736 Journal ofNeurology, , and Psychiatry 1990;53:736-744 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from Microneurography in relation to intraneural topography: somatotopic organisation of median fascicles in humans

Rolf G Hallin

Abstract solid tungsten needle microelectrodes. This Microneurography was performed in technique records multiunit and single unit median nerve sensory fascicles with con- activity in myelinated fibres.9 Multiunit centric needle electrodes and with con- activity in C fibres innervating muscle'0 and ventional tungsten microneedles. The skin,"1 12 as well as single unit activity in both latter electrodes preferentially recorded afferent and sympathetic C fibres,"'35 can also activity from the myelinated fibres in be discerned. the whole fascicle. By contrast, due to its Hallin and Wiesenfeld introduced a stan- special design, a concentric needle can dardised, thin diameter concentric needle record activity selectively from even a electrode for percutaneous recording of A and small part of a fascicle. High amplitude C fibre units in humans.'6 In this investigation signals in C fibres can be discriminated the recording properties of the concentric close to Schwann cells that envelope needle electrode were compared with those of unmyelinated axons. Apart from being the tungsten needle. Further, individual biased for activity in thin fibres, the con- median nerve fascicles were screened for their centric needles can also record signals relative contents of myelinated and unmyelin- from nearby myelinated fibres. The pal- ated fibres and to obtain information about mar receptive fields of such fibre groups the cutaneous palmar distribution of these were not congruent with the areas fibres. Preliminary data'6 17 and our results traditionally attributed to multiunit skin indicate that the concentric electrode is biased afferents in humans, namely the towards recording C fibre activity. The data innervation zone(s) of one or two obtained also suggest the presence of a adjacent digital nerve(s). Instead, the hitherto not described somatotopic organisa- multiunit fields often comprised small tion in human sensory nerve fascicles. parts of a digital nerve innervation area, frequently only the pulp of a finger. Single units were always localised within Material and methods previously screened multiunit areas. Our findings were obtained from 67 Contrary to some previously accepted experiments performed on 15 healthy subjects tenets it is probable that single unit of both sexes aged between 20-42 years. They http://jnnp.bmj.com/ activity in myelinated fibres in these all gave their informed consent to participate studies is recorded extra-axonally near in the trials. In eight experimental sessions to a node of Ranvier. The findings also skin nerve activity was recorded from the suggest the presence of a somatotopy in median nerve at the wrist and in 49 sessions human limb nerve fascicles, comparable from the nerve just proximal to the elbow. For to that previously established in the comparison ten experiments with tungsten

and the somatosensory cor- electrodes were carried out under equivalent on September 24, 2021 by guest. Protected copyright. tex. conditions. A Recording electrodes By using surface electrodes, Eichler succeeded In most experiments concentric needle elec- in recording synchronous mass activity trodes were used.'6 They consisted of com- through the skin from a mixed nerve in situ.' mercially available hypodermic needles with The subsequent use of improved macroelec- outer shaft diameters of 200-250 gm and Department of trodes placed in the vicinity of a peripheral inner diameters of 90-100 pm (fig 1). A thin Clinical nerve,` later combined with averaging insulated tungsten wire, diameter 10-30 pm or , procedures, refined the technique of recording a thin platinum-iridium wire of diameter 20- Huddinge University Hospital, Huddinge, activity from intact limb in humans.45 30 gm was positioned inside the needle, which Sweden These procedures have been used for both was then filled with Araldite. The leads from R G Hallin experimental and clinical purposes.7 the central core and the shaft (ground lead) Correspondence to: Single unit activity in humans was first were thin copper wires. The impedance of R G Hallin, Department of Clinical Neurophysiology, recorded experimentally from excised and/or electrodes with small diameter recording Huddinge University exposed nerves in situ, an approach which wires (10 pm) was 500-700 kQ, and of those Hospital, S 141 86 Huddinge, Sweden. obviously is precluded from wide adoption in with the largest threads (30 pm) 200-300 kQ Received 21 February 1989 humans.8 Vallbo and Hagbarth described a at 1000 Hz.'8 Solid tungsten electrodes (bare and in final revised form percutaneous technique to explore human tip length 30-100 pm, impedance 50-75 kQ) 27 November 1989. Accepted 6 December 1989 limb nerves with intraneurally positioned were used in a few experiments.9l920 Microneurography in relation to intraneural topography: somatotopic organisation ofmedian nervefascicles in humans 737 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from

