J Physiol Volume 510, Number 1, 261-267, July 1, 1998
The Journal of Physiology (1998), 510.1, pp. 261-267
© Copyright 1998 The Physiological Society
Central projection of proprioceptive information from the wrist joint via a forearm 'muscle' nerve in the cat
P. D. Mackie and M. J. Rowe
School of Physiology & Pharmacology, The University of New South Wales, Sydney 2052, Australia
Received 20 November 1997; accepted after revision 23 March 1998.
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ABSTRACT |
- Peripheral nerves arising in joint capsules are known to contain a 'contaminating' contribution from muscle afferent fibres. In the present report we provide the first electrophysiological evidence that some joint afferent fibres may take an 'ectopic' path to the central nervous system via a nearby muscle nerve.
- Experiments were conducted in anaesthetized cats in which a distal extension of the indicis proprius nerve was observed to project beyond its own muscle to the dorsal surface of the wrist joint capsule which is also supplied by the 'classic' wrist joint nerve, a branch of the dorsal interosseous nerve. Both the proximal and distal segments of the indicis proprius nerve were exposed for recording, by means of silver hook electrodes, while each segment remained in continuity.
- Individual wrist joint afferent fibres with receptive fields on the dorsal surface of the joint capsule could be identified electrophysiologically within the distal segment of the indicis proprius nerve. In each of these cases the same fibre could also be identified at the proximal recording site. The identity of each of these simultaneously recorded units was established (1) by the short fixed interval between their times of spike occurrence, (2) from the exact correspondence of the capsular receptive field for the simultaneously recorded spikes, and (3) by the unfailing correlation in the presence, or absence, of the distally and proximally recorded spikes in association with either manual or controlled stimulation of the wrist joint capsule. Most joint afferent fibres identified with this projection path were in the group II range of conduction velocities and had conventional properties but group III fibres also appeared to be represented.
- The present demonstration that some joint afferent fibres may be located within 'muscle' nerves emphasizes the importance of activating deep inputs, of joint or muscle origin, by adequate stimulation of the peripheral receptors in order to examine selectively the central actions of either source of input. Electrical stimulation of the peripheral nerves may lead to interpretative ambiguities.
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INTRODUCTION |
Contributions to kinaesthetic sensation arise from deep receptors in muscles and joints, and also from cutaneous sources (McCloskey, 1978; Edin & Abbs, 1991). However, the electrophysiological analysis of their separate contributions to kinaesthetic processing may prove ambiguous, in particular for the deep inputs since joint nerves may be contaminated by afferent fibres of muscle origin. One example of this is found with the posterior articular nerve (PAN) which supplies the posterior region of the knee joint. Burgess & Clark (1969) were the first to describe afferent fibres in the PAN which were sensitive to succinyl choline, strongly suggesting that these were associated with muscle spindle endings, and later work by McIntyre, Proske & Tracey (1978) confirmed that the group I population in the nerve was principally associated with the primary spindle endings of the popliteus muscle. There is also evidence that popliteus group II fibres, from secondary spindle endings, and group I fibres from tendon organ receptors are also represented in the PAN (Gregory, McIntyre & Proske, 1989). Of the approximately 250 myelinated nerve fibres that make up the PAN, 
10 % are group I fibres (Heppelmann, Heuss & Schmidt, 1988). The experimental consequences of this contamination of the PAN by muscle afferent fibres are, first, that electrical stimulation of the 'joint' nerve will activate a mixed muscle and joint input to the central nervous system and, second, that stimulation of the popliteus muscle nerve will activate only part of that muscle's afferent input to the central nervous system.
Although there have been some anatomical descriptions of muscle nerve branches which continue through the muscle to supply a joint in both the cat (Gardner, 1944; Skoglund, 1956; Freeman & Wyke, 1967) and the human (Wrete, 1949), there has been no electrophysiological confirmation that joint afferent fibres may traverse an afferent path via 'muscle' nerves. In the present report we provide electrophysiological evidence that some group II joint afferent fibres supplying the dorsal surface of the wrist joint capsule take an 'ectopic' path via a nearby muscle nerve, rather than the recognized route (Tracey, 1979) through the wrist joint extension of the dorsal interosseus branch of the deep radial nerve (Fig. 1A).
