On the controversy of autotomy: a response to L. Kruger

120

ical. and electrophysiological either PAIN

02157

similarity

of the behavioral

els. Kruger minimized

On the controversy Kruger

of autotomy:

a response

to L.

repeated

among deafferented alluded

expressed

including

by him (Rodin

(Kruger

presented

of this journal,

pain.

by one of us (Levitt primary

animal

tors interpret perceived

objection

skepticism

was earlier

1984) and again in a recent

to rebut that skeptical

view was

19850 several years ago. Now,

of

it is

and in this journal.

Kruger

is the principal this anomolous

chronic

This

negative

abnormal

interpretation

aesthetics

was directed

intercede.

We

dependent

variable.

behavioral

against

those

was rejected

by Kruger;

in other

that

these

formats (Levitt

1992), but they received not yet appeared Major

lest animal-rights two conclusions

of major

the word

unfortunate havioral

of London (Wall

and they have

to denote

of reduced

of ‘autotomy

signs of positive

emphasis

as a

investigators That

was an

the total be-

is placed

behavior

upon

self-

which is directed

noxious sensibility; (b) the logic and

scores’ remain

sensory disorders

sensory loss (Bennett

Those

this effect.

than the compulsive

territories

by rodents

as it misrepresents

misleading

which

et al. 1979). That work

neurectomy.

inasmuch

(a)

rather

interpretation

poorly

to the work

acral self-mutilation

‘autotomy’

syndrome:

abnormalities

among these animal modthose changes that occur

non-sensory disturbances

widely distributed

moot; and (c) behavioral

in cutaneous

areas

and Xie 1988; Kingery and Vallin

of partial

1989; Seltzer

et al. 1990) tend to be ignored.

With tion

untestable.

his conclusion

that autotomy

is solely attributable

reasoned

of nerve or root deafferenta-

to central

neural

disturbances.

that almost any psychophysiological

able for the explanation sensations. derived

This

from

of autotomy,

specious

and

two claims: (a)

of pain.

except

obscure

disturbing was mainly

occurs when

there

does not occur when

be examined. Examples of self-mutilation, tions are presumed first claim. These afflicted

in which persistent disturbing

not to be present, included:

the animal

by the Lesch-Nyhan

severe social isolation, three examples (Levitt

caught

syndrome,

in a trap,

the animal

were considered the

to be likely.

such examples ts supported

in an earlier

presence

That

rebuttal

of disturbing

point

of this claim

sensations

can also be argued

does not allow a strong argument

by unambiguous

do not present with autotomy response

to chronic

pain.

autotomy.

experimental

of the pathophysi-

studies. The early statement

that autotomy

is a response to ongoing

sprouts of C fibers. Despite hypothesis,

generated

essential

in injured

and this is the

It is important

to notice

consists of at least two hypotheses: perceived

pain, and (b) autotomy

impulses in injured

assessment of many experiments

of abnormal

activity

then proceeded

afferents

give

such a statement

really

is a response

to abnormal

by Kruger

to

nerve

has been his

He might be correct.

then made was also to reject the

that since autotomy primary

is not a function

afferents,

sensations. Other

it is not a

considerations

nociception,

autotomy

inflammation.

whereas

the experimental

is limited to territories in hyperalgesic derives (Levitt

of chronic

models

increased

in which

nociception.

autotomy Autotomy

of reduced pain sensibility and does not occur

or allodynic areas. Moreover,

a misconception

cannot be a

to models of re-

This claim is misleading

occurs are based upon conditions of reduced

of the

behavioral

this claim derives from

pattern

1985, 1988, 1990, 1991a.

models of chronic peripheral

self-mutilation

from

which

1992). That

inflammation

autotomy

behavioral

(Albe-Fessard

to the likely conclusion

to a chronic disturbance

that autotomy

is

in the CNS, as in cases of dorsal

and such central alterations

of abnormal

peripheral

are essentially independent

input from injured primary afferents.

1985, 1987, 1988, 1990. 1991a,

sion long ago, based on the comparability

1992) reached

One of

that conclu-

of morphological,

biochem-

than in the inflammation

of the analgesic dependent

self-directed

of reduced

pain

theoretical

The

primary

models,

or hypoalgesic

variable

behavior.

sensibility

significance.

evidence.

pat-

et al. 1990).

