- Email: [email protected]
Correlation of histology and sensibility after nerve repair
Correlation of histology and sensibility after nerve repair The partially denervated human fingertip was used as a model to correlate results of a detailed evaluation of sensibility with the presence of reinnervated sensory corpuscles identified by light and electron microscopy. In each of the three patients studied, the histologically identified reinnervated mechanoreceptors were appropriate to provide the neurophysiologic basis for the observed results of clinically tested sensibility. (J HAND SURG 8:871-5, 1983.)
A. Lee Dellan, M.D .,* and Bryce L. Munger, M.D.,** Baltimore, Md., and Hershey, Pa.
T he high density of mechanoreceptive af-
ferents in the distal glabrous skin of primates makes it technically difficult to obtain single-fiber nerve recordings that can be correlated with specific mechanoreceptors in the normally-innervated hand. The single-fiber nerve recordings that have correlated the pacinian corpuscle in the cat with high frequency, quickly-adapting afferents, 1. 2 the Iggo-touch corpuscle in the cat,3. 4 and the Merkel cell-rete papilla in the raccoon5 with slowlyadapting afferents were made possible by the unique presence of a relatively large mechanoreceptor in relative isolation from other mechanoreceptors. By inference,6. 7 the Meissner corpuscle was associated with the low-frequency, quickly-adapting afferents. These findings in lower mammals can be extrapolated to humans on the basis of percutaneous records in awake subjects, 8 and this entire topic has been reviewed recently in detail. 9 These correlations now have been confirmed in a preliminary report of a model that used dorsal root ganglionectomized primates. 10 The human fingertip after nerve repair offers a similar area of greatly reduced innervation density in which it may be possible to correlate the presence of reinnervated mechanoreceptors with the clinically evaluated sensibility . This study reports a detailed histologic evaluation of fingertip biopsies from three patients after nerve repair . *From the Division of Plastic Surgery. Johns Hopkins University and Curtis Hand Center. Union Memorial Hospital. Baltimore . Md .• and **Department of Anatomy. Milton S. Hershey Medical Center. Pennsylvania State University School of Medicine. Hershey. Pa . Presented at the meeting of The American Association of Plastic and Reconstructive Surgeons. Williamsburg. Va .• May 13. 1981. Received for publication Nov . 19. 1981; accepted in revised form Nov . 23. 1982. Reprint requests: A. Lee Dellon. M.D .• The Hampton Plaza . 300 E. Joppa Rd .• Baltimore. MD 21204.
Method Evaluation of sensibility. Before fingertip biopsy, each fingertip had the following tests carried out as originally described: moving-touch, constant-touch7 • 9; 30 and 256 cycles/sec tuning fork 7 • 9; SemmesWeinstein monofilaments ll ; vibrometer l 2 • 13; static two-point discrimination l4 ; and moving two-point discrimination. 15 Evaluation of sensory end-organs. After obtaining informed consent, an elliptical biopsy was taken from the tip of the long finger in each of the three patients. The biopsy was taken deeply enough to include the subcutis. Specimens were placed in cacodylate buffer for 48 hours. Each elliptical block of skin was bisected with one half prepared for electron microscopy and one half for light microscopy . For light microscopy, the tissue was then fixed for several days in 10% neutral buffered formalin and embedded in paraffin. Two hundred serial sections were mounted and stained with a modified Bielschowsky method. 16 For electron microscopy , small cylinders of skin were postfixed in 1% osmium tetroxide and embedded in oxalalite. Thin sections were cut with diamond knives and examined in a Phillips 300 and 400 electron microscope. The histologic evaluation was done without benefit of knowing the results of the clinical evaluation . Patient reports These three patients were selected for study because they represented early stages in the recovery of sensibility subsequent to median nerve division and repair. Thus the fingertips would be only partially reinnervated. Patient C. E. A 24-year-old man was evaluated 11 months after grafting of median nerve at the wrist. Perception of moving-touch and 30 and 256 cycles/sec vibratory stimuli were present in the long finger. There was no perception of THE JOURNAL OF HAND SURGERY
871
872
The Journal of HAND SURGERY
Dellon and MUI1Xer
PATIE TC. E. AGE 24 IIMOTIIS SIP M[OIAN ERVE GRAn 30 ~PS
o
YE VI H
5.46
yes M2 PD
.82
IOmm