The anatomical substrate of this alternative projection path consisted of a distal extension of the indicis proprius muscle (IPr) nerve beyond its own muscle to the dorsal surface of the wrist joint capsule (Fig. 1A). This projection was observed in separate recording studies, from the IPr nerve (Mackie & Rowe 1997), in which we were examining the central actions of identified, single proprioceptive afferents using the paired simultaneous recording procedure employed previously in our laboratory for analysing central actions of single tactile afferents (Ferrington, Rowe & Tarvin, 1986, 1987a,b; Vickery, Gynther & Rowe, 1994; Gynther, Vickery & Rowe, 1995).
A preliminary report of this additional peripheral path for wrist joint afferent fibres was presented in conference proceedings (Mackie & Rowe, 1996).
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METHODS |
Adult cats, 2-3·5 kg, were anaesthetized initially with Saffan (24 mg kg-1 I.M.; Pitman-Moore, Australia Ltd) and maintained with supplementary I.V. doses as needed to maintain surgical anaesthesia. Atropine sulphate was administered subcutaneously to minimize respiratory secretions (0·05-0·1 mg kg-1). The femoral artery and vein were cannulated, and a tracheal cannula inserted. Blood pressure and heart rate were monitored continuously, and pupillary aperture and responsiveness, together with withdrawal reflexes, were frequently examined to ensure that deep levels of anaesthesia were maintained throughout the course of experiments. Rectal temperature was maintained at 37-38·5°C. All the experimental work conformed with the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes. Animals were killed at the end of experiments by an I.V. administered anaesthetic overdose.
The IPr muscle and its associated nerve were exposed in the left forearm by removing the extensor digitorum communis, extensor digitorum lateralis and extensor carpi ulnaris muscles. When the distal extension of the IPr nerve was present (see Results), the dorsal surface of the wrist joint was exposed, along with the 'classic' wrist joint nerve in its proximal projection as the dorsal interosseous nerve which joins the deep radial nerve near the elbow (Fig. 1A). Skin flaps were attached to a long, oval-shaped brass ring to create a paraffin-filled pool, held at 34-36°C, to protect the exposed wrist joint, the IPr muscle, and the associated nerves (Fig. 1A). The extensor pollicis longus muscle, which runs alongside the IPr, was cut at the tendon and separated from the IPr. The tendon of the IPr was also sectioned at the wrist, but the muscle attachments along the ulna bone were left intact. A segment of the IPr nerve 2 cm long was then carefully isolated from the more proximal portion of its associated muscle, but left in continuity with the parent deep radial nerve. A plastic film was inserted under this dissected nerve segment to improve electrical isolation, from the muscle and other tissue, and a silver hook recording electrode (RP in Fig. 1A) was placed beneath the nerve approximately halfway along the dissected proximal segment. A second recording electrode (RD in Fig. 1A) was placed beneath a distal extension of the IPr nerve that was observed in almost half of the cats used in the present series of studies.
Signals recorded between the RP or RD recording electrodes and an indifferent electrode fixed in nearby subcutaneous tissue were fed to separate differential amplifiers (1000 × gain) and filter units. They were displayed on an oscilloscope, passed to an audio amplifier and speaker, and were stored on separate channels of a modified 6-channel videocassette recorder (Vetter, model 400). The two channels of spike signals were also stored in a computer after sampling with an analog-to-digital converter (National Instruments) at 20 µs intervals. Spike occurrence times were stored in the computer for the two recording sites enabling construction of latency histograms (Fig. 2C).
Individual afferent fibres from the wrist joint were identified initially at the distal recording site, RD, and activated first by gentle mechanical stimulation of the joint capsule with fine glass probes or von Frey hairs (0·35-2 g). Once the receptive field location of a joint mechanoreceptor was established, a feedback-controlled mechanical stimulator (Ferrington et al. 1987a,b; Mackie, Zhang, Schmidt & Rowe, 1995) could be used to apply controlled stimuli (steady displacement or trains of sinusoidal vibration) to the focus of maximum sensitivity.