./ \ number of stimuli, such as application of skin b j a taps or pressure with various small objects. f The thresholds of individual units and boun- daries of the unitary receptive fields were examined by using von Frey's hairs. Afferent C fibre activity was also evoked by squeezing or applying pressure to the skin, needle pricks ,. .., in the receptive area or by applying warm or '! hot stimuli derived from a radiant heat source (Quartslampen GmbH, Original Hanaan, *..'. aX West Germany) or from a commercially ... .' available temperature stimulator (Somedic AB, Stockholm, Sweden) operating according to the Peltier principle.21 ,; 4 S P: D Electrical stimulation % Electrical stimulation (square wave pulses of

:. 01-1 ms duration) was performed using a X DISA stimulator unit (Type 14E D1). Sur- face or needle electrodes were used for skin Figure I Photomicrographs of a tungsten wire microelectrode and its tip region (A) and similar photographs of a concentric needle electrode, as described in the text, in stimulation. Intraneural electrical stimulation profile (B) and with its recording surface infull view (C). The sizes of the two types of was performed with the recording area of the electrodes are similar. The length of the tip of this tungsten electrode was 135 pm (side of electrode as cathode and the shaft of the cone formed by the tip 140 pm, base 67 pm) and the size of its conical recording area was estimated as 14 200 pm2. The recording surface of this concentric electrode was 20 x 50 needle as anode. pm as estimated in the microscope and its oval recording area amounted to 785 pum. (The measures of the recording area of the concentric electrode appear overemphasised due to E Nerve exploration procedure an unproportionally strong light reflex in the metal surface.) Magnification x 38. Bar 200 plm. The experiments were carried out as des- The flat oval recording areas of the concen- cribed previously.'6 19 To minimise the risks of tric electrodes were much smaller than the inducing nerve fibre damage the bevelled sur- conical recording surfaces of the tungsten face of the concentric needle was directed the skin in with needles. The recording area of the concentric through parallel and into the nerve to be explored. Weak electrical pulses electrode in fig 1C was calculated to 785 gm2. With a core diameter of 30 the maximal (1-6 V, 0 2 ms duration) intraneurally elicit- gm in recording areas of these electrodes were about ing paraesthesias the fascicle territory, were 2100 um2. The somewhat asymmetrical delivered through the electrode during the mantle area of the tungsten electrode shown search procedure to guide the electrode tip into the nerve. A number of criteria were for comparison in fig 1A was calculated to used to decide whether the electrode picked up about 14 200 gm'. If the tip of such a tungsten electrode had extended only 70 respectively activity from fascicles destined for skin or "' was to 100 pm, the base of the cone would have been muscle.9 Occasionally it tedious reach and a about 28 pm respectively 38 pm and the keep recording position but sometimes

