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Deep innervation of sural nerve
Brain Research. 279 (1983) 262-265 Elsevier
262
Deep innervation of sural nerve S. C. CHANG, J. Y. WEI* and C. P. MAO**
Shanghai Institute of Physiology, Academia Sinica, 320 Yo-Yang Road, Shanghai (People's Republic of China) (Accepted July 26th, 1983)
Key words: deep innervation - - sural nerve - - pain - - nociceptor
Discharges of 37 sural afferents in the Aa to C fiber range have been recorded during stimulation of subcutaneous tissues after removal of the skin. Except for one Aa unit with muscle spindle properties, fibers were not easily excited by muscle stretching. The more slowly conducting fibers tended to have higher thresholds. After repeated stimulation, most A6 and C units displayed a persistent afterdischarge which lasted from several minutes to more than half an hour. It is well known that the sural nerve innervates skin covering the ankle and foot. However, Stiiwell 7 demonstrated morphologically in the cat that small fasciculi of the sural nerve supply small (up to 2 u m ) and large (5-7 g m ) fibers to the superficial surface of the Achilles tendon. Small fibers o u t n u m b e r e d large ones by about 4 to 1, and both formed free endings. This suggests that some sural sensory fibers innervate deep structures. The aim of the present work was to see whether electrophysiological methods would give evidence of deep receptors supplied by surat nerve. A preliminary report has a p p e a r e d in Chinese 2. Experiments were carried out on 15 adult cats (2-3 kg), under pentobarbital anesthesia (40 mg/kg, i.p.). Supplementary doses were regularly given to maintain deep anesthesia. A small segment of sural nerve trunk was isolated from its surrounding tissue in the distal part of the popliteal fossa and put on a pair of stimulating electrodes. The single unit afferent discharges were recorded with a bipolar recording electrode (30 g m diameter, platinum wire) from nerve filaments dissected from a more proximal part of the nerve. The distance between stimulating and recording electrodes was 3-4 cm. The detailed description of this method was given in another paperl~. The skin around the lower leg and ankle joint was
separated completely from the deep tissue, so that no afferent discharges could be recorded from sural nerve when wiping or squeezing the zone of sural innervation. The natural stimuli used to search for deep receptors supplied by the sural nerve were needling with an acupuncture needle, pressing with a glass rod or spring b a r o m e t e r , pinching the Achilles tendon and nearby deep tissues, and stretching the triceps surae muscles. A f t e r a unit's receptive field was carefully localized with natural stimuli, the deep tissue was cut away under magnification ( 2 5 - 4 0 x ) , layer by layer, until no afferent discharges could be p r o d u c e d by reapplying the same stimuli to the receptive field. Sural nerve fibers that innervate deep tissue were isolated in each of the 15 successful experiments. Thirty-seven sural fibers activated from deep tissue were studied. Fig. 1 shows the distribution of the conduction velocities of 32 of these afferent fibers. The conduction velocities of the other 5 units were not measured accurately, but 3 of them could still be identified as C fibers. In accordance with Gasser's criterion 3, the 6 fibers having conduction velocities between 40 and 85 m/s will be called ' A a ' fibers, the 12 fibers conducting more slowly than 30 m/s but faster than 2.5 m/s will be called 'Ac~' and the 14 fibers conducting more slowly than 2.5 m/s will be called 'C"
* Address for correspondence: Department of Physiology, 410 Chipeta Way, Research Park, Salt Lake City, Utah 84108, U.S.A. *~ Present address: Shanghai Brain Research Institute, 319 Yo-Yang Road, Shanghai, China. 0006-8993/83/$03.00 © 1983 Elsevier Science Publishers B.V.