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RESULTS |
The deep radial nerve divides in the forearm below the elbow into a number of small branches, one of which becomes the dorsal interosseous nerve which supplies the interosseous membrane and a more distal extension, the 'classic' wrist joint nerve, supplying the dorsal surface of the wrist joint (Tracey, 1979). Other small branches of the deep radial nerve extend into individual forearm muscles, including the IPr. The branch of deep radial that supplies the IPr muscle and the branch, known as the dorsal interosseus nerve, that supplies the wrist joint capsule are very fine in calibre (< 0·5 mm) and, in both cases, can be freed over considerable lengths (2-5 cm) from nearby tissue while remaining in continuity with the central nervous system. Because of these attributes it is possible, with a simple hook electrode, to record from both these nerves in continuity and to monitor the responses of any large diameter fibre (group I or II) that is active in the nerve (Mackie et al. 1995; Coleman, Zhang, Mackie & Rowe, 1995; Mackie & Rowe, 1997). This conclusion is based upon the observation that there was a clear discontinuity between the noise level on the recording trace and the height of the spike activity associated with any active group I or II fibre. Furthermore, in most cases, the signal-to-noise ratio attained in these recordings exceeds 10 : 1 and ensures that no active fibre in the group I-II range can remain undetected in the recording from the intact nerve. In the course of our recent studies referred to in the Introduction, on the central actions of the proprioceptive afferents (Mackie & Rowe, 1997), we observed that 21/47 (45 %) of cats displayed a clear distal extension of the IPr nerve to supply the dorsal region of the wrist joint capsule (Fig. 1A). We cannot be certain whether this extension exists in other cases in a less obvious form, for example, in more intimate association with the IPr tendon. Where the distal extension of the nerve was identified it proved just as suitable as the proximal IPr nerve division for recording, with an excellent signal-to-noise ratio, from individual afferent fibres in the intact nerve (Figs 1B-D, 2 and 3).
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Figure 1. Paired, simultaneous recording from wrist joint afferent fibres within both distal (RD) and proximal (RP) segments of the IPr nerve
A, schematic representation of recording arrangement and of the dual paths over which wrist joint information may project to the central nervous system. Simultaneous recordings were made from the two electrodes, RD (distal) and RP (proximal), which were placed under the intact segments of the IPr nerve of the left forelimb. The separate 'classic' wrist joint nerve is also shown. B-D, three different wrist joint afferent units were activated by manual stimulation of their receptive fields with a fine (1 mm diameter) glass probe (B and C) or 2 g von Frey hair (D). Response traces on the left in B, C and D were 100 ms in length. In these, and in traces in subsequent figures, the upper trace in each pair is the recording from the proximal electrode (RP), the lower trace from the distal electrode (RD). To the right of each pair the six superimposed, expanded spike waveform pairs illustrate the consistency of individual spike waveforms and their time relations, and allow measurement of conduction velocities, based on the time delay between spike peaks and RP and RD electrode separation distances. Voltage calibration bar between C and D for impulse traces is 0·25 mV for B, 0·18 mV for C and 0·5 mV for D.
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When recordings were made in this way with a silver hook electrode from the distal extension of the IPr nerve, individual fibres were found that could be activated by means of gentle mechanical stimulation of the wrist joint capsule with fine glass probes or von Frey hairs. Their receptive fields were punctate, in agreement with previous descriptions for joint afferent fibres that innervate either the wrist joint or knee joint (Clark, 1975; Dorn, Schaible & Schmidt, 1991; Mackie et al. 1995; Coleman et al. 1995). In order to confirm that wrist joint afferent fibres recorded at RD in Fig. 1A, from the distal extension of the IPr nerve, completed their central path via the proximal IPr nerve (rather than looping back in a less distinct path to the 'classic' wrist joint nerve), we carried out simultaneous recording from the main IPr nerve at site RP in Fig. 1A. In each case in which a wrist joint afferent fibre could be recorded at RD, the same fibre could also be identified at the RP recording site (Figs 1B-D, 2 and 3).
The criteria that established the identity of wrist joint afferent units recorded at the RD and RP sites in Fig. 1A were, first, that the RP recorded spike followed RD, at a short, fixed latency. This is evident, in particular, in the expanded impulse trace pairs in Fig. 1B -D and in the latency histogram of Fig. 2C which was constructed from the impulse activity recorded at RP (Fig. 1A) when the RD spike served as a timing marker corresponding to time zero in the histogram. The latency histogram is effectively a cross-correlogram (Vickery et al. 1994; Gynther et al. 1995) and reveals the precise time delay between the occurrence of the RD and RP recorded spikes. The second argument for the identity of the unit recorded at the two sites was the exact correspondence of the receptive fields on the wrist joint capsule for the RD and RP recorded spikes and their identical thresholds for activation. Third, there was an unfailing correlation in the presence or absence of the RD and RP spikes as repeated manual or controlled stimuli were delivered to the wrist joint (Figs 1B-D, 2 and 3). This perfect correlation between the recorded spikes at the two locations may be seen (1) in response to repeated, irregular manual stimulation of the joint capsule by means of a fine (1 mm diameter) glass probe in Fig. 1B and C , (2) in response to stimulation with a 2 g von Frey hair in Fig. 1D, and (3) in Figs 2 and 3, in the responses to amplitude-modulated vibratory stimulation, applied by means of a 250 µm diameter stimulus probe attached to the feedback-controlled mechanical stimulator. It should also be emphasized that the spike responses in Figs 1B-D, 2 and 3 which were simultaneously recorded at RD and RP, were generated only from the wrist joint receptive field and were never elicited by stimulation of the IPr muscle itself.