the nerve http://jnnp.bmj.com/ recording areas would have been about 3100 activity had stable amplitudes allow- ing studies for up to several hours. pm' respectively 6000 pm2.20 PRECAUTIONS B Recording and display system The electrodes were sterilised in 350,° for- The recording electrodes were connected maline vapour at 80°C at a variable under- to commercially available preamplifiers pressure. The skin at the electrode site was (Neurolog System, Digitimer Ltd). For carefully cleaned with pure alcohol and then maximal recording safety the ground was with sterile injection swabs. The same record- on September 24, 2021 by guest. Protected copyright. close to the recording point/intraneural ing site was not explored again until 4-6 stimulating site. The safety measures taken weeks after an examination. With these corresponded to those of class I, group B. The measures no enduring neurological symptoms bandwidth of the whole system was generally were encountered in any of the subjects. 200 Hz-10 KHz (-40 dB/decade), but it could be modified when needed by applying other filter settings. An improvement to the Results signal-to-noise ratio was obtainable by an NERVE TOPOGRAPHY IN RELATION TO amplitude discriminator which could elimin- RECORDING SITES ate about 50% of the noise.'9 The noise of the Extrafascicular sites recording system peak-to-peak was about 10- The concentric electrode could be gently 15 pV. The best units had amplitudes of 40- pushed stepwise through the nerve without 60 ,V. During the experiments the signals causing too much discomfort to the subject.'9 were displayed on an oscilloscope, fed into a Electrical silence on a number of tests sugges- loudspeaker and were simultaneously stored ted that the recording surface often was on tape. located in extrafascicular sites. Judging from the frequency of occurrence of such situations C Mechanical and thermal stimuli a substantial portion of human peripheral The receptive field location and extent of low nerve is made up of non neural tissue ele- threshold mechanoreceptors was mapped by a ments.2223 738 Hallin J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from

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Figure 2 Anatomical distribution of receptivefields for RA (A) and SAI units (B). The circles and dots mark receptivefield locations, not actualfield sizes in thisfigure and infig 4. In thisfigure andfigs 4 and 6-7 all receptive fields are displayed on diagrams of the right hand.

Intrafascicular sites dominated by A fibre By contrast, tungsten electrodes may in a activity single site discriminate several units in the I Single unit activity median nerve, especially at the elbow. The When the needle was in a stable intrafas- RA and SAI units were most commonly iden- cicular site single unit activity in myelinated tified in recording sites where the correspond- fibres was regularly identified either directly ing multiunit receptive field(s) involved the or after repeated needle adjustments. The pulp and an adjacent small skin region at the occurrence of single unit activity in the recor- ding was sometimes preceded by the appearance of injury discharges. Injury activity often occurs before unit activity is reached with tungsten microelectrodes.919 The characteristics of stable single A fibre - 150 units agreed well with those previously des- (i3 ;" - 100 cribed in 26 Out of a microneurography.192 http://jnnp.bmj.com/ total of 82 units 42 RA (rapidly adapting) ;~~~~~~~~~~~~~I.__ units, 5 PC (Pacinian afferents), 27 SAI (slowly adapting type I) and 4 SAII (slowly adapting type II) units were reliably identified (figs 2, 3) on the basis of action potential distribution size of amplitude and shape, and A __; receptive fields, firing characteristics etc. Four I ~~~~~~~~~~ Hz could not be classified The on September 24, 2021 by guest. Protected copyright. units satisfactorily. I75 localisations of the units' receptive fields (fig 2) were essentially the same as previously 0 _ 50 reported when using tungsten microelectrodes .I.. .s*;. ;,. ,.,.:, for sampling24 with a high concentration of the _ RA and SAI units on the tip of the digits and a lower density in the rest of the hand. The ____ i sizes of their receptive fields were also as Figure 3 Discharge pattern and instantaneousfiring frequency ofa RA unit localised in glabrous skin of the previously reported. Furthermore, the extent thirdfinger tip (A) and a SAI t(nit with receptivefield and sensitivity of an individual unit's recep- in the pulp of the indexfinger (B). Time barfor A-B 1 s, tive area remained the same during an for impulses of respective unit to the right I ms. experiment and no tendency to "blocking" of A: The RA unit was phasic and responded with only one or afew spikes at the application and removal ofa even a part of a unitary receptive field was constant pressure of 0-6 g (bar) exerted with a von Frey seen.27 Representative recording sequences hair (left). Brisk strokings along the dermal ridges illustrating the firing characteristics of these (bars) induced briefbursts with an instantaneousfiring of 60-90 Hz (middle). In response to equally brisk strokings units are shown in fig 3. Various details in the across the dermal ridges the unitaryfiring rose to 150 Hz firing characteristics of single units were (right). sometimes possible to test over several hours. B: The illustrated SAI unitfired in a typical manner with an initial burst at the application of the stimulus and Generally only one (core diameter 10 4um) then slowly adapting in a graded manner depending upon or a few units (1-3) (core diameter 20-30 gm) the stimulus strength (4 1 g to the left, 9-2g to the right) were recorded at each site even at elbow level. as long as the pressure was maintained (bars). Microneurography in relation to intraneural topography: somatotopic organisation ofmedian nervefascicles in humans 739 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from