Fig. 1. Correlation of histology and sensibility in patient C. E. See text for discussion. constant-touch stimuli, even when applied with heavy pressure. The cutaneous pressure threshold (Semmes-Weinstein monofilament) was 5.46 . The cutaneous vibratory threshold was 0.82 /-L . The moving two-point discrimination was 10 mm . The static two-point discrimination was not obtainable (>30 mm). Corresponding control values were 2.83, 0 .09 /-L, 2 mm, and 3 mm. Patient L. T. A 30-year-old woman was evaluated 27 months after median nerve repair at the wrist. Perception of moving-touch, constant-touch (to heavy pressure), and 30 and 256 cps vibratory stimuli were in the long finger. The cutaneous pressure threshold was 5.46. The cutaneous vibratory threshold was 0.36 /-L. The moving two-point discrimination was 4 mm. The static two-point discrimination was not obtainable (>30 mm) . Corresponding control values were 3.84, 0 . 16 /-L . 2 mm , and 3 mm . Patient E. L. A 60-year-old man was evaluated II months after median nerve repair at the wrist. Perception of movingtouch. constant-touch (to heavy pressure) and 30 and 256 cps vibratory stimuli were present in the long finger. The cutaneous pressure threshold was 6.45. The cutaneous vibratory threshold was 0.36 /-L. The moving two-point discrimination was 4 mm. The static two-point discrimination was not obtainable (> 30 mm). Corresponding control values were 3.22. 0.12 /-L, 2 mm. and 4 mm.
Results Patient C. E. The specimen had one reinnervated pacinian corpuscle. There were no recognizable innervated or denervated Merkel cells. There were four reinnervated and numerous degenerated Meissner corpuscles in a 5 mm 2 area of serial paraffin sections from the center of the biopsy. Dermal nerve networks were present , although sparse. These results are correlated with the sensory evaluation and depicted in Fig. I. Patient L. T. The specimen had one reinnervated pacinian corpuscle. One reinnervated Merkel Cell-Neurite complex was identified (Fig. 2) . No denervated Merkel cells were identified . There were numerous reinnervated Meissner corpuscles (Fig. 3) and some degenerating Meissner corpuscles.
Dermal nerve networks were present in abundance but still abnormal in density. The axons in these networks had smaller diameters than normal. The results are correlated with the sensory evaluation and depicted in Fig. 4. Patient E. L. The specimen had one reinnervated pacinian corpuscle. There was a reinnervated Merkel cell- neurite complex near the proximal end of the specimen. In addition to the presence of numerous degenerating Meissner corpuscles. there were 10 reinnervated Meissner corpuscles (Fig. 3) in a 5 mm 2 area of serial paraffin sections from the middle of the biopsy. Dermal nerve networks were well represented . A figure showing their correlation is not included in the text as it would be identical to Fig. 4.
Discussion
This study demonstrated that there is an excellent correlation between the results of an evaluation of sensibility of a fingertip and the reinnervated sensory end-organs present within that fingertip. It is assumed that the patient tested is maximally able to use the altered profile of neural impulses arising from his fingertip after the nerve repair. To help this assumption approximate reality, each of the patients with biopsied fingertips had a course of sensory reeducation 17. IH before their final evaluation of sensibility and fingertip biopsy. There have been two similar attempts to make these correlations in the past, and each has found a negative correlation. In the first study, 19 3 mm punch biopsies were taken of patients' fingertips at varying times after nerve repairs. Although the evaluation of sensibility was almost identical to that used in the present study (the moving two-point discrimination test was not included because it had not been described at that time), the patients had not received sensory reeducation before testing, and the observed sensory end-organs in the biopsy were not correlated with the appropriate test of sensibility. Furthermore, the biopsy size was small to assess fully the pattern of reinnervation, and electron microscopy was not used to identify the Merkel cells. The most recent report described biopsies of fingertips and palms resurfaced with grafts of hairy skin .20 These patients reportedly had "tactile gnosis" (term undefined in the study) but their biopsies showed no "sensory end-organs. " Published photomicrographs ofthese patients did, however, show well-innervated hair follicles which, of course, are fully capable of fine tactile discrimination. 21 - 23 We suggest these reinnervated hair follicles served as the "sensory end-organs" for the patients' reported "tactile gnosis." Figs. I and 4 demonstrate the pattern of sensory end-organ reinnervation after nerve repair. In Fig. I, there was no perception of constant-touch or static
Vol. 8 , No.6 November 1983
Histology and sensibility after nerve repair
873
Fig. 2. Reinnervated Merkel cell-neurite complex from patient L. T. Note presence of multiple axons adjacent to Merkel cell and the abundant and dense intracytoplasmic vesicles polarized toward the axons. (Magnification x 10,800.)
two-point discrimination, and no innervated Merkel cells were observed. In Fig. 3, where constant-touch had recovered, there was a reinnervated Merkel cellneurite complex. These are the appropriate correlations since the Merkel cell-neurite complex is the receptor for the slowly-adapting fiber/receptor system, which mediates perception of constant-touch and pressure. 4 • 5 The cutaneous pressure thresholds were high in both
these cases, and the perceived sensation was probably pain and not touch. Where moving-touch and perception of 30 cycles/ sec vibratory stimuli were present, vibratory threshold was near normal , and moving two-point discrimination was near normal (patients L. T. and E. L.), there were numerous (although still less than half the normal number) reinnervated Meissner corpuscles (Fig. 3). In pa-
874
Dellon and Mung er
The Journal of HAND SURGERY
Fig. 3. Reinnervated Meissner corpuscles from patient L. T . (A) and patient C. E . (8). (Original Magnifications: A, x 6800; B, x 2750 .)
Vol. 8, No.6 November 1983
Histology and sensibility after nerve repair
PATIE T L .T.
\(,[ 30 27 ~IONTIIS S. P \llDIA "lRVl RlPAIR "0\1'" 10\.:( It
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7.
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5,46
.36
8.
9.
4mm
10. Fig. 4. Correlation of histology and sensibility in patient L. T. See text for discussion.
tient C. E., in whom perception of 30 cycles/sec vibratory stimuli and moving-touch were present, vibratory threshold was abnormal, and moving two-point discrimination was almost absent (a lower peripheral innervation density), there were markedly fewer innervated Meissner corpuscles (Fig. 1). In all three patients the 256 cycles/sec vibratory stimuli could be perceived, and there was a reinnervated pacinian corpuscle present (Figs. I and 3). These are the appropriate correlations since the Meissner and pacinian corpuscles are the receptors of the quickly-adapting fiber/receptor system, mediating the perception of moving-touch. The Meissner afferents are most sensitive to vibrations at 30 cycles/sec while the pacinian afferents are most sensitive at 256 cycles/sec. 2 • 6 We thank Susan E. Mackinnon, M.D., F.R.C.S.(C)., for critical help in manuscript revision. REFERENCES I. Lowenstein WR, Mendelson M: Components of receptor adaptation in a pacinian corpuscle. J Physiol 177:377-97, 1965 2. Werner G, Mountcastle VB: Neural activity in mechanoreceptive afferents: Stimulus response relations, Weber functions, and information transmission. J Neurophysiol 28: 359-97, 1965 3. Brown AG, Iggo A: A quantitative study of cutaneous receptor and afferent fibers in the cat and rabbit. J Physiol 193:707-33, 1967 4. Iggo A, Muir AR: The structure and function of a slowly-adaptinng sensory receptor in mammalian glabrous skin. Brain Res 29:47-61, 1971 5. Munger BL, Pubols LM, Pubols BH Jr: The Merkel rete papilla-a slowly-adapting sensory receptor in mammalian glabrous skin. Brain Res 29:47-61, 1971 6. Talbot WH, Darian-Smith I, Kornhuber HH, et al: The
II.
12. 13. 14.
15.
16.
17.
18.
19.
20. 21.
22. 23.