263 unit, Table I) showed that stretching the Achilles tendon with a force of 500-700 g could only excite 2 A 6 units to fire 1-2 impulses. The other 6 units did not respond at all. On the other hand, all 8 units could be stimulated by pressing their receptive fields. The maximum averaged frequency (averaged over 1 s) was usually in the range of 10-30 imp/s. There were two different response patterns. Twenty-six of the 35 units that were tested showed persistent discharge during pressing (Fig. 2A). These included 4 A a , 12 A6, and 10 C fibers. The other 9 units, 2 A a and 7 C units, responded only transiently to pressure changes (Fig. 2C). The thresholds of the units varied. We divided the manually applied pressure stimuli into 3 categories: heavy (more than 200 g), moderate (50-200 g) and light (less than 50 g). Only 3 C units could be activated by light pressure; the others required moderate to heavy pressure. A a and A6 units behaved differently. Most of them needed only light or moderate pressure for activation (Table I). The highest threshold measurement was for a C unit, about 500-700 g force; the lowest for an A6 unit at only 10 g. This difference is similar to our previous observations of the threshold range for pressure receptors of the tibialis anterior musclel0,11. After locating the most sensitive receptive point of 20 units with a glass rod, we inserted an acupuncture, needle into the point and manipulated it. Nineteen of the 20 units responded with either a persistent (Fig. 2B) or a burst of discharges. The maximum average firing rates for different units varied from 1 to 80 imp/s with 11 of the 19 units discharging between
I0
Az
A~
8
D=
2
0
0 0.5
1.5
I0
C~GTION
30
50
70
9O
VELOCffY (M/SEC)
Fig. 1. Distribution of conduction velocities of Aa, A6 and C fibers of sural nerve which innervated deep structures. fibers. The ratio between small (A6 + C) and large (Aa) fibers was about 4:1. This result is similar with the result from the morphological study by Stilwell 7. The main results of this experiment have been summarized in the Table. Spontaneous discharges. Eight out of 35 units displayed irregular spontaneous discharges (Table I). The discharge rates were 1--4 imp/s for C fibers and 5-14 imp/s for A6 fibers. There was one A a unit with a regular resting discharge of 24 imp/s. It responded to muscle stretch like a spindle afferent. Response to mechanical stimuli. Except for the one spindle-like receptor, these units were like the pressure receptors supplied by muscle nervesl,4,5,10. They could not easily be excited by muscle stretching but could be activated by pressing their receptive fields. The results of testing 8 units (excluding the spindle TABLE I Fiber type
Number of fibers
Spontaneous discharge
Aa A6 C
6 12 17
1 3 4
Total
35
8
After-
Mechanicalstimuli Needling
Pressing Threshold
Response pattern
Response pattern
More than 200g
Persistent
Bu~t
Per s&tent
Less than 50g
50200g
4* 5 3
1 6 8
1 1 6
4* 12 10
2 0 7
15
8
26
9
12
* The one spindle-like Ace unit fell into this group.
Response to muscle stretch
discharge
Bunt
No
Yes
No
0 7 5
2 2 3
1 0 0
1" 2 0
1 4 1
0 6 9
12
7
1
3
6
15
264
A o•
°Q
~o
o,
°°
.'.
:
• g
..
o*
m
.~:-.....~.~.~
-
= -'. i"
,.
o
. -,~. -4
m
C
| Fig. 2. Record of discharge frequency vs time. A shows the persistent discharge of an A6 unit when pressing on the receptive field (line under spike trace) and the after-discharge when pressure was released. The conduction velocity was 30 m/s. B shows the response to needling stimulation of a C unit with 0.52 m/s conduction velocity. J' indicates inserting a needle into the receptive field center; - - shows period of manipulating the needle; --- represents no manipulation but needle still in the point; ], shows withdrawal of the needle. The vertical position of each dot in A and B represents the number of spikes in 1 s. Calibration in B for both A and B, vertical bar = 5 spikes; horizontal bar = 28 s. C is a record of an Aa unit with conduction velocity 60 m/s, showing a bursting discharge in response to maintained pressure. The vertical position of each dot represents the number of spikes in 100 ms. Calibration: 4 spikes and 16s.
10-30 imp/s. Two A a units displayed a short burst of activity and most C and A d units displayed a persistent response (Table I). After-discharge. In 15 units, all A 6 or C, manual needling or r e p e a t e d pressing on the receptive field was followed by an after-discharge that was persistent, irregular and low in frequency and lasted for variable time periods (Fig. 2A, B). F o u r of these 15 units originally had spontaneous firing; after the stimulation the firing rate increased. For two units the after-discharge lasted more than half an hour. This p h e n o m e n o n is similar to our previous observation on the pressure receptors supplied by C fibers of the tibialis anterior muscle nerve II . The rates of af-
ter-discharge ranged from 2 imp/s to 24 imp/s, most being less than 10 imp/s. Receptive fields. The receptive fields of these receptors usually were not as easily located as those of cutaneous m e c h a n o r e c e p t o r s , especially if the receptive field was deep within the muscle or tendon. This is because the direction of the mechanical stimuli can influence the accuracy of the threshold m e a s u r e m e n t and localization of the receptive field. Fibers were found to innervate a variety of deep structures. The receptive fields of 17 units were located on or in the Achilles tendon and the musculotendinous junction, 6 around the distal part of lateral malleolus, 11 in the lateral gastrocnemius muscle, one in the medial gastrocnemius muscle, and the other 2 in the connective tissue around the sural nerve. The structure of the receptive fields differed somewhat. Eight units had small relatively well-defined receptive fields; five (3 A 6 , 2 C) were located on superficial connective tissue layers, one in the muscle, one in the tendon and the other at the musculotendinous junction. A n o t h e r 4 units showed band-like receptive fields. Of these, two A 6 units had 1 × 0.2 cm and 2.5 × 0.2 cm receptive fields, one A a had a 2.5 × 1.3 cm receptive field, the other A a unit terminated along a blood vessel and had 4 small, separate receptive fields. O n e of the C units had two separate sensitive spots; one on the connective tissue around the nerve trunk and the other on the superficial connective tissue near the nerve trunk. In relation to conduction velocity, 14 out of 37 total units, (3 A a , 5 A 6 , 4 C and the two units for which conduction velocity was not d e t e r m i n e d ) , were located deep within the tendon; 6 units (1 Act, 5 C) deep within the muscle; 3 units (2 A 6 , 1 C) were deeply located at the muscle-tendon conjunction; 12 units (2 Aa, 5 A 6 , 5 C) on the superficial layers of the connective tissue covering muscle, tendon and adjacent deep structures. The other 2 units were located on the connective tissue around the nerve. In summary, we have recorded the discharges of 37 sural afferents during stimulation of subcutaneous tissues after removal of the skin. Receptive fields were located in the Achilles tendon and adjacent deep tissues and in the gastrocnemius muscle. The conduction velocities of 32 units were m e a s u r e d ; 6 fell into the A a , 12 into the A 6 and 14 into the C fiber range. Except for one A a unit with muscle spindle
265 properties, the fibers were not easily excited by muscle stretching but could be activated by pressing on their receptive fields. There was a tendency for more slowly conducting fibers to have higher thresholds; most of the C and A 6 fibers required stimuli that were probably noxious. Four C units fired spontaneously (1-4 imp/s) and 3 A 6 had spontaneous activity (5-14 imp/s). After repeated stimulation, most A6 and C units displayed a persistent afterdischarge that was irregular and low in frequency and which lasted from several minutes to more than half an hour. This appears to be the first electrophysiological study demonstrating that fibers of a cutaneous nerve innervate deep tissue. We did not completely search a whole sural nerve trunk in a single experiment and so no estimate can be made of the percentage of deep fibers that travel in the sural nerve. However, together with the histological work of Stilwell 7 our study demonstrates that normally there are fibers in the sural nerve which supply deep structures and hence, strictly speaking, the sural is not a pure cutaneous nerve. Most of the deep fibers are small myelinated or C fibers with high thresholds suggesting a nociceptive function. A more general issue is whether other cutaneous
nerves also have this kind of deep innervation. Selective block of the superficial radial nerve at the wrist decreases but does not eliminate, deep pain elicited by squeezing or inserting a needle into the first dorsal interosseous muscle of the hand (unpublished observations). Thus, the superficial radial nerve (a cutaneous nerve) probably contains some fibers supplying deep tissues. Weddell et al. in 1941 pointed out that the peripheral nerve fields from adjacent nerves usually overlap 9. In addition, it may be that overlapping innervation in the third dimension (i.e. vertical overlapping directed from superficial to deep tissues) is also common, providing an additional safety factor for an animal when a deep nerve is damaged• The presence of deep fibers in cutaneous nerves may help to explain the reduction of low back pain by cutaneous nerve section8 and the relief of deep pain from a wounded area by cutaneous nerve block6.