(often

That

including

Autotomy question

tissues. Hence,

unappreciated)

it is directed analgesic

is merely

A constructive compulsive provided

rationale

for the

behavior,

the

toward

1985, 1988, 1991a). That evidence

animal

self-directed

learned

responses

readily

observed

toward tissues

scratching,

revealed

was

evidence

that in the intact

which

un-

are evoked

Veterinarians

by

accept

as a clinical sign of somatic pain or itch. A

recently

published

historical

(Kirkup

1988) cited records of compelling

survey

of

human cases with persistent social isolation,

human

pain

relevance.

individuals

management Those records

somatic pain, due to disease

those individuals

hand or foot. Moreover,

analgesics or anesthetics,

of pertinent

licking and biting were natural

to the aversive sensations

of behavior

of the chronic

results in autotomy,

many forms of acute noxious somatic stimuli.

obtaining

tissues

the facts wherein

interpretation

which

(Levitt

the painful

the

is the

tissues has special

should concern

previously by an objective evaluation

dcscrihed

is

insensitive.

self-directed

or injury; during

pattern

and it causes

this chronic compulsive pattern of behavior is directed which are peripherally

this pattern

to be unwarranted.

rhizotomies, us (Levitt

viz.,

cause of chronic

(a) autotomy

to be untenable.

in nociceptive

indicate this latter conclusion attributable

that

remain.

which pertain to the second of these

function of pain or other abnormal Kruger

nociceptive

is a response

but the logical error which Kruger first hypothesis. He concluded

evolving modifi-

elements

principal

C fibers. A main effort

hypotheses, which he inferred

of

against the view

alludes

because these models are based on conditions

compulsive

pain,

the

is that other models of chronic pain and, therefore,

He apparently

sponse to chronic peripheral

is generated

impulses

was

for

evidence.

The second claim of Kruger

most significant

rise to ongoing

under

example of tail removal. The essential point is that the uncertainty

pain which is based upon ongoing ectopic nerve impulse activity that

abnormal

the

the child

reared

of longer duration

in neuroma

sensa-

to support

and the lizard which sheds its tail. The first

19X5), wherein

considered

were offered

has generated

cations of the original

is

evidence of pain in other widely accepted models. These claims must

In the models with nervous system lesions, this behavioral

indicated

is no

there

tern includes scratching, licking, biting, etc., which also occurs in the

The London school provided an interpretation numerous

Kruger

is reason-

abnormal

interpretation

autotomy

and (b) autotomy

hypothesis

ological mechanism which gives rise to autotomy, and that hypothesis of the hypothesis

in

that persistent disturbing sensations motivate autotomy: a view which

peripheral

designation.

amputation,

extremists were

have been made

from Kruger,

has been given by Kruger

has focused upon the chronic adopted

the

to urge

1985, 1987, 1988, 1990, 1991a,b,

little attention

at the University

consequence

Kruger

in this journal.

attention

originated

of

moreover,

prompted

be discontinued,

will argue

Some investiga-

pains or dysesthesias in analgesic body

derived and are ill advised. Some of our arguments previously

after

sensory neurons in the dorsal horn and instead

to ubiquitous

evidence

effect to be a reflection

of this phenomenon

that scientific enquiry

toward

(1992)

models of nervous system injury in which acral self-mutila-

tion, autotomy,

parts.

That

and Kruger

1991). An attempt

timely to pursue the polemics further, The

Kruger

of certain animal models of chronic abnormal

sensation,

horn

and also based upon the

the CNS; this is an hypothesis which has not been specifically tested.

to the editor

his rejection

unpleasant article

letter

in the dorsal

the facts concerning

and which is virtually In a recent

alterations

nerve injury or dorsal rhizotomies,

‘self-amputated’

before the discovery of medical with such pains sought aid in

relief by surgical amputations.

Literature reviews (Levitt 1985, 1988, 1990, 199ia) have revealed that chronic compulsive self-directed behavior and acral self-mutilation by animals occur in the veterinary clinic or in the experimental laboratory as consequences of lesions in either peripheral sensory nerve, dorsal root ganglia, dorsal roots, or dorsal piexi. They also occur as a result of lesions in the spinal cord or brain (Levitt 199ib; Xu et al. 1992). Signs of ali~ynia and hyperalgesia have been sometimes noted. Signs of acral self-mutilation have been also noted i young human cases with peripheral sensory neuropathy or syringomyelia (Levitt 1985, 199ia,b); it also has been described in an human infant with brachial plexus injury (Rossitch et al. 1992). These cases were verbally incompetent patients who could not communicate positive sensory disturbances. Two adult human cases with brachiