- Email: [email protected]
‘Autotomy’: A terminological inexactitude
286
Letters to the Editor / Pain 128 (2007) 283–294
Angelo G. Rocco* Opal Towers 215S, 1147 Hillsboro Mile, Hillsboro Beach, FL 33062-1715, USA E-mail address: [email protected] Stephen A. Raymond Chief Scientific Officer PHT Corporation, 500 Rutherford Ave., Charlestown MA 02129, USA
*
Corresponding author. Tel.: +1 603 772 5260. 0304-3959/$32.00 Ó 2006 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.pain.2006.10.005
ÔAutotomyÕ: A terminological inexactitude Dear Editor, The term ÔautotomyÕ is used currently in the scientific literature to refer to two biologically unrelated phenomena: the adaptive self-detachment of animal structures, which is employed as a defensive strategy, and the pathological self-mutilation displayed by mammals as a result of dysfunctioning of the central or peripheral nervous system. Below we show that the latter usage is completely inappropriate and has led to a misapprehension amongst pain physiologists that the two phenomena are connected, and we propose a change in terminology. The Belgian zoologist Le´on Fredericq introduced the term ÔautotomieÕ in 1883 to describe the self-detachment of the limbs of crabs and the tails of reptiles (specifically slow worms and lizards) that is provoked by external stimulation (Fredericq, 1883). In this and in a subsequent paper (Fredericq, 1887) he made it clear that he intended the term to be restricted to the shedding of animal body parts where this serves a defensive (usually anti-predator) function, is achieved by an intrinsic mechanism and is mediated via the nervous system. Autotomy in this sense is practised by a wide range of animals in addition to crabs and reptiles, including jellyfish, snails, earthworms, spiders, insects and starfish.
In all these animals autotomy always occurs at an anatomically distinct breakage plane at which there are specific adaptations for facilitating detachment, minimising tissue damage (via localised planes of weakness), minimising loss of body fluids, accelerating wound healing or promoting regeneration. There are always physiological adaptations for bringing about breakage: muscular mechanisms in jellyfish, crabs and lizards, and connective tissue weakening mechanisms in starfish and their relations (see e.g. Sheppard and Bellairs, 1972; McVean, 1973; Bickell-Page and Mackie, 1991; Wilkie, 2001). The Greek root ÔtomeÕ, meaning ÔcuttingÕ, is particularly appropriate because of the ÔcleanÕ appearance of wound surfaces after autotomy, which in some cases can look as if the structure had been cut across with a sharp blade. In addition, autotomy is always the response component of a neural reflex (activated when sensory stimuli exceed a certain threshold) and it always increases an animalÕs chances of survival (usually by permitting rapid escape from a predator). ÔAutotomyÕ is thus a zoological term with a precise and delimited meaning. In the century following its invention, however, the term was applied to an ever-widening range of phenomena, at least by mainland European authors. For example, Declich (1956) noted that ÔautotomyÕ had become synonymous with ÔautomutilationÕ and was employed for any form of self-injuring behaviour, including self-castration in humans. This application of the term received a particular boost when Wall et al. (1979), in the pages of this journal, used it for the self-inflicted injury, ranging from cutaneous lacerations to amputation of digits by gnawing, exhibited by laboratory rats following experimentally contrived neural lesions, such as transection of the sciatic nerve. Wall et al. introduced this usage in the briefest of sentences (‘‘We call this phenomenon ÔautotomyÕ.’’) without further explanation, implying it was a neologism and thus ignoring both its zoological origins and the precedent set by Continental authors for applying it to self-mutilation in general. The term has subsequently been applied to every type of compulsive self-directed behaviour resulting in tissue damage, whatever the aetiology, from head banging in mentally disturbed humans to the biting off of whole surgically denervated limbs in