1 Bessou, P. and Laporte, Y., Some observation on receptors of the soleus muscle innervated by Group III afferent fibers, J. Physiol, (Lond.), 155 (1961) 19p. 2 Chang, S. C., Wei, J. Y. and Mao, C. P., Discharges of su• ral nerve fibers produced by needling or pinching Achilles tendon, (in Chinese) Kexue Tongbao, 23 (1978) 565-567. 3 Gasser, H. S., Effect of method leading on the recording of the nerve fiber spectrum, J. gen. Physiol., 43 (1960) 927-940. 4 Mense, S. and Schmidt, R. F., Activation of Group IV afferent units from muscle by algesic agents, Brain Research, 72 (1974) 305-310. 5 Paintal, A. S., Functional analysis of Group III afferents of mammalian muscle, J. Physiol. (Lond.), 152 (1960) 250-270. 6 Shanghai First People's Hospital and Shanghai Institute of Physiology, Preliminary report of the analgesic effect of electro-acupuncture exerted on the nerve innervated the
operation or wounded areas, (in Chinese) Chinese Surg. J., 15 (1977) 19-21. 7 Stilwell, D. L., The innervation of tendons and aponeuroses, Amer. J. Anat., 100 (1957) 289-318. 8 Strong, E. R. and Davila, J. C., The cluneal nerve syndrome --A distinct type of low back pain, Industr. Med. Surg., 26 (1957) 417-429. 9 Weddell, G., Guttmann, L. and Gutmann, E., The local extension of nerve fibers into denervated areas of skin, J. Neurol., Psychiat., 4 (1941) 206-225. 10 Wei, J. Y., Feng, C. C., Chu, T. H. and Chang, S. C., Observations of activity of some deep receptors in cat hindlimb during acupuncture, (in Chinese) Kexue Tongbao, 18 (1973) 184-186. 11 Wei, J. Y., Chang, S. C. and Feng, C• C., Activation ofunmyelinated muscle afferents by acupuncture or pressure exerted on muscle, (in Chinese with English abstract) Acta zool. sin., 24 (1978) 21-28.
The authors thank Dr. H. T. Chang and Dr. E. Shen for their help and encouragement throughout this study. We wish to thank Dr. P. R. Burgess for his encouragement to publish this work in English and for his help with the manuscript, and Dr. R. P. Tuckett for his helpful suggestions on the manuscript.
262
Deep innervation of sural nerve S. C. CHANG, J. Y. WEI* and C. P. MAO**
Shanghai Institute of Physiology, Academia Sinica, 320 Yo-Yang Road, Shanghai (People's Republic of China) (Accepted July 26th, 1983)
Key words: deep innervation - - sural nerve - - pain - - nociceptor
Discharges of 37 sural afferents in the Aa to C fiber range have been recorded during stimulation of subcutaneous tissues after removal of the skin. Except for one Aa unit with muscle spindle properties, fibers were not easily excited by muscle stretching. The more slowly conducting fibers tended to have higher thresholds. After repeated stimulation, most A6 and C units displayed a persistent afterdischarge which lasted from several minutes to more than half an hour. It is well known that the sural nerve innervates skin covering the ankle and foot. However, Stiiwell 7 demonstrated morphologically in the cat that small fasciculi of the sural nerve supply small (up to 2 u m ) and large (5-7 g m ) fibers to the superficial surface of the Achilles tendon. Small fibers o u t n u m b e r e d large ones by about 4 to 1, and both formed free endings. This suggests that some sural sensory fibers innervate deep structures. The aim of the present work was to see whether electrophysiological methods would give evidence of deep receptors supplied by surat nerve. A preliminary report has a p p e a r e d in Chinese 2. Experiments were carried out on 15 adult cats (2-3 kg), under pentobarbital anesthesia (40 mg/kg, i.p.). Supplementary doses were regularly given to maintain deep anesthesia. A small segment of sural nerve trunk was isolated from its surrounding tissue in the distal part of the popliteal fossa and put on a pair of stimulating electrodes. The single unit afferent discharges were recorded with a bipolar recording electrode (30 g m diameter, platinum wire) from nerve filaments dissected from a more proximal part of the nerve. The distance between stimulating and recording electrodes was 3-4 cm. The detailed description of this method was given in another paperl~. The skin around the lower leg and ankle joint was