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Figure 4 Relationship between identified single unit receptive sites and corresponding multiunit receptivefields. RA and PC receptor sites are shown in A, SAI and SAII sites in B. The units were either identified when the multiunit area was initially mapped or encountered in the course of a few needle adjustments when abandoning the original recording site. The hatched areas display the established extent of the receptivefields for PC and SAII receptors and the black dot the point of maximal sensitivity of these receptors. A: The RA units (circles) were always localised within the previously established multiunitfield (grey area) irrespective offield size and complexity. The outcome offive different experiments are shown to the left. To the right above an example of a split multiunit receptivefield comprising a relatively large part of the pulp of the thumb (maximal extension of not visible area indicated by broken lines) and part of the indexfinger is shown. Below to the right is displayed thefield of one PC receptor. B: Seven SAI receptor sites (dots) and one SAII site (below right) obtainedfrom different experiments and their relation to the corresponding multiunit receptivefields are shown. Moderate skin tension in the directions indicated by the arrows enhanced thefiring of the SAII unit.

finger tip (see below). When sampling tactile recorded with the concentric needles often afferents in such a situation by repositioning had considerably lower amplitudes than such the electrode intraneurally, the units were activity recorded with tungsten needles (5C, always encountered within or sometimes on D). In some cases, however, and particularly the border of the receptive field for the when the activity was derived from pulp previously recorded multiunit activity (fig 4) afferents, well discriminated responses to both which was reduced in amplitude when a large local touch stimuli and maintained pressure amplitude single unit was discriminated. were discerned, especially in the integrated These findings were consistent irrespective of neurogram (fig 5A, B). http://jnnp.bmj.com/ recording site and irrespective of whether the The receptive field locations and distribution previously identified multiunit field was small, in the hand were as described earlier.'9 large or split (figs 4, 6, 7). Sometimes succes- However, the multiunit areas recorded with the sive units were of the same modality and had concentric needle electrodes were usually adjacent receptive fields. In one recording at smaller (50}70Oo less) than those normally the elbow four units, three RA units and one found with the tungsten needles (figs 4, 6).

SAI unit were found in a cluster in the pulp of When exploring the median nerve at the wrist on September 24, 2021 by guest. Protected copyright. the thumb (fig 4A, bottom row left). the receptive area generally included an elon- At the end of the experiments the electrode gated, slightly asymmetrical part of a finger tip was sometimes successively withdrawn from and a coherent small region on the phalanx next the recording site in the nerve. During this to the pulp. Sometimes the innervation area procedure previously identified units tended was more proximal and then involved glabrous to reappear in the neurogram in the reverse skin of the two proximal phalanges on the ulnar order to that in which they had been iden- or radial aspect of the finger (fig 6A). Similar tified. size multiunit receptive fields were found at the elbow level, although larger receptive areas II Multiunit activity were also found there, corresponding to the The multiunit activity evoked by weak innervation area of one or two or sometimes mechanical stimuli appeared as low amplitude, parts of two adjacent digital nerves (fig 6B). In mainly negative directional mass discharges. almost all experiments the position, extension The most intense activity was evoked by brief and complexity of the multiunit receptive fields repeated stimulation with, for example, rough of low threshold skin afferents changed slightly emery cloth or vibratory stimuli (fig 5A). when repositioning the electrode surface in the Responses occurred at the onset and offset of nerve fascicle in small steps. This finding was local pressure whereas often only relatively consistent irrespective of whether the record- sparse discharges were recorded during main- ing site was at the wrist or at the elbow level tained stimulation. The multiunit discharges (fig 7). 740 Hallin J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from

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Figure 5 Integrated neurograms (above) and multiunit responses (below) to repeated strokings of the skin with an emery cloth (left, bars) and to a continuously applied constant pressure with a metal springholder (right, bar). Time constant of integrater 500 ms. Time calibration Is. A, B: The afferent multiunit discharges were sometimes well discriminated. The phasic component of these responses appeared most distinctly. C, D: Different recording site than A-B. The multiunit receptive field was split and comprised the pulp region and the skin covering the ulnar part of the first phalanx of the thumb and the basal radial part of the indexfinger on the left hand. This recording was dominated by sympathetic activity. The afferent multiunit discharges to skin strokings and constant pressure in the thumb were discrete but sometimes the amplitudes of the responses were as high as that ofspontaneous outbursts ofsympathetic skin nerve activity (arrows).

Intrafascicular sites dominated by Cfibre activity 0 In many experiments the initial recording was that ofC fibre activity, generally as sympathetic multiunit discharges. This was less common

with tungsten than concentric needles, 1~ ~ ~ ~ ~ ~ -5 especially when exploring the median nerve.

The general occurrence of the sympathetic http://jnnp.bmj.com/ bursts during resting conditions and under a variety of manoeuvres, such as cooling or stressing the subject, fully agreed with previously described characteristics of cutan- eous sympathetic outflow in humans.2829 The sympathetic multiunit discharges often had higher amplitudes than concomitantly recor- ded A fibre multiunit activity (fig 5) and the on September 24, 2021 by guest. Protected copyright. corresponding receptive area for myelinated fibres on many occasions was positioned proximally in the fingers and palm. Slight needle adjustments occasionally dramatically improved the signal-to-noise-ratio in such a recording so that single unit activity in sym- pathetic fibres could be recorded. Afferent C fibre activity was recorded on several occasions, but was not, like sympathetic activity, encountered at every recording site. The activity was in many instances of a unitary character already when first identified and the signal-to-noise-ratio of the discharges could sometimes be improved on needle adjustment. In most recording sites about two or three C afferents were identified. Only exceptionally Figure 6 Typical examples of multiunit receptivefields was an afferent C unit recorded in isolation. of low threshold mechanoreceptive afferents (shaded areas) as encountered when exploring the median nerve Additional data on C fibre activity will be with concentric needle electrodes at the wrist (A) and at published separately.0 the elbow (B). Microneurography in relation to intraneural topography: somatotopic organisation of median nervefascicles in humans 741 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from

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1 2 3 1 2 3 Figure 7 Transition of localIsation and extent of multiunit receptivefields (shaded areas) in successive intraneural sites (1-3) when mapping the median nerve at the wrist (A-C) and at the elbow (D-F). Both at the wrist (three experiments) and at the elbow (three experiments) changes in the multiunit receptivefield were noted upon minute adjustments of the concentric recording needle (1-3) irrespective ofwhether the needle was advanced into (A, D, E) or withdrawn from the nerve (B, C, F). Discussion could not be verified.3' Possible hazards involved in the exploring Another unconsidered possibility to account procedures which might influence the for how unit activity can be recorded in these interpretation of the results studies would be that the unitary signals in the Electrodes inserted into human nerve fascicles case of myelinated fibres represent activity at might mechanically or otherwise interfere with the nodes ofRanvier. This does not exclude the and distort the intraneural environment so possibility that the tip of a tungsten electrode that neurophysiological events become mis- recording unit activity may occasionally be represented in the recorded activity. Wall and partially penetrating the axon."" As will be McMahon27 paid particular attention to this discussed, the present data would be easily problem and suggested that single unit record- accounted for ifthe proposed idea ofunit origin ings from human peripheral nerves only are is accepted. Furthermore, some major dis- possible because almost all of the nerve fibres crepancies between the present results and near the electrode tip are pressure blocked previous microneurographic data acquired during the exploring procedure and therefore with the tungsten electrode could then be unable to conduct action potentials. Only one explained. or a few fibres near the tip would stay active, Concentric electrodes with small recording making action potentials recordable as unitary surfaces seldom recorded single unit activity discharges.27 in myelinated fibres whereas electrodes with http://jnnp.bmj.com/ In a study utilising concentric needle elec- somewhat larger surfaces did so regularly, trodes with two recording surfaces we estab- sometimes from several units. These data fitted lished the probability of recording neural well with our experience that sampling ofunits activity at both surfaces at the same time.3' In with myelinated fibres tended to be more 80% of the experiments nerve signals were rewarding when using tungsten electrodes discerned at both recording areas simultan- (unpublished observations). Obviously, the big