875
sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive at"ferents from the monkey hand. J Neurophysiol 31:301-34, 1968 Dellon AL, Curtis RM, Edgerton MT: Evaluating recovery of sensation in the hand following nerve injury. Johns Hopkins Med J 130:235-43, 1972 Johansson RS, Vallbo AB: Tactile sensibility in the human hand: Relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol 286:283-300, 1979 Dellon AL: Evaluation of sensibility and re-education of sensation in the hand. Baltimore, 1981, The Williams & Wilkins Co, chapt 2, 3, 10 Munger BL, Page RB, Pubols BH Jr: Identification of specific mechanosensory receptors in glabrous skin of dorsal root ganglionectomized primates. Anat Rec 193:630-1, 1979 Levin S, Pearsall G, Ruderman RJ: von Frey's method of measuring pressure sensibility in the hand: An engineering analysis of the Weinstein-Semmes pressure esthesiometer. J HAND SURG 3:211-6, 1978 Daniel CR, Bower JD, Pearson JE, et al: Vibrometryand neuropathy. J Miss State Med Assoc 18: 30-4, 1977 Dellon AL: The vibrometer. Plast Reconstr Surg 71: 427-31,1983 Moberg E: Objective methods of determining functional value of sensibility in the hand. J Bone Joint Surg [Br] 40:454-66, 1958 Dellon AL: The moving two-point discrimination test: Clinical evaluation of the quickly-adapting fiber/receptor system. J HAND SURG 3:474-81, 1978 Sevier AC, Munger BL: A silver method applicable to paraffin sections of formol-fixed tissue. J Neuropathol Exp Neurol 24: 130-5, 1965 Dellon AL, Curtis RM, Edgerton MT: Re-education of sensation in the hand following nerve injury. Plast Reconstr Surg 53:297-305, 1974 Dellon AL: Evaluation of sensibility and re-education of sensation in the hand. Baltimore, 1981, The Williams & Wilkins Co, chapt 12 Jabaley ME, Burns JE, Ortt BS, et al: Comparison of histologic and functional recovery after peripheral nerve repair. J HAND SURG 1:119-30, 1976 Matev IB: Tactile gnosis in free skin grafts in the hand. Br J Plast Surg 33:434-9, 1980 Merzenich MM, Harrington T: The sense of fluttervibration evoked by stimulation of the hairy skin of primates: Comparison of human sensory capacity with responses of mechanoreceptive afferents innervating the hairy skin of monkeys. Exp Brain Res 9:236-60, 1969 Halata Z, Munger BL: Sensory nerve endings in rhesus monkey sinus hairs. 1. Comp Neural 192:645-63, 1980 Munger BL: Multiple afferent innervation of primate facial hairs-Henry Head and Max von Frey revisited. Brain Res Rev 4: 1-43, 1982
A. Lee Dellan, M.D .,* and Bryce L. Munger, M.D.,** Baltimore, Md., and Hershey, Pa.
T he high density of mechanoreceptive af-
ferents in the distal glabrous skin of primates makes it technically difficult to obtain single-fiber nerve recordings that can be correlated with specific mechanoreceptors in the normally-innervated hand. The single-fiber nerve recordings that have correlated the pacinian corpuscle in the cat with high frequency, quickly-adapting afferents, 1. 2 the Iggo-touch corpuscle in the cat,3. 4 and the Merkel cell-rete papilla in the raccoon5 with slowlyadapting afferents were made possible by the unique presence of a relatively large mechanoreceptor in relative isolation from other mechanoreceptors. By inference,6. 7 the Meissner corpuscle was associated with the low-frequency, quickly-adapting afferents. These findings in lower mammals can be extrapolated to humans on the basis of percutaneous records in awake subjects, 8 and this entire topic has been reviewed recently in detail. 9 These correlations now have been confirmed in a preliminary report of a model that used dorsal root ganglionectomized primates. 10 The human fingertip after nerve repair offers a similar area of greatly reduced innervation density in which it may be possible to correlate the presence of reinnervated mechanoreceptors with the clinically evaluated sensibility . This study reports a detailed histologic evaluation of fingertip biopsies from three patients after nerve repair . *From the Division of Plastic Surgery. Johns Hopkins University and Curtis Hand Center. Union Memorial Hospital. Baltimore . Md .• and **Department of Anatomy. Milton S. Hershey Medical Center. Pennsylvania State University School of Medicine. Hershey. Pa . Presented at the meeting of The American Association of Plastic and Reconstructive Surgeons. Williamsburg. Va .• May 13. 1981. Received for publication Nov . 19. 1981; accepted in revised form Nov . 23. 1982. Reprint requests: A. Lee Dellon. M.D .• The Hampton Plaza . 300 E. Joppa Rd .• Baltimore. MD 21204.