The conduction velocities for the joint afferent fibres whose responses are illustrated in Figs 1B-D and 2 were calculated from the time delay between the occurrence of the RD and RP spike peaks and the measured distances between the RD and RP recording sites in the two segments of the IPr nerve. This method of calculation eliminated any delay for 'initiation time' at the receptor and gave conduction velocity values for six of the group II units identified in the range 30-60 m s-1 (Figs 1B-D and 2), consistent with values reported previously for group II joint afferent fibres (Tracey, 1979; Dorn et al. 1991; Mackie et al. 1995) and values of < 30 m s-1 for two units, which may place them within the group III fibre category (Tracey, 1979). The conduction velocity distribution for all eight wrist joint afferents studied in the IPr nerve extension is shown in Fig. 2D. One of the possible group III units was identified in sampled traces in which the group II unit of Fig. 2 was studied. Evidence of the presence of this group III unit at both RP and RD sites is shown in Fig. 3 (larger linking dots between RP and RD traces in A and B), in association with further recordings of the group II unit (smaller linking dots in A and B), activated by 50 and 80 Hz vibration stimuli applied (A and B, respectively) to the group II fibre's receptive field. C and D in Fig. 3 show, respectively, superimposed expanded waveforms of the wrist joint group II and group III spikes. No attempt was made to identify the receptive field of the group III fibre; however, joint afferent fibres of this class are generally associated with free nerve endings, and may serve a nociceptive function (e.g. Grigg, Schaible & Schmidt, 1986).
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Figure 2. Paired, simultaneous recording from a wrist joint afferent, in both distal and proximal IPr segments, in response to controlled stimulation of the joint capsule
A and B, response segments recorded at RP and RD, respectively, to a 500 ms train of vibration (100 Hz) applied to the receptive field of a wrist joint afferent fibre at two amplitudes (40 µm in A and 20 µm in B). C, latency histogram constructed from impulse counts of the unit recorded at RP in response to the 100 Hz stimulus of the form shown in A and B (> 500 paired spike events counted). D, conduction velocity distribution for all eight wrist joint afferent fibres studied. Six units were within the group II range, two possibly in the group III range. Voltage calibration bar between A and B is 0·5 mV for all traces.
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In Fig. 3A and B, an additional, predominantly negative-going spike is present in the RP (upper), but not in the RD recording traces. The receptive field of this spontaneously active fibre was localized to a spot within the IPr muscle only, and could be activated by very gentle manual probing with the glass probe, and therefore was almost certainly associated with a proximally projecting muscle spindle ending.
Each of the group II joint afferent fibres recorded from the IPr nerve appeared to be purely dynamically sensitive when tested with the hand-held glass probe or with von Frey hairs, and none of the fibres studied could be activated with controlled static displacements applied to the receptive field focus by means of a feedback-controlled mechanical stimulator. Although none was able to respond in a maintained way to static displacement, it was possible to elicit a maintained discharge if a continuous form of dynamic mechanical disturbance such as trains of vibration was applied (Figs 2A and B and 3A and B). As shown in Fig. 3A and B, vibration could be applied at different frequencies and intensities in order to vary between a sub-threshold and suprathreshold level for continuous activation of the joint afferent fibre responsible for the group II RD and RP recorded spikes. A perfect correlation was observed for the absence of both Rd and Rp spikes at subthreshold levels, and for the presence of both spikes at vibration levels that exceeded threshold. In this circumstance the unit responded repetitively with impulses on successive cycles of the vibration, that is, a 1:1 pattern of response (for example, in response to the first five cycles of vibration in Fig. 3B).
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Figure 3. Paired simultaneous recording at RP and RD sites of IPr from group II and probable group III wrist joint afferent fibres
The group II unit (large spike linked by small dots in paired traces) responded weakly to the 50 Hz (30 µm) vibration in A, but in a 1: 1 manner to the 80 Hz, 50 µm vibration in B. The group III unit's paired spike activity (indicated by the large dots) was unaffected by the stimulus and occurred at a low spontaneous rate. C and D, six superimposed expanded spike waveform pairs (as in Fig. 1) for the large fibre spike (C) and the small spike (D), including conduction velocity measurements, which place the fibre of the large spike (C) in the group II range and that of the small spike (D) in the probable group III range. The spontaneously active, predominantly down-going large spike present in only the upper trace (RP site in A and B) was associated with a proximally projecting IPr muscle afferent fibre and hence was not detectable at the RD site. Voltage calibration bar near D is 0·25 mV for lower (RD) trace in D, and 0·5 mV for all other impulse traces in A-D.