Table 1 Comparison of the diagnostic features of autotomy and autoblaby Autotomy
Autoblaby
Self-inflicted injury in form of anatomical loss
Self-inflicted injury in form of anatomical loss or of mutilation without anatomical loss Injury caused by effectors external to site of injury No specific anatomical adaptations No specific physiological adaptations Not response component of neural reflex Usually reduces survival chances (pathological)
Injury caused predominantly by effectors localised to site of injury Specific anatomical adaptations Specific physiological adaptations Response component of neural reflex Increases survival chances (adaptive)
Letters to the Editor / Pain 128 (2007) 283–294
laboratory mammals (see e.g. Gybels and Kupers, 1991; Bowsher, 2002). This has become by far the commoner usage. An internet search in August 2006 for articles published in the period 1980 to 2006 with ÔautotomyÕ in the title or abstract generated 249 ÔhitsÕ, 193 (77%) referring to pathological self-inflicted injury, 52 (21%) to defensive self-detachment and 4 (2%) to neither. One factor contributing to the widespread adoption of this usage in recent decades is that Wall et al. (1979) is a frequently cited paper, because it introduced a scoring system for quantifying self-inflicted damage, which has been popular amongst researchers employing the self-injuring behaviour of nerve-damaged rodents and other animals as a model for the investigation of neuropathic pain. Rodin and Kruger (1984) acknowledged the scientific provenance of the term, but unfortunately legitimised its misuse by implying wrongly that there are important similarities between lizard tail shedding and neuropathic self-mutilation in mammals. They stated that ÔautotomyÕ is ‘‘a common term in biology used to denote the biting and scraping behaviour of lizards in shedding a denervated tail’’. This is quite mistaken. As is plainly evident from the literature, lizards discard normal tails, which are fully innervated and fully sensate, by an internal muscular mechanism that may be assisted by, but does not depend on, leverage of the tail against an external object (such as the mouth of a predator), and certainly involves nothing comparable to the repetitive self-directed rubbing, scratching or gnawing associated with neuropathic self-mutilation (Sheppard and Bellairs, 1972; Arnold, 1984). The myth that lizard tail autotomy is a response to denervation was perpetuated by Levitt (1985) and by Kruger (1991). Although they both involve self-inflicted damage, there is no biological link between defensive self-detachment and neuropathic or psychopathological self-injury, i.e. they are neither analogous (evolved independently but serving a similar function) nor homologous (evolved from each other or from a common ancestral mechanism). The former is a strategy for promoting survival and the latter is a symptom of a pathological condition and as such has no biological function (in the sense of a function for which the behaviour and responsible anatomical structures have been specifically adapted via natural selection). It is therefore misleading and unhelpful to apply a single term to two entirely different categories of phenomena. A separate term is required for pathological selfinjury and we suggest that this should be a new term untainted by past imprecision. For this purpose we propose ÔautoblabyÕ (from the Greek ÔblabeÕ, damage, injury; suggested to us by the Classics scholar R.M. Orr), which we define as: self-mutilation resulting from a neurological or psychological dysfunction. Whilst we are reluctant to expand further the already over-inflated
287
lexicon of biology, we hope that scrutiny of Table 1, which highlights the differences between autotomy sensu stricto and autoblaby, will convince pain physiologists that a new term is justified.