Method Evaluation of sensibility. Before fingertip biopsy, each fingertip had the following tests carried out as originally described: moving-touch, constant-touch7 • 9; 30 and 256 cycles/sec tuning fork 7 • 9; SemmesWeinstein monofilaments ll ; vibrometer l 2 • 13; static two-point discrimination l4 ; and moving two-point discrimination. 15 Evaluation of sensory end-organs. After obtaining informed consent, an elliptical biopsy was taken from the tip of the long finger in each of the three patients. The biopsy was taken deeply enough to include the subcutis. Specimens were placed in cacodylate buffer for 48 hours. Each elliptical block of skin was bisected with one half prepared for electron microscopy and one half for light microscopy . For light microscopy, the tissue was then fixed for several days in 10% neutral buffered formalin and embedded in paraffin. Two hundred serial sections were mounted and stained with a modified Bielschowsky method. 16 For electron microscopy , small cylinders of skin were postfixed in 1% osmium tetroxide and embedded in oxalalite. Thin sections were cut with diamond knives and examined in a Phillips 300 and 400 electron microscope. The histologic evaluation was done without benefit of knowing the results of the clinical evaluation . Patient reports These three patients were selected for study because they represented early stages in the recovery of sensibility subsequent to median nerve division and repair. Thus the fingertips would be only partially reinnervated. Patient C. E. A 24-year-old man was evaluated 11 months after grafting of median nerve at the wrist. Perception of moving-touch and 30 and 256 cycles/sec vibratory stimuli were present in the long finger. There was no perception of THE JOURNAL OF HAND SURGERY
871
872
The Journal of HAND SURGERY
Dellon and MUI1Xer
PATIE TC. E. AGE 24 IIMOTIIS SIP M[OIAN ERVE GRAn 30 ~PS
o
YE VI H
5.46
yes M2 PD
.82
IOmm
Fig. 1. Correlation of histology and sensibility in patient C. E. See text for discussion. constant-touch stimuli, even when applied with heavy pressure. The cutaneous pressure threshold (Semmes-Weinstein monofilament) was 5.46 . The cutaneous vibratory threshold was 0.82 /-L . The moving two-point discrimination was 10 mm . The static two-point discrimination was not obtainable (>30 mm). Corresponding control values were 2.83, 0 .09 /-L, 2 mm, and 3 mm. Patient L. T. A 30-year-old woman was evaluated 27 months after median nerve repair at the wrist. Perception of moving-touch, constant-touch (to heavy pressure), and 30 and 256 cps vibratory stimuli were in the long finger. The cutaneous pressure threshold was 5.46. The cutaneous vibratory threshold was 0.36 /-L. The moving two-point discrimination was 4 mm. The static two-point discrimination was not obtainable (>30 mm) . Corresponding control values were 3.84, 0 . 16 /-L . 2 mm , and 3 mm . Patient E. L. A 60-year-old man was evaluated II months after median nerve repair at the wrist. Perception of movingtouch. constant-touch (to heavy pressure) and 30 and 256 cps vibratory stimuli were present in the long finger. The cutaneous pressure threshold was 6.45. The cutaneous vibratory threshold was 0.36 /-L. The moving two-point discrimination was 4 mm. The static two-point discrimination was not obtainable (> 30 mm). Corresponding control values were 3.22. 0.12 /-L, 2 mm. and 4 mm.
Results Patient C. E. The specimen had one reinnervated pacinian corpuscle. There were no recognizable innervated or denervated Merkel cells. There were four reinnervated and numerous degenerated Meissner corpuscles in a 5 mm 2 area of serial paraffin sections from the center of the biopsy. Dermal nerve networks were present , although sparse. These results are correlated with the sensory evaluation and depicted in Fig. I. Patient L. T. The specimen had one reinnervated pacinian corpuscle. One reinnervated Merkel Cell-Neurite complex was identified (Fig. 2) . No denervated Merkel cells were identified . There were numerous reinnervated Meissner corpuscles (Fig. 3) and some degenerating Meissner corpuscles.