eously. Furthermore, the properties of the three dimensional tip area of such an electrode on September 24, 2021 by guest. Protected copyright. identified units to a diversity of stimuli were will record from a larger number of nodes similar to characteristics ascribed to normal, of Ranvier than the concentric needles used previously established receptor types in sub- (fig 8). human species.3236 Therefore, gross functional The unitary characteristics, for example, abnormalities engaging the explored nerve fas- shape and duration of the recorded potentials cicle do not seem to be prevailing during and firing pattern to various stimuli were microneurographic investigations. virtually the same irrespective of recording technique. However, injury discharges were Electrophysiology related to intraneural more rare with the concentric needle and the topography. Impulse generatorsfor single and identified units (fig 3) in many cases showed no multiunit A and Cfibre activity overt signs of nerve fibre damage.'73' In this As pointed out in a critical review unitary context it should be recalled that previously discharges in microneurography are not likely identified but abandoned unit(s) tended to to be recorded intra-axonally.27 Furthermore, reappear in focus for the electrode when it was unit activity in myelinated fibres recorded with moved out of the nerve. The likelihood for the concentric needle can hardly originate from such events to occur would be much higher if an intra-axonally positioned electrode surface. the unit recordings originated near some On the other hand, the suggestion of a pressure anatomical structure(s) than ifrelocation of the block for most nerve fibres at the electrode site, recording surface intra-axonally in one or more thereby making unit identification possible, previously penetrated axons would be neces- 742 Hallin J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from likely at the internodes. Also, the shape of the unitary impulses were of the types to be expected when recording the electrical activity from a fibre very close to a node ofRanvier with the kind of electrodes used in this investigation (Frankenhaeuser, personal communication). Multiunit A (discussed under next heading) and C fibre signals probably represented extracellular activity recorded close to a num- ber offibres, but distant from a node. Since the intervals between the nodes may amount to several hundred microns,"445 which is long in relation to the length of the electrode surface, and the nodes are not always randomly dis- tributed within the fascicle (Hallin and Ekedahl, unpublished observations), the loca- tion ofthe active surface ofthe needle will often be at the internodes. Solely multiunit activity therefore should (and does) occur in the recor- dings quite frequently during microneuro- graphy. The receptive fields were smaller than those found using solid tungsten electrodes for nerve exploration'9 and the evoked multiunit mechanoreceptor activity from these fields was often of very low amplitudes. Reasons were given above to explain why the concentric needles used in this investigation often sampled fewer units in a recording site than tungsten needles. The same line of argument could explain why the multiunit mechanoreceptor activity often had lower amplitudes and regularly derived from smaller receptive fields when screened with the concentric needle than when the tungsten electrode was used for Figure 8 Schematic illustration of the proposed recording site when using the concentric needle (A) and similar nerve explorations (fig 8). the tungsten electrode (B) for microneurography. The Multiunit C activity was often better dis- small illustration in the middle indicates that a recording criminated than multiunit A fibre discharges electrode inserted in a nerve has entered into a fascicle. In A is shown how 10 fibres lie near to the recording surface with the present technique (fig 5). This finding (shaded area measuring about 30 x 85 pm) of the would also relate to the design ofthe concentric concentric electrode (hatched oval indicates the Araldite needle. Since it often records activity from only filled lumen of the needle). Sometimes a node of Ranvier may lie close to the recording area resulting in a unit a small part of the myelinated fibres of the recording. Many more fibres (20) lie close to the fascicle, multiunit discharges in A fibres were http://jnnp.bmj.com/ recording area of a tungsten electrode (length offree tip less prominent than they would have been if (shaded area) in this case 100 pm) in the same recording recorded a electrode in the same site (B). Apart from afew more fibres lying in front of by tungsten the needle, most of the additional fibres (indicated by site (fig 8). Thus simultaneously recorded C black ellipses to the right) are located "behind" the fibre activity tended to be favourably enhan- needle. (Their course behind the needle is not indicated.) ced, especially close to the electrode when Addititional nodes of Ranvier may get close to such a needle with its conical recording area resulting in exploring nerve fascicles with the concentric additional unit recordings. It is also apparent that the needle. concentric needle records multiunit activity preferentially on September 24, 2021 by guest. Protected copyright. from fibres close to and in front of its recording surface. Somatotopy in human median nervefascicles The tungsten electrode records multiunit activity from fibres abutting on any part of its bare conical tip and will A number of mapping experiments were