References Arnold EN. Evolutionary aspects of tail shedding in lizards and their relatives. J Nat Hist 1984;18:127–69. Bickell-Page LR, Mackie GO. Tentacle autotomy in the hydromedusa Aglantha digitale (Cnidaria): an ultrastructural and neurphysiological analysis. Philos Trans R Soc Lond B 1991;331:155–70. Bowsher D. Human ÔautotomyÕ. Pain 2002;95:187–9. Declich M. Alcune considerazioni sul problema psicopatologico dellÕautotomia (a proposito di due case di autoevirazione). Rass Studi Psichiatr 1956;45:603–21. Fredericq L. Sur lÕautotomie. Archs Zool Exp Ge´n 1883;1: 413–26. Fredericq L. LÕautotomie chez les e´toiles de mer. Rev Scient Paris se´r 3 1887;13:589–92. Gybels J, Kupers R. Significance of autotomy and scratching after peripheral nerve injury. In: Besson JM, Guilbaud G, editors. Lesions of Primary Afferent Fibers as a Tool for the Study of Clinical Pain. Amsterdam: Elsevier Publishers B.V.; 1991. p. 101–16. Kruger L. Deafferentation: the name of the game ainÕt mainly in the pain. In: Besson JM, Guilbaud G, editors. Lesions of Primary Afferent Fibers as a Tool for the Study of Clinical Pain. Amsterdam: Elsevier Publishers; 1991. p. 117–33. Levitt M. Dysesthesias and self-mutilation in humans and subhumans: a review of clinical and experimental studies. Brain Res Rev 1985;10:247–90. McVean AR. Autotomy in Carcinus maenas (Decapoda: Crustacea). J Zool Lond 1973;169:349–64. Rodin BE, Kruger L. Deafferentation in animals as a model for the study of pain: and alternative hypothesis. Brain Res Rev 1984;7:213–28. Sheppard L, Bellairs AD. The mechanism of autotomy in Lacerta. Br J Herpetol 1972;4:276–86. Wall PD, Devor M, Inbal R, Scadding JW, Schonfeld D, Seltzer Z, Tomkiewicz MM. Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain 1979;7:103–13. Wilkie IC. Autotomy as a prelude to regeneration in echinoderms. Microsc Res Tech 2001;55:369–96.
I.C. Wilkie* S. Dolan Department of Biological and Biomedical Sciences, Glasgow Caledonian University, Glasgow G4 0BA, UK E-mail address: [email protected] ðI:C: WilkieÞ: J. Lewis D.R. Blake The Royal National Hospital for Rheumatic Diseases, Bath BA1 1RL, UK
* Corresponding author. Tel.: +44 141 331 8515. 0304-3959/$32.00 Ó 2006 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.pain.2006.10.033
Letters to the Editor / Pain 128 (2007) 283–294
Angelo G. Rocco* Opal Towers 215S, 1147 Hillsboro Mile, Hillsboro Beach, FL 33062-1715, USA E-mail address: [email protected] Stephen A. Raymond Chief Scientific Officer PHT Corporation, 500 Rutherford Ave., Charlestown MA 02129, USA
*
Corresponding author. Tel.: +1 603 772 5260. 0304-3959/$32.00 Ó 2006 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.pain.2006.10.005
ÔAutotomyÕ: A terminological inexactitude Dear Editor, The term ÔautotomyÕ is used currently in the scientific literature to refer to two biologically unrelated phenomena: the adaptive self-detachment of animal structures, which is employed as a defensive strategy, and the pathological self-mutilation displayed by mammals as a result of dysfunctioning of the central or peripheral nervous system. Below we show that the latter usage is completely inappropriate and has led to a misapprehension amongst pain physiologists that the two phenomena are connected, and we propose a change in terminology. The Belgian zoologist Le´on Fredericq introduced the term ÔautotomieÕ in 1883 to describe the self-detachment of the limbs of crabs and the tails of reptiles (specifically slow worms and lizards) that is provoked by external stimulation (Fredericq, 1883). In this and in a subsequent paper (Fredericq, 1887) he made it clear that he intended the term to be restricted to the shedding of animal body parts where this serves a defensive (usually anti-predator) function, is achieved by an intrinsic mechanism and is mediated via the nervous system. Autotomy in this sense is practised by a wide range of animals in addition to crabs and reptiles, including jellyfish, snails, earthworms, spiders, insects and starfish.
In all these animals autotomy always occurs at an anatomically distinct breakage plane at which there are specific adaptations for facilitating detachment, minimising tissue damage (via localised planes of weakness), minimising loss of body fluids, accelerating wound healing or promoting regeneration. There are always physiological adaptations for bringing about breakage: muscular mechanisms in jellyfish, crabs and lizards, and connective tissue weakening mechanisms in starfish and their relations (see e.g. Sheppard and Bellairs, 1972; McVean, 1973; Bickell-Page and Mackie, 1991; Wilkie, 2001). The Greek root ÔtomeÕ, meaning ÔcuttingÕ, is particularly appropriate because of the ÔcleanÕ appearance of wound surfaces after autotomy, which in some cases can look as if the structure had been cut across with a sharp blade. In addition, autotomy is always the response component of a neural reflex (activated when sensory stimuli exceed a certain threshold) and it always increases an animalÕs chances of survival (usually by permitting rapid escape from a predator). ÔAutotomyÕ is thus a zoological term with a precise and delimited meaning. In the century following its invention, however, the term was applied to an ever-widening range of phenomena, at least by mainland European authors. For example, Declich (1956) noted that ÔautotomyÕ had become synonymous with ÔautomutilationÕ and was employed for any form of self-injuring behaviour, including self-castration in humans. This application of the term received a particular boost when Wall et al. (1979), in the pages of this journal, used it for the self-inflicted injury, ranging from cutaneous lacerations to amputation of digits by gnawing, exhibited by laboratory rats following experimentally contrived neural lesions, such as transection of the sciatic nerve. Wall et al. introduced this usage in the briefest of sentences (‘‘We call this phenomenon ÔautotomyÕ.’’) without further explanation, implying it was a neologism and thus ignoring both its zoological origins and the precedent set by Continental authors for applying it to self-mutilation in general. The term has subsequently been applied to every type of compulsive self-directed behaviour resulting in tissue damage, whatever the aetiology, from head banging in mentally disturbed humans to the biting off of whole surgically denervated limbs in
Table 1 Comparison of the diagnostic features of autotomy and autoblaby Autotomy
Autoblaby
Self-inflicted injury in form of anatomical loss
Self-inflicted injury in form of anatomical loss or of mutilation without anatomical loss Injury caused by effectors external to site of injury No specific anatomical adaptations No specific physiological adaptations Not response component of neural reflex Usually reduces survival chances (pathological)
Injury caused predominantly by effectors localised to site of injury Specific anatomical adaptations Specific physiological adaptations Response component of neural reflex Increases survival chances (adaptive)
Letters to the Editor / Pain 128 (2007) 283–294
laboratory mammals (see e.g. Gybels and Kupers, 1991; Bowsher, 2002). This has become by far the commoner usage. An internet search in August 2006 for articles published in the period 1980 to 2006 with ÔautotomyÕ in the title or abstract generated 249 ÔhitsÕ, 193 (77%) referring to pathological self-inflicted injury, 52 (21%) to defensive self-detachment and 4 (2%) to neither. One factor contributing to the widespread adoption of this usage in recent decades is that Wall et al. (1979) is a frequently cited paper, because it introduced a scoring system for quantifying self-inflicted damage, which has been popular amongst researchers employing the self-injuring behaviour of nerve-damaged rodents and other animals as a model for the investigation of neuropathic pain. Rodin and Kruger (1984) acknowledged the scientific provenance of the term, but unfortunately legitimised its misuse by implying wrongly that there are important similarities between lizard tail shedding and neuropathic self-mutilation in mammals. They stated that ÔautotomyÕ is ‘‘a common term in biology used to denote the biting and scraping behaviour of lizards in shedding a denervated tail’’. This is quite mistaken. As is plainly evident from the literature, lizards discard normal tails, which are fully innervated and fully sensate, by an internal muscular mechanism that may be assisted by, but does not depend on, leverage of the tail against an external object (such as the mouth of a predator), and certainly involves nothing comparable to the repetitive self-directed rubbing, scratching or gnawing associated with neuropathic self-mutilation (Sheppard and Bellairs, 1972; Arnold, 1984). The myth that lizard tail autotomy is a response to denervation was perpetuated by Levitt (1985) and by Kruger (1991). Although they both involve self-inflicted damage, there is no biological link between defensive self-detachment and neuropathic or psychopathological self-injury, i.e. they are neither analogous (evolved independently but serving a similar function) nor homologous (evolved from each other or from a common ancestral mechanism). The former is a strategy for promoting survival and the latter is a symptom of a pathological condition and as such has no biological function (in the sense of a function for which the behaviour and responsible anatomical structures have been specifically adapted via natural selection). It is therefore misleading and unhelpful to apply a single term to two entirely different categories of phenomena. A separate term is required for pathological selfinjury and we suggest that this should be a new term untainted by past imprecision. For this purpose we propose ÔautoblabyÕ (from the Greek ÔblabeÕ, damage, injury; suggested to us by the Classics scholar R.M. Orr), which we define as: self-mutilation resulting from a neurological or psychological dysfunction. Whilst we are reluctant to expand further the already over-inflated
287
lexicon of biology, we hope that scrutiny of Table 1, which highlights the differences between autotomy sensu stricto and autoblaby, will convince pain physiologists that a new term is justified.
References Arnold EN. Evolutionary aspects of tail shedding in lizards and their relatives. J Nat Hist 1984;18:127–69. Bickell-Page LR, Mackie GO. Tentacle autotomy in the hydromedusa Aglantha digitale (Cnidaria): an ultrastructural and neurphysiological analysis. Philos Trans R Soc Lond B 1991;331:155–70. Bowsher D. Human ÔautotomyÕ. Pain 2002;95:187–9. Declich M. Alcune considerazioni sul problema psicopatologico dellÕautotomia (a proposito di due case di autoevirazione). Rass Studi Psichiatr 1956;45:603–21. Fredericq L. Sur lÕautotomie. Archs Zool Exp Ge´n 1883;1: 413–26. Fredericq L. LÕautotomie chez les e´toiles de mer. Rev Scient Paris se´r 3 1887;13:589–92. Gybels J, Kupers R. Significance of autotomy and scratching after peripheral nerve injury. In: Besson JM, Guilbaud G, editors. Lesions of Primary Afferent Fibers as a Tool for the Study of Clinical Pain. Amsterdam: Elsevier Publishers B.V.; 1991. p. 101–16. Kruger L. Deafferentation: the name of the game ainÕt mainly in the pain. In: Besson JM, Guilbaud G, editors. Lesions of Primary Afferent Fibers as a Tool for the Study of Clinical Pain. Amsterdam: Elsevier Publishers; 1991. p. 117–33. Levitt M. Dysesthesias and self-mutilation in humans and subhumans: a review of clinical and experimental studies. Brain Res Rev 1985;10:247–90. McVean AR. Autotomy in Carcinus maenas (Decapoda: Crustacea). J Zool Lond 1973;169:349–64. Rodin BE, Kruger L. Deafferentation in animals as a model for the study of pain: and alternative hypothesis. Brain Res Rev 1984;7:213–28. Sheppard L, Bellairs AD. The mechanism of autotomy in Lacerta. Br J Herpetol 1972;4:276–86. Wall PD, Devor M, Inbal R, Scadding JW, Schonfeld D, Seltzer Z, Tomkiewicz MM. Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain 1979;7:103–13. Wilkie IC. Autotomy as a prelude to regeneration in echinoderms. Microsc Res Tech 2001;55:369–96.
I.C. Wilkie* S. Dolan Department of Biological and Biomedical Sciences, Glasgow Caledonian University, Glasgow G4 0BA, UK E-mail address: [email protected] ðI:C: WilkieÞ: J. Lewis D.R. Blake The Royal National Hospital for Rheumatic Diseases, Bath BA1 1RL, UK
* Corresponding author. Tel.: +44 141 331 8515. 0304-3959/$32.00 Ó 2006 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.pain.2006.10.033