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DISCUSSION |
The present observations, made in the course of investigations on the central actions of identified proprioceptive afferent fibres of joint or muscle origin (Mackie et al. 1995, 1996; Mackie & Rowe, 1997), have revealed an 'ectopic' projection, through a forearm 'muscle' nerve, of joint afferent fibres that arise from the dorsal surface of the wrist joint capsule. Although the presence of muscle afferent fibres within 'joint' nerves has been well recognized, for example, for the posterior articular nerve (McIntyre et al. 1978; Gregory et al. 1989), the 'contamination' of muscle nerves with nearby joint afferents has not previously been verified electrophysiologically. However, the present observations demonstrate that both group II and III afferent fibres originating in the wrist joint capsule may project centrally via a 'muscle' nerve, the indicis proprius. This discovery therefore emphasizes the importance of activating deep inputs of joint or muscle origin by means of appropriate adequate stimulation of the peripheral receptors in order to examine selectively the central actions and processing of either source of input. Electrical stimulation of the nerve to the IPr muscle would activate, at least in the 45 % of cases in which the nerve extends beyond the muscle to the wrist joint capsule, a mixed muscle and joint afferent input to the central nervous system and would preclude unambiguous identification of central projection targets and processing mechanisms that were specific to muscle inputs. The observations therefore establish that the same interpretative ambiguity may be associated with the consequences of electrical stimulation of some muscle nerves as has applied for joint nerves such as the PAN of the knee joint, in which 10 % of the myelinated fibres are of muscle rather than joint origin. We do not have any estimates of the extent of this 'contamination' of the IPr nerve by joint afferent fibres. However, in view of the fine calibre of this nerve it may not require large numbers of joint afferents to constitute a substantial contribution to the input. The IPr muscle itself is small and, based on reports of other functionally related forearm extensor muscles in the cat (Oshima 1938, cited in Hosokawa, 1961; Cooper, 1966), and given its size, is likely to contain fewer than ten spindles and have no more than 100 myelinated fibres in the associated nerve (Mackie & Rowe, 1997). Whether any of the IPr muscle afferent fibres take an indirect, 'ectopic' path to the spinal cord via the wrist joint nerve is another possibility that should be considered in view of the anatomical arrangement we have described.
The group II wrist joint afferent fibres that were shown to take the alternative path via the indicis proprius nerve had functional characteristics that were entirely consistent with those of group II joint afferent fibres studied in recognized joint nerves such as the wrist joint nerve itself (Tracey, 1979) and the medial articular nerve that supplies the medial surface of the knee joint (Clark, 1975; Dorn et al. 1991; Mackie et al. 1995). These common characteristics include punctate receptive field foci on the joint capsule, similar thresholds, adaptation characteristics and responsiveness to mechanical stimulation applied to the receptive fields on the joint capsule, and a range of typical group II conduction velocities. How the group II fibres of the present study were able to respond to joint angulation could not be determined, as the preparation for recording from individual units from the intact nerves in continuity precluded the imposition of these changes in joint angle. However, the distinct advantage of this form of recording from intact nerves in continuity, which is only possible from very fine calibre peripheral nerves that can be freed over some distance (Ferrington et al. 1986, 1987a,b; Vickery et al. 1994; Gynther et al. 1995; Mackie et al. 1995), is that it permitted the simultaneous monitoring of the activity of an individual fibre at the two locations, in the main IPr nerve and in its distal extension to the wrist joint. The conventional method of sectioning and teasing peripheral nerves for single fibre recording does not permit such simultaneous recording, and would therefore not permit identification of the presence of the one fibre in both segments of the nerve.
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REFERENCES |
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Acknowledgements
The authors acknowledge the technical assistance of C. Riordan, P. Farrell and T. Ingall. The work was supported by the National Health and Medical Research Council of Australia and the Australian Research Council.
Corresponding author
M. J. Rowe: School of Physiology & Pharmacology, University of New South Wales, Sydney, NSW 2052, Australia.
Email: M.Rowe{at}unsw.edu.au
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