating electrode rather thanterminating at the recording electrode. Specifically,a total of 259 monophasic positive waveform runs,either in isolation or in combination with negativespikes, were detected at the initiating electrode,thereby comprising a total of 60% of waveformsconforming to a monophasic positive spike initiatedat the electrode (Table 1). This is in contradistinc-tion to only 9% (Table 1) of all waveform runsyielding a monophasic positive spike as detected atthe passive recording electrode—that is, a blockedsingle muscle-fiber discharge at an electrode-induced peri-electrode crushed zone. This clearlysubstantiates the supposition that a single muscle-fiber discharge can indeed block at the recordingelectrode consistent with a crush effect, but it iscertainly far less common than an actual inductioncoincident with the inserting electrode. Rather, it ismore likely that a propagating single muscle-fiberdischarge will travel past the recording electrode(triphasic waveform configuration) with little if anyeffect 91% of the time (Table 1). It appears that theact of inserting the electrode primarily induces atransient region of muscle membrane crush becausethe passive recording electrode (channel 2) docu-mented primarily triphasic waveforms. This impliesthat the muscle tissue, at least to some degree, can

accommodate over a relatively short time-frame tothe needle’s mass effect with a sufficient recoveryfrom the crush zone effect to permit action-potentialpropagation instead of blockade. A limited numberof fibers, however, continued to experience a crushregion because a small number of monophasic pos-itive waveforms were detected by the channel 2 elec-trode (Table 1). This accommodation may explainwhy PSWs transition to fibrillation potentials3,9 andwhy myotonic discharges change their configurationfrom a PSW to that of a fibrillation potential.

In conclusion, the data from this investigationsuggest that, although a PSW may indeed arise froma blocked fibrillation potential, it is much morelikely that the majority of detected PSWs are gener-ated as a result of depolarization adjacent to a peri-electrode crush zone during needle insertion. It isanticipated that this reconceptualization of PSW or-igin will lead to further insights into the mechanismunderlying PSW generation.

REFERENCES

1. Buchthal F, Rosenfalck P. Spontaneous electrical activity ofhuman muscle. Electroecephalogr Clin Neurophysiol 1966;20:321–336.

2. Dumitru D, King JC, Stegeman DF. Normal needle electro-myographic insertional activity morphology: a clinical andsimulation study. Muscle Nerve 1998;21:910–920.

3. Dumitru D, King JC, McCarter RJM. Single muscle fiber dis-charge transformations: fibrillation potential to positive sharpwave. Muscle Nerve 1998;21:1759–1768.

4. Dumitru D, King JC, Rogers WE, Stegeman DF. Positive sharpwave and fibrillation potential modeling. Muscle Nerve 1999;22:242–251.

5. Dumitru D. Configuration of normal and abnormal non-volitional single muscle fiber discharges. Clin Neurophysiol2000;111:1400–1410.

6. Dumitru D. Physiologic basis of potentials recorded in elec-tromyography. Muscle Nerve 2000;23:1667–1685.

7. Kraft G. Fibrillation potentials and positive sharp waves: arethey the same? Electroencephalogr Clin Neurophysiol 1991;81:163–166.

8. Kugelberg E. “Insertional activity” in electromyography.J Neurol Neurosurg Psychiatry 1949;129:268–273.

9. Nandedkar SD, Barkhaus PE, Stalberg EV. Some observationson fibrillations and positive sharp waves. Muscle Nerve 2000;23:888–894.

10. Platzer W. Pernkopf anatomy, 3rd ed. Vol. II. Munich: Urban& Schwarzenberg; 1989. 360 p.

11. Thesleff S. Spontaneous electrical activity in denervated ratskeletal muscle. In: Guttmann E, Hnik P, editors. The effectof use and disuse on neuromuscular functions. Prague:Czechoslovak Academy of Science; 1963. p 41–51.

12. Wiechers DO. Electromyographic insertional activity in nor-mal limb muscles. Arch Phys Med Rehabil 1979;60:359–363.


propagated insertional activity: a model of positive sharp wave generation

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