separated completely from the deep tissue, so that no afferent discharges could be recorded from sural nerve when wiping or squeezing the zone of sural innervation. The natural stimuli used to search for deep receptors supplied by the sural nerve were needling with an acupuncture needle, pressing with a glass rod or spring b a r o m e t e r , pinching the Achilles tendon and nearby deep tissues, and stretching the triceps surae muscles. A f t e r a unit's receptive field was carefully localized with natural stimuli, the deep tissue was cut away under magnification ( 2 5 - 4 0 x ) , layer by layer, until no afferent discharges could be p r o d u c e d by reapplying the same stimuli to the receptive field. Sural nerve fibers that innervate deep tissue were isolated in each of the 15 successful experiments. Thirty-seven sural fibers activated from deep tissue were studied. Fig. 1 shows the distribution of the conduction velocities of 32 of these afferent fibers. The conduction velocities of the other 5 units were not measured accurately, but 3 of them could still be identified as C fibers. In accordance with Gasser's criterion 3, the 6 fibers having conduction velocities between 40 and 85 m/s will be called ' A a ' fibers, the 12 fibers conducting more slowly than 30 m/s but faster than 2.5 m/s will be called 'Ac~' and the 14 fibers conducting more slowly than 2.5 m/s will be called 'C"
* Address for correspondence: Department of Physiology, 410 Chipeta Way, Research Park, Salt Lake City, Utah 84108, U.S.A. *~ Present address: Shanghai Brain Research Institute, 319 Yo-Yang Road, Shanghai, China. 0006-8993/83/$03.00 © 1983 Elsevier Science Publishers B.V.
263 unit, Table I) showed that stretching the Achilles tendon with a force of 500-700 g could only excite 2 A 6 units to fire 1-2 impulses. The other 6 units did not respond at all. On the other hand, all 8 units could be stimulated by pressing their receptive fields. The maximum averaged frequency (averaged over 1 s) was usually in the range of 10-30 imp/s. There were two different response patterns. Twenty-six of the 35 units that were tested showed persistent discharge during pressing (Fig. 2A). These included 4 A a , 12 A6, and 10 C fibers. The other 9 units, 2 A a and 7 C units, responded only transiently to pressure changes (Fig. 2C). The thresholds of the units varied. We divided the manually applied pressure stimuli into 3 categories: heavy (more than 200 g), moderate (50-200 g) and light (less than 50 g). Only 3 C units could be activated by light pressure; the others required moderate to heavy pressure. A a and A6 units behaved differently. Most of them needed only light or moderate pressure for activation (Table I). The highest threshold measurement was for a C unit, about 500-700 g force; the lowest for an A6 unit at only 10 g. This difference is similar to our previous observations of the threshold range for pressure receptors of the tibialis anterior musclel0,11. After locating the most sensitive receptive point of 20 units with a glass rod, we inserted an acupuncture, needle into the point and manipulated it. Nineteen of the 20 units responded with either a persistent (Fig. 2B) or a burst of discharges. The maximum average firing rates for different units varied from 1 to 80 imp/s with 11 of the 19 units discharging between
I0
Az
A~
8
D=
2
0
0 0.5
1.5
I0
C~GTION
30
50
70
9O
VELOCffY (M/SEC)
Fig. 1. Distribution of conduction velocities of Aa, A6 and C fibers of sural nerve which innervated deep structures. fibers. The ratio between small (A6 + C) and large (Aa) fibers was about 4:1. This result is similar with the result from the morphological study by Stilwell 7. The main results of this experiment have been summarized in the Table. Spontaneous discharges. Eight out of 35 units displayed irregular spontaneous discharges (Table I). The discharge rates were 1--4 imp/s for C fibers and 5-14 imp/s for A6 fibers. There was one A a unit with a regular resting discharge of 24 imp/s. It responded to muscle stretch like a spindle afferent. Response to mechanical stimuli. Except for the one spindle-like receptor, these units were like the pressure receptors supplied by muscle nervesl,4,5,10. They could not easily be excited by muscle stretching but could be activated by pressing their receptive fields. The results of testing 8 units (excluding the spindle TABLE I Fiber type
Number of fibers
Spontaneous discharge
Aa A6 C
6 12 17
1 3 4
Total
35
8
After-
Mechanicalstimuli Needling
Pressing Threshold
Response pattern
Response pattern
More than 200g
Persistent
Bu~t
Per s&tent
Less than 50g
50200g
4* 5 3
1 6 8
1 1 6
4* 12 10
2 0 7
15
8
26
9
12
* The one spindle-like Ace unit fell into this group.