Dermal nerve networks were present in abundance but still abnormal in density. The axons in these networks had smaller diameters than normal. The results are correlated with the sensory evaluation and depicted in Fig. 4. Patient E. L. The specimen had one reinnervated pacinian corpuscle. There was a reinnervated Merkel cell- neurite complex near the proximal end of the specimen. In addition to the presence of numerous degenerating Meissner corpuscles. there were 10 reinnervated Meissner corpuscles (Fig. 3) in a 5 mm 2 area of serial paraffin sections from the middle of the biopsy. Dermal nerve networks were well represented . A figure showing their correlation is not included in the text as it would be identical to Fig. 4.
Discussion
This study demonstrated that there is an excellent correlation between the results of an evaluation of sensibility of a fingertip and the reinnervated sensory end-organs present within that fingertip. It is assumed that the patient tested is maximally able to use the altered profile of neural impulses arising from his fingertip after the nerve repair. To help this assumption approximate reality, each of the patients with biopsied fingertips had a course of sensory reeducation 17. IH before their final evaluation of sensibility and fingertip biopsy. There have been two similar attempts to make these correlations in the past, and each has found a negative correlation. In the first study, 19 3 mm punch biopsies were taken of patients' fingertips at varying times after nerve repairs. Although the evaluation of sensibility was almost identical to that used in the present study (the moving two-point discrimination test was not included because it had not been described at that time), the patients had not received sensory reeducation before testing, and the observed sensory end-organs in the biopsy were not correlated with the appropriate test of sensibility. Furthermore, the biopsy size was small to assess fully the pattern of reinnervation, and electron microscopy was not used to identify the Merkel cells. The most recent report described biopsies of fingertips and palms resurfaced with grafts of hairy skin .20 These patients reportedly had "tactile gnosis" (term undefined in the study) but their biopsies showed no "sensory end-organs. " Published photomicrographs ofthese patients did, however, show well-innervated hair follicles which, of course, are fully capable of fine tactile discrimination. 21 - 23 We suggest these reinnervated hair follicles served as the "sensory end-organs" for the patients' reported "tactile gnosis." Figs. I and 4 demonstrate the pattern of sensory end-organ reinnervation after nerve repair. In Fig. I, there was no perception of constant-touch or static
Vol. 8 , No.6 November 1983
Histology and sensibility after nerve repair
873
Fig. 2. Reinnervated Merkel cell-neurite complex from patient L. T. Note presence of multiple axons adjacent to Merkel cell and the abundant and dense intracytoplasmic vesicles polarized toward the axons. (Magnification x 10,800.)
two-point discrimination, and no innervated Merkel cells were observed. In Fig. 3, where constant-touch had recovered, there was a reinnervated Merkel cellneurite complex. These are the appropriate correlations since the Merkel cell-neurite complex is the receptor for the slowly-adapting fiber/receptor system, which mediates perception of constant-touch and pressure. 4 • 5 The cutaneous pressure thresholds were high in both
these cases, and the perceived sensation was probably pain and not touch. Where moving-touch and perception of 30 cycles/ sec vibratory stimuli were present, vibratory threshold was near normal , and moving two-point discrimination was near normal (patients L. T. and E. L.), there were numerous (although still less than half the normal number) reinnervated Meissner corpuscles (Fig. 3). In pa-
874
Dellon and Mung er
The Journal of HAND SURGERY
Fig. 3. Reinnervated Meissner corpuscles from patient L. T . (A) and patient C. E . (8). (Original Magnifications: A, x 6800; B, x 2750 .)
Vol. 8, No.6 November 1983
Histology and sensibility after nerve repair
PATIE T L .T.
\(,[ 30 27 ~IONTIIS S. P \llDIA "lRVl RlPAIR "0\1'" 10\.:( It
'L~
7.
l"b
JO
lOUt H
(P\
(.I')
YES
Y~S
YES
(0'')1'\
I
(Hb"VV)
====
\l,?PD
5,46
.36
8.
9.
