- Email: [email protected]
Adaptation in Mechanoreceptors of Amphibian Skin
Adaptation in Mechanoreceptors of Amphibian Skin W. T. CATTON Physiology Department, Medical School, The University, Newcastle upon Tyne (Great Britain)
The mechanoreceptive terminals in the dermal and epidermal layers of frog and toad skin consist largely of free nerve endings, with widespread overlapping distribution (e.g. Whitear, 1955). They show a wide range of adaptation rates to prolonged steady stimuli (e.g. Catton, 1958; Lindblom, 1958). The capsule of the Pacinian corpuscle has been regarded as a high-pass mechanical filter, giving to this receptor organ the property of very rapid adaptation (e.g. Hubbard, 1958; Loewenstein and Skalak, 1966), such that only one or two spikes may be fired a t the onset of the stimulus. But many receptors in frog skin (“tactile receptors”) show similar rapid adaptation, along with others which are more slowly adapting. Recent anatomical studies have revealed the presence of highly organised encapsulated endings in the skin of Rana esculenta, resembling the structure of mammalian Pacinian corpuscles (During and Seiler, 1974). These corpuscles were found in all skin areas, but were densest near the tips of the digits. The existence of these structures was not known when the work now to be described was performed, but this fact is not considered to invalidate the theoretical basis or the conclusions reached. Thus it was proposed (Catton and PeToe, 1966) that mechanical “slip” of the terminal, with respect to the surrounding tissue, can largely account for the adapta-
S = zf(i-e-47). -f
Fig. 1. a: series visco-elasticmodel. b: force F, moves skin cylinder through distance x, and sensory terminal moves through distance S. References P . 230
228
W. T. CATTON
tion shown by skin mechanoreceptors; a quantitative theory was developed. A little earlier, Catton (1966) had shown that a brief delay occurs in the mechanical mode of stirnulation, and that this delay varied with stimulus parameters. This conclusion was reached by comparing the latencies of responses, recorded close to the receptor, to mechanical and electrical pulse stimulation of the same receptor. The concept of “slip” led to the consideration of a simple series visco-elastic model (Fig. I), in which the force extending the terminal was dependent on viscous drag, and the restoring force was the elastic property of the axon terminal. Analysis of such a model yields the following relation between velocity of skin movement (dx/dt) and resulting change in length of the terminal (S). Thus
S
=
(
~ d x / d t 1 - exp
(-
where 7 is a time constant and t is the time taken for S to reach its new and final value. x depends on the coefficient of viscosity of the coupling fluid and on the geometry
of the terminal itself. The firing of the spike is assumed to occur when S reaches a threshold value S‘, at time t‘ (see Fig. 2). The steeper the rise of the stimulus (dx/dt) the sooner is S‘ (and hence t’) attained, which corresponds with the experimental observation that the response latency shortens as the stimulus slope becomes steeper. An alternative statement of Equation 1 is thus: (2)
Stimulus slope was plotted against latency for a large number of skin receptors (experimental results). Computer solutions of Equation 2 were obtained for different chosen values of S’ and T ; these constants could not be known beforehand. An approximation for S‘ was given by the threshold amplitude for a very steep slope, where “slip” is least, and by the restriction that S’ is always less than X (skin dis-
100
6
5
-
90 80
r
70 60 50
2 40 -x
30 20 10
10
20
30
40
50
t (rnsrc)
Fig. 2. S (and x) plotted against time, for a range of velocities <); from 1 to 10 ,urn/msec, as calculated from the basic equation. The t value was 20 msec and S’, the arbitrary threshold, was set at 15 ,urn.
ADAPTATION IN MECHANORECEPTORS OF AMPHIBIAN SKlN
229
18
5
10-
2-
I I I I I
10
- 1
20
-
30
-
40
d
50
Latency (msec)
Fig. 3. Experimental slope-latency curve for a frog skin receptor, compared with theoretical curve derived from the basic equation, after compensation for afferent conduction time. (S’ = 5 ,urn; t = 40 msec.)
placement). The constant z was estimated by taking an arbitrary value oft‘, being that intercept on the time axis corresponding to twice the critical slope, and designated t,. It was shown that t, = 0.693 7. With these data it was possible to obtain very close fits with experimental slopelatency curves (Catton and PeToe, 1966) (Fig. 3). However, this is not an absolute proof that visco-elastic behaviour explains adaptation. A different process, such as accommodation of the receptor terminal, could obey a similar law with respect to stimulus slope and lead to a similar result. This was not investigated, but instead some experiments were performed to test the mechanical hypothesis. Thus whole skin-nerve preparations were treated with tissue-destroying enzymes, such as collagenase, hyaluronidase and trypsin. After an appropriate time for enzyme action the responses were tested again and there were found to be changes in slope-latency curves and in critical slopes in accordance with expectations from the visco-elastic model. Such treatments would not be expected to affect accommodative properties, but only mechanical linkage. Both dynamic and static excitability changes were produced by long duration mechanical deflections (Catton, 1962). The static change was assumed to be due to an additional elastic coupling between terminal and tissue, so that in a prolonged deflection the terminal was held in some degree of steady extension. In this type of experiment, using long subliminal stimuli, it was found that enzyme treatments resulted in a marked decline in the static phase, indicating a loosening in the elastic bonding (Catton and PeToe, 1966). Where both viscous and elastic coupling is assumed the mathematical analysis is more complex and theoretical prediction is not possible in a quantitative manner. In addition to the publications mentioned above there will appear a further account in a forthcoming book, “Frog Neurobiology”, to be published by Springer Verlag, 1975. Mechanoreceptor adaptation in a wider context is discussed in a recent review (Catton, 1970). References p .
230
230
W. T. CATTON
SUMMARY
The mechanoreceptors in amphibian skin are found to show a wide range in rates of adaptation to constant stimuli. Whereas most of the sensory terminals are free nerve endings, some lamellated corpuscles have recently been found, and these are probably the fast adapting “touch” receptors. By comparing the latencies of responses to electrical and mechanical stimulation of the same receptor it was shown that there is a brief delay in mechanical excitation. A theory of “slip” was proposed to explain this delay, and the behaviour of a series visco-elastic model was analysed. The model predicted that response latency would vary with slope of stimulus. This relationship was studied experimentally on skin receptors, and the slope-latency curves plotted were compared with curves derived from the analysis of the model. Good fits could be obtained when allowance was made for conduction time in the sensory axon, and when selection was made of two constants. One of these represented threshold extension of the terminal, the other was a time constant. The values selected were always within physiological range. Treatment with tissue-destroying enzymes, expected to increase the degree of “slip”, produced changes in slope-latency curves in accord with the theory. Experiments on the excitability changes under long subliminal conditioning pulses demonstrated both a dynamic and a static phase. The latter was ascribed to elastic (in addition to viscous) coupling between tissue and terminal. Again, enzyme treatment caused changes which would be expected from theory. A model which included an elastic coupling element yielded equations with too many unknown constants to enable quantitative theoretical predictions to be made. REFERENCES CATTON, W. T. (1958) Some properties of frog skin rnechanoreceptors. J, Physiol. (Lond.), 141, 305-322. CATTON, W. T. (1962) The effects of subliminal stimulation on the excitability of frog skin tactile receptors. J. Physiol. (Lond.), 164,90-102. CATTON, W. T. (1966) A comparison of the responses of frog skin receptors to mechanical and electrical stimulation. J. Physiol. ( L o n d ) , 187, 23-34. CATTON, W. T. (1970) Mechanoreceptor function. Physiol. Rev., 50, 297-318. CATTON,W. T. AND PETOE,N. (1966) A visco-elastic theory of mechanoreceptor adaptation. J. Physiol. (Lond.), 187, 35-50. DURING, M. VON AND SEILER, W. (1974) The fine structure of lamellated receptors in the skin of Rana esculenta. Z . Anat. Entwick1.-Gescli., 144, 165-172. HUBBARD, S . J. (1958) A study of rapid mechanical events in a mechanoreceptor.J. Physiol. ( L o n d ) , 141,198-218. LINDBLOM, U. F. (1958) Excitability and functional organisation within a peripheral tactile unit. Acta physiol. scand., 44, Suppl. 153, 5-82. LOEWENSTEIN, W. R. AND SKALAK, R. (1966) Mechanical transmission in a Pacinian corpuscle. An analysis and a theory. J. Physiol. (Lond.), 182, 347-378. WHITEAR, M. (1955) Dermal nerve endings in Rana and Bufo. Quart. J. micr. Sci., 96, 343-349.
ADAPTATION IN MECHANORECEPTORS OF AMPHIBIAN SKIN
23 1
DISCUSSION ANDRES: I should ask you what diameter have the fibers, from which you made your recordings. In your morphological experiments we had two types of fibers from mechanoreceptors in the skin, the one with a very large diameter and another of one-half of this. CATTON: I did not in fact measure the diameter of fibers in the skin nerves but most of the experiments were on large fibers.