Response to muscle stretch
discharge
Bunt
No
Yes
No
0 7 5
2 2 3
1 0 0
1" 2 0
1 4 1
0 6 9
12
7
1
3
6
15
264
A o•
°Q
~o
o,
°°
.'.
:
• g
..
o*
m
.~:-.....~.~.~
-
= -'. i"
,.
o
. -,~. -4
m
C
| Fig. 2. Record of discharge frequency vs time. A shows the persistent discharge of an A6 unit when pressing on the receptive field (line under spike trace) and the after-discharge when pressure was released. The conduction velocity was 30 m/s. B shows the response to needling stimulation of a C unit with 0.52 m/s conduction velocity. J' indicates inserting a needle into the receptive field center; - - shows period of manipulating the needle; --- represents no manipulation but needle still in the point; ], shows withdrawal of the needle. The vertical position of each dot in A and B represents the number of spikes in 1 s. Calibration in B for both A and B, vertical bar = 5 spikes; horizontal bar = 28 s. C is a record of an Aa unit with conduction velocity 60 m/s, showing a bursting discharge in response to maintained pressure. The vertical position of each dot represents the number of spikes in 100 ms. Calibration: 4 spikes and 16s.
10-30 imp/s. Two A a units displayed a short burst of activity and most C and A d units displayed a persistent response (Table I). After-discharge. In 15 units, all A 6 or C, manual needling or r e p e a t e d pressing on the receptive field was followed by an after-discharge that was persistent, irregular and low in frequency and lasted for variable time periods (Fig. 2A, B). F o u r of these 15 units originally had spontaneous firing; after the stimulation the firing rate increased. For two units the after-discharge lasted more than half an hour. This p h e n o m e n o n is similar to our previous observation on the pressure receptors supplied by C fibers of the tibialis anterior muscle nerve II . The rates of af-
ter-discharge ranged from 2 imp/s to 24 imp/s, most being less than 10 imp/s. Receptive fields. The receptive fields of these receptors usually were not as easily located as those of cutaneous m e c h a n o r e c e p t o r s , especially if the receptive field was deep within the muscle or tendon. This is because the direction of the mechanical stimuli can influence the accuracy of the threshold m e a s u r e m e n t and localization of the receptive field. Fibers were found to innervate a variety of deep structures. The receptive fields of 17 units were located on or in the Achilles tendon and the musculotendinous junction, 6 around the distal part of lateral malleolus, 11 in the lateral gastrocnemius muscle, one in the medial gastrocnemius muscle, and the other 2 in the connective tissue around the sural nerve. The structure of the receptive fields differed somewhat. Eight units had small relatively well-defined receptive fields; five (3 A 6 , 2 C) were located on superficial connective tissue layers, one in the muscle, one in the tendon and the other at the musculotendinous junction. A n o t h e r 4 units showed band-like receptive fields. Of these, two A 6 units had 1 × 0.2 cm and 2.5 × 0.2 cm receptive fields, one A a had a 2.5 × 1.3 cm receptive field, the other A a unit terminated along a blood vessel and had 4 small, separate receptive fields. O n e of the C units had two separate sensitive spots; one on the connective tissue around the nerve trunk and the other on the superficial connective tissue near the nerve trunk. In relation to conduction velocity, 14 out of 37 total units, (3 A a , 5 A 6 , 4 C and the two units for which conduction velocity was not d e t e r m i n e d ) , were located deep within the tendon; 6 units (1 Act, 5 C) deep within the muscle; 3 units (2 A 6 , 1 C) were deeply located at the muscle-tendon conjunction; 12 units (2 Aa, 5 A 6 , 5 C) on the superficial layers of the connective tissue covering muscle, tendon and adjacent deep structures. The other 2 units were located on the connective tissue around the nerve. In summary, we have recorded the discharges of 37 sural afferents during stimulation of subcutaneous tissues after removal of the skin. Receptive fields were located in the Achilles tendon and adjacent deep tissues and in the gastrocnemius muscle. The conduction velocities of 32 units were m e a s u r e d ; 6 fell into the A a , 12 into the A 6 and 14 into the C fiber range. Except for one A a unit with muscle spindle