per- therefore reflect the overall activity from a large part or formed to study intraneural fascicular topogra- the entirety of the explored fascicle. Bar 100jpm. phy with the more selective concentric needle. In many trials the multiunit fields of myelin- sary for unit recording. ated afferents comprised a part or the entire Thus it is suggested that unitary activity in pulp of a finger (figs 4, 6, 7). In about 30% of myelinated fibres sampled during micro- the cases the fields were split in at least two neurography is recorded extra-axonally near a distinct areas, suggesting simultaneous record- node of Ranvier. In the nodal-paranodal part of ings from more than one nerve fibre popula- the membrane the number of ion channels is tion. Following adjustments of the electrode maximal.'' Furthermore, the generation of position there were minor changes in the extent action currents is concentrated to the node."142 and localisation of the multiunit innervation At the node, high amplitude signals from a area (fig 7). There were also striking transitions thick fibre would therefore be expected, from fields composed by separate parts to fields provided that the two closely spaced electrode which were coherent and vice versa. The single surfaces of the concentric needle are close to the units, however, which were found in the course active site.4' Away from the nodal region the ofthe changes in recording site were all situated longitudinal current density outside the fibre is within the boundaries of the previously mall,41 42 maki;ngr s;r1jingl uit 1recordV- screened multiunit receptive fields (fig 4) and in ings from a myelinated fibre substantially less one experiment several single A fibre elements Microneurography in relation to intraneural topography: somatotopic organisation ofmedian nervefascicles in humans 743 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from (three RA and one SAI unit) with separate but Some clinical implications nearby receptive areas were successively iden- The fingers in primates have a dense mech- tified in a cluster in the pulp of the thumb. anoreceptive innervation.2435 The intrafas- These findings provide strong evidence for cicular grouping of the myelinated fibres sup- the presence of intrafascicularly localised plying palmar skin must also have bearing on microbundles of myelinated fibres in human tactile gnosis in humans. Thus the relatively nerves. Some microbundles seem to be des- common early complaint of finger tip numb- tined to the finger pulp, others to more prox- ness occurring in patients with carpal tunnel imal parts on the side of a finger. Furthermore, syndrome might be accounted for as a compres- cutaneous median nerve fascicles at the elbow sion involving microbundles destined to the level, which typically contain fibres supplying finger tips. Ifneighbouring median nerve fibres the innervation areas of two adjacent digital destined to the whole hand and the finger pulps nerves, probably contain at least four (fig 7), were randomly distributed in each individual probably more, bundles of myelinated fibres fascicle as suggested in another study2" the which innervate adjacent sides and pulp distal numbness occurring in the carpal tunnel regions of two neighbouring fingers. syndrome would be much less likely to develop In contrast to our results, Schady et al found especially if the massive central representation that the myelinated fibres in human peripheral of the fingers is considered. Clinically, reality nerve fascicles are randomly distributed points in the opposite direction. intrafascicularly.2" The issue then is whether or Our results may also be of relevance for not the interpretation of our data can also corrective micro-surgery aiming to re-establish account for the discrepancies in the results innervation after nerve trauma. It is well between the two studies. Due to its design, the known that the manual discriminatory capacity concentric electrode is quite useful in analysing restored after peripheral nerve suture to a the neural activity from small groups of fibres substantial part depends on the extent of the close to the recording surface (fig 8A). Since the nerve injury. Patients with partial nerve lesions tungsten microelectrode discriminates activity generally regain a functionally more complete in many more fibres around its entire conical tactile gnosis than those with total severance of tip (fig 8B) it is simply not possible by the nerve48 which is easily understood in the physiological recordings to study microanat- light of the present findings. omy reliably in small portions ofthe fascicle by Judging from the number of recording sites using this technique. Hence, the now dis- where sympathetic activity occurred, sympath- covered fascicular organisation was not detec- etic fibres are quite numerous in the median ted in previous microneurographic recordings nerve."' This is not surprising as the unmyelin- with tungsten electrodes.'9 Neither micro- ated fibres far outnumber myelinated fibres in stimulation through the intrafascicularly inser- human nerves,49 5" but quite the contrary to the ted tungsten electrode,39 used by Schady et al experience with the tungsten microelectrode to study intrafascicular fibre organisation in which records preferentially from the myelin- detail,20 seems accurate enough in the present ated fibre population of the whole fascicle.'924 context. In the trials described it was assumed The fact that sympathetic fibres are numerous that individual nodes of Ranvier within small in the median nerve might be one necessary