ANDRES: Though we have had 4 different types of the endings in the skin, only one is published. Three other types were stretch receptors too.
The mechanoreceptive terminals in the dermal and epidermal layers of frog and toad skin consist largely of free nerve endings, with widespread overlapping distribution (e.g. Whitear, 1955). They show a wide range of adaptation rates to prolonged steady stimuli (e.g. Catton, 1958; Lindblom, 1958). The capsule of the Pacinian corpuscle has been regarded as a high-pass mechanical filter, giving to this receptor organ the property of very rapid adaptation (e.g. Hubbard, 1958; Loewenstein and Skalak, 1966), such that only one or two spikes may be fired a t the onset of the stimulus. But many receptors in frog skin (“tactile receptors”) show similar rapid adaptation, along with others which are more slowly adapting. Recent anatomical studies have revealed the presence of highly organised encapsulated endings in the skin of Rana esculenta, resembling the structure of mammalian Pacinian corpuscles (During and Seiler, 1974). These corpuscles were found in all skin areas, but were densest near the tips of the digits. The existence of these structures was not known when the work now to be described was performed, but this fact is not considered to invalidate the theoretical basis or the conclusions reached. Thus it was proposed (Catton and PeToe, 1966) that mechanical “slip” of the terminal, with respect to the surrounding tissue, can largely account for the adapta-
S = zf(i-e-47). -f
Fig. 1. a: series visco-elasticmodel. b: force F, moves skin cylinder through distance x, and sensory terminal moves through distance S. References P . 230
228
W. T. CATTON
tion shown by skin mechanoreceptors; a quantitative theory was developed. A little earlier, Catton (1966) had shown that a brief delay occurs in the mechanical mode of stirnulation, and that this delay varied with stimulus parameters. This conclusion was reached by comparing the latencies of responses, recorded close to the receptor, to mechanical and electrical pulse stimulation of the same receptor. The concept of “slip” led to the consideration of a simple series visco-elastic model (Fig. I), in which the force extending the terminal was dependent on viscous drag, and the restoring force was the elastic property of the axon terminal. Analysis of such a model yields the following relation between velocity of skin movement (dx/dt) and resulting change in length of the terminal (S). Thus
S
=
(
~ d x / d t 1 - exp
(-
where 7 is a time constant and t is the time taken for S to reach its new and final value. x depends on the coefficient of viscosity of the coupling fluid and on the geometry
of the terminal itself. The firing of the spike is assumed to occur when S reaches a threshold value S‘, at time t‘ (see Fig. 2). The steeper the rise of the stimulus (dx/dt) the sooner is S‘ (and hence t’) attained, which corresponds with the experimental observation that the response latency shortens as the stimulus slope becomes steeper. An alternative statement of Equation 1 is thus: (2)
Stimulus slope was plotted against latency for a large number of skin receptors (experimental results). Computer solutions of Equation 2 were obtained for different chosen values of S’ and T ; these constants could not be known beforehand. An approximation for S‘ was given by the threshold amplitude for a very steep slope, where “slip” is least, and by the restriction that S’ is always less than X (skin dis-
100
6
5
-
90 80
r
70 60 50
2 40 -x
30 20 10
10
20
30
40
50
t (rnsrc)
Fig. 2. S (and x) plotted against time, for a range of velocities <); from 1 to 10 ,urn/msec, as calculated from the basic equation. The t value was 20 msec and S’, the arbitrary threshold, was set at 15 ,urn.
ADAPTATION IN MECHANORECEPTORS OF AMPHIBIAN SKlN
229
18
5
10-
2-
I I I I I
10
- 1
20
-
30
-
40
d
50
Latency (msec)
Fig. 3. Experimental slope-latency curve for a frog skin receptor, compared with theoretical curve derived from the basic equation, after compensation for afferent conduction time. (S’ = 5 ,urn; t = 40 msec.)