4mm
10. Fig. 4. Correlation of histology and sensibility in patient L. T. See text for discussion.
tient C. E., in whom perception of 30 cycles/sec vibratory stimuli and moving-touch were present, vibratory threshold was abnormal, and moving two-point discrimination was almost absent (a lower peripheral innervation density), there were markedly fewer innervated Meissner corpuscles (Fig. 1). In all three patients the 256 cycles/sec vibratory stimuli could be perceived, and there was a reinnervated pacinian corpuscle present (Figs. I and 3). These are the appropriate correlations since the Meissner and pacinian corpuscles are the receptors of the quickly-adapting fiber/receptor system, mediating the perception of moving-touch. The Meissner afferents are most sensitive to vibrations at 30 cycles/sec while the pacinian afferents are most sensitive at 256 cycles/sec. 2 • 6 We thank Susan E. Mackinnon, M.D., F.R.C.S.(C)., for critical help in manuscript revision. REFERENCES I. Lowenstein WR, Mendelson M: Components of receptor adaptation in a pacinian corpuscle. J Physiol 177:377-97, 1965 2. Werner G, Mountcastle VB: Neural activity in mechanoreceptive afferents: Stimulus response relations, Weber functions, and information transmission. J Neurophysiol 28: 359-97, 1965 3. Brown AG, Iggo A: A quantitative study of cutaneous receptor and afferent fibers in the cat and rabbit. J Physiol 193:707-33, 1967 4. Iggo A, Muir AR: The structure and function of a slowly-adaptinng sensory receptor in mammalian glabrous skin. Brain Res 29:47-61, 1971 5. Munger BL, Pubols LM, Pubols BH Jr: The Merkel rete papilla-a slowly-adapting sensory receptor in mammalian glabrous skin. Brain Res 29:47-61, 1971 6. Talbot WH, Darian-Smith I, Kornhuber HH, et al: The
II.
12. 13. 14.
15.
16.
17.
18.
19.
20. 21.
22. 23.
875
sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive at"ferents from the monkey hand. J Neurophysiol 31:301-34, 1968 Dellon AL, Curtis RM, Edgerton MT: Evaluating recovery of sensation in the hand following nerve injury. Johns Hopkins Med J 130:235-43, 1972 Johansson RS, Vallbo AB: Tactile sensibility in the human hand: Relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol 286:283-300, 1979 Dellon AL: Evaluation of sensibility and re-education of sensation in the hand. Baltimore, 1981, The Williams & Wilkins Co, chapt 2, 3, 10 Munger BL, Page RB, Pubols BH Jr: Identification of specific mechanosensory receptors in glabrous skin of dorsal root ganglionectomized primates. Anat Rec 193:630-1, 1979 Levin S, Pearsall G, Ruderman RJ: von Frey's method of measuring pressure sensibility in the hand: An engineering analysis of the Weinstein-Semmes pressure esthesiometer. J HAND SURG 3:211-6, 1978 Daniel CR, Bower JD, Pearson JE, et al: Vibrometryand neuropathy. J Miss State Med Assoc 18: 30-4, 1977 Dellon AL: The vibrometer. Plast Reconstr Surg 71: 427-31,1983 Moberg E: Objective methods of determining functional value of sensibility in the hand. J Bone Joint Surg [Br] 40:454-66, 1958 Dellon AL: The moving two-point discrimination test: Clinical evaluation of the quickly-adapting fiber/receptor system. J HAND SURG 3:474-81, 1978 Sevier AC, Munger BL: A silver method applicable to paraffin sections of formol-fixed tissue. J Neuropathol Exp Neurol 24: 130-5, 1965 Dellon AL, Curtis RM, Edgerton MT: Re-education of sensation in the hand following nerve injury. Plast Reconstr Surg 53:297-305, 1974 Dellon AL: Evaluation of sensibility and re-education of sensation in the hand. Baltimore, 1981, The Williams & Wilkins Co, chapt 12 Jabaley ME, Burns JE, Ortt BS, et al: Comparison of histologic and functional recovery after peripheral nerve repair. J HAND SURG 1:119-30, 1976 Matev IB: Tactile gnosis in free skin grafts in the hand. Br J Plast Surg 33:434-9, 1980 Merzenich MM, Harrington T: The sense of fluttervibration evoked by stimulation of the hairy skin of primates: Comparison of human sensory capacity with responses of mechanoreceptive afferents innervating the hairy skin of monkeys. Exp Brain Res 9:236-60, 1969 Halata Z, Munger BL: Sensory nerve endings in rhesus monkey sinus hairs. 1. Comp Neural 192:645-63, 1980 Munger BL: Multiple afferent innervation of primate facial hairs-Henry Head and Max von Frey revisited. Brain Res Rev 4: 1-43, 1982