groups of fibres close to the electrode tip were prerequisite for the occurrence of pain syn- http://jnnp.bmj.com/ stimulated. However, since the recording/ dromes involving the median nerve area.5' stimulating tungsten electrode sometimes had a free tip extending as much as 180 gim,20 which I am grateful to Professor Bernhard Franken- presumably was totally enclosed intrafas- haeuser for valuable discussion of the manu- cicularly, and there was no way to judge the script. The expert secretarial aid of Maj-Len distribution of the stimulating currents used, Holm and Eli Froyen-Stenberg is gratefully the nodes of Ranvier of the stimulated fibres acknowledged. This research was supported by near such a big tip might well have been spread funds at the Karolinska Institute and The on September 24, 2021 by guest. Protected copyright. out within a comparatively large intrafascicular Swedish Society of Medicine. volume. Intraneural stimulation of several dis- persed nodes of Ranvier near the whole free tip would evoke randomly scattered projected 1 Eichler W. tCber die Ableitung der Aktionspotentiale vom fields, indicative of unit activation, within a menschlichen Nerven in situ. Z Biol 1937;98:182-214. large cutaneous area within the explored fas- 2 Dawson GD, Scott JW. The recording of nerve action potentials through skin in man. J Neurol Neurosurg cicular territory, thus accounting for the repor- Psychiatry 1949;12:259-67. ted results.20 However, in view of the present 3 Dawson GD. The relative excitability and conduction velocity of sensory and motor nerve fibres in man. J data it is apparent that the microstimulation Physiol 1956;131:436-51. technique is not sufficiently precise to use as a 4 Buchthal F, Rosenfalck A. Evoked action potentials and conduction velocity in human sensory nerves. Brain Res tool for studying the intrafascicular fibre 1966;3:1-122. organisation in 5 Gilliat RW, Mellville JD, Velate AS, Willison RG. A study detail."' of normal nerve action potentials using an averaging Thus we conclude that an orderly technique (Barrier grid storage tube). J Neurol Neurosurg microsomatotopy is present in human median Psychiatry 1965;28:191-200. 6 McLeod JG. Digital nerve conduction in the carpal tunnel nerve fascicles. The results adhere to a com- syndrome after mechanical stimulation of the finger. J mon principle of a somatotopical organisation Neurol Neurosurg Psychiatry 1966;29:12-22. 7 Sears TA. Action potentials evoked in digital nerves by in the somatosensory system which starts in the stimulation of mechanoreceptors in the human finger. J peripheral nerves and relays via the spinal Physiol 1959;148:30-31. 8 Hensel H, Boman KKA. Afferent impulses in cutaneous cord' to end in a well organised manner at sensory nerves in human subjects. J Neurophysiol more central levels.47 1960;23:564-78. 744 Hallin J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.9.736 on 1 September 1990. Downloaded from

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