placement). The constant z was estimated by taking an arbitrary value oft‘, being that intercept on the time axis corresponding to twice the critical slope, and designated t,. It was shown that t, = 0.693 7. With these data it was possible to obtain very close fits with experimental slopelatency curves (Catton and PeToe, 1966) (Fig. 3). However, this is not an absolute proof that visco-elastic behaviour explains adaptation. A different process, such as accommodation of the receptor terminal, could obey a similar law with respect to stimulus slope and lead to a similar result. This was not investigated, but instead some experiments were performed to test the mechanical hypothesis. Thus whole skin-nerve preparations were treated with tissue-destroying enzymes, such as collagenase, hyaluronidase and trypsin. After an appropriate time for enzyme action the responses were tested again and there were found to be changes in slope-latency curves and in critical slopes in accordance with expectations from the visco-elastic model. Such treatments would not be expected to affect accommodative properties, but only mechanical linkage. Both dynamic and static excitability changes were produced by long duration mechanical deflections (Catton, 1962). The static change was assumed to be due to an additional elastic coupling between terminal and tissue, so that in a prolonged deflection the terminal was held in some degree of steady extension. In this type of experiment, using long subliminal stimuli, it was found that enzyme treatments resulted in a marked decline in the static phase, indicating a loosening in the elastic bonding (Catton and PeToe, 1966). Where both viscous and elastic coupling is assumed the mathematical analysis is more complex and theoretical prediction is not possible in a quantitative manner. In addition to the publications mentioned above there will appear a further account in a forthcoming book, “Frog Neurobiology”, to be published by Springer Verlag, 1975. Mechanoreceptor adaptation in a wider context is discussed in a recent review (Catton, 1970). References p .
230
230
W. T. CATTON
SUMMARY
The mechanoreceptors in amphibian skin are found to show a wide range in rates of adaptation to constant stimuli. Whereas most of the sensory terminals are free nerve endings, some lamellated corpuscles have recently been found, and these are probably the fast adapting “touch” receptors. By comparing the latencies of responses to electrical and mechanical stimulation of the same receptor it was shown that there is a brief delay in mechanical excitation. A theory of “slip” was proposed to explain this delay, and the behaviour of a series visco-elastic model was analysed. The model predicted that response latency would vary with slope of stimulus. This relationship was studied experimentally on skin receptors, and the slope-latency curves plotted were compared with curves derived from the analysis of the model. Good fits could be obtained when allowance was made for conduction time in the sensory axon, and when selection was made of two constants. One of these represented threshold extension of the terminal, the other was a time constant. The values selected were always within physiological range. Treatment with tissue-destroying enzymes, expected to increase the degree of “slip”, produced changes in slope-latency curves in accord with the theory. Experiments on the excitability changes under long subliminal conditioning pulses demonstrated both a dynamic and a static phase. The latter was ascribed to elastic (in addition to viscous) coupling between tissue and terminal. Again, enzyme treatment caused changes which would be expected from theory. A model which included an elastic coupling element yielded equations with too many unknown constants to enable quantitative theoretical predictions to be made. REFERENCES CATTON, W. T. (1958) Some properties of frog skin rnechanoreceptors. J, Physiol. (Lond.), 141, 305-322. CATTON, W. T. (1962) The effects of subliminal stimulation on the excitability of frog skin tactile receptors. J. Physiol. (Lond.), 164,90-102. CATTON, W. T. (1966) A comparison of the responses of frog skin receptors to mechanical and electrical stimulation. J. Physiol. ( L o n d ) , 187, 23-34. CATTON, W. T. (1970) Mechanoreceptor function. Physiol. Rev., 50, 297-318. CATTON,W. T. AND PETOE,N. (1966) A visco-elastic theory of mechanoreceptor adaptation. J. Physiol. (Lond.), 187, 35-50. DURING, M. VON AND SEILER, W. (1974) The fine structure of lamellated receptors in the skin of Rana esculenta. Z . Anat. Entwick1.-Gescli., 144, 165-172. HUBBARD, S . J. (1958) A study of rapid mechanical events in a mechanoreceptor.J. Physiol. ( L o n d ) , 141,198-218. LINDBLOM, U. F. (1958) Excitability and functional organisation within a peripheral tactile unit. Acta physiol. scand., 44, Suppl. 153, 5-82. LOEWENSTEIN, W. R. AND SKALAK, R. (1966) Mechanical transmission in a Pacinian corpuscle. An analysis and a theory. J. Physiol. (Lond.), 182, 347-378. WHITEAR, M. (1955) Dermal nerve endings in Rana and Bufo. Quart. J. micr. Sci., 96, 343-349.
ADAPTATION IN MECHANORECEPTORS OF AMPHIBIAN SKIN
23 1
DISCUSSION ANDRES: I should ask you what diameter have the fibers, from which you made your recordings. In your morphological experiments we had two types of fibers from mechanoreceptors in the skin, the one with a very large diameter and another of one-half of this. CATTON: I did not in fact measure the diameter of fibers in the skin nerves but most of the experiments were on large fibers.
ANDRES: Though we have had 4 different types of the endings in the skin, only one is published. Three other types were stretch receptors too.