265 properties, the fibers were not easily excited by muscle stretching but could be activated by pressing on their receptive fields. There was a tendency for more slowly conducting fibers to have higher thresholds; most of the C and A 6 fibers required stimuli that were probably noxious. Four C units fired spontaneously (1-4 imp/s) and 3 A 6 had spontaneous activity (5-14 imp/s). After repeated stimulation, most A6 and C units displayed a persistent afterdischarge that was irregular and low in frequency and which lasted from several minutes to more than half an hour. This appears to be the first electrophysiological study demonstrating that fibers of a cutaneous nerve innervate deep tissue. We did not completely search a whole sural nerve trunk in a single experiment and so no estimate can be made of the percentage of deep fibers that travel in the sural nerve. However, together with the histological work of Stilwell 7 our study demonstrates that normally there are fibers in the sural nerve which supply deep structures and hence, strictly speaking, the sural is not a pure cutaneous nerve. Most of the deep fibers are small myelinated or C fibers with high thresholds suggesting a nociceptive function. A more general issue is whether other cutaneous
nerves also have this kind of deep innervation. Selective block of the superficial radial nerve at the wrist decreases but does not eliminate, deep pain elicited by squeezing or inserting a needle into the first dorsal interosseous muscle of the hand (unpublished observations). Thus, the superficial radial nerve (a cutaneous nerve) probably contains some fibers supplying deep tissues. Weddell et al. in 1941 pointed out that the peripheral nerve fields from adjacent nerves usually overlap 9. In addition, it may be that overlapping innervation in the third dimension (i.e. vertical overlapping directed from superficial to deep tissues) is also common, providing an additional safety factor for an animal when a deep nerve is damaged• The presence of deep fibers in cutaneous nerves may help to explain the reduction of low back pain by cutaneous nerve section8 and the relief of deep pain from a wounded area by cutaneous nerve block6.
1 Bessou, P. and Laporte, Y., Some observation on receptors of the soleus muscle innervated by Group III afferent fibers, J. Physiol, (Lond.), 155 (1961) 19p. 2 Chang, S. C., Wei, J. Y. and Mao, C. P., Discharges of su• ral nerve fibers produced by needling or pinching Achilles tendon, (in Chinese) Kexue Tongbao, 23 (1978) 565-567. 3 Gasser, H. S., Effect of method leading on the recording of the nerve fiber spectrum, J. gen. Physiol., 43 (1960) 927-940. 4 Mense, S. and Schmidt, R. F., Activation of Group IV afferent units from muscle by algesic agents, Brain Research, 72 (1974) 305-310. 5 Paintal, A. S., Functional analysis of Group III afferents of mammalian muscle, J. Physiol. (Lond.), 152 (1960) 250-270. 6 Shanghai First People's Hospital and Shanghai Institute of Physiology, Preliminary report of the analgesic effect of electro-acupuncture exerted on the nerve innervated the
operation or wounded areas, (in Chinese) Chinese Surg. J., 15 (1977) 19-21. 7 Stilwell, D. L., The innervation of tendons and aponeuroses, Amer. J. Anat., 100 (1957) 289-318. 8 Strong, E. R. and Davila, J. C., The cluneal nerve syndrome --A distinct type of low back pain, Industr. Med. Surg., 26 (1957) 417-429. 9 Weddell, G., Guttmann, L. and Gutmann, E., The local extension of nerve fibers into denervated areas of skin, J. Neurol., Psychiat., 4 (1941) 206-225. 10 Wei, J. Y., Feng, C. C., Chu, T. H. and Chang, S. C., Observations of activity of some deep receptors in cat hindlimb during acupuncture, (in Chinese) Kexue Tongbao, 18 (1973) 184-186. 11 Wei, J. Y., Chang, S. C. and Feng, C• C., Activation ofunmyelinated muscle afferents by acupuncture or pressure exerted on muscle, (in Chinese with English abstract) Acta zool. sin., 24 (1978) 21-28.
The authors thank Dr. H. T. Chang and Dr. E. Shen for their help and encouragement throughout this study. We wish to thank Dr. P. R. Burgess for his encouragement to publish this work in English and for his help with the manuscript, and Dr. R. P. Tuckett for his helpful suggestions on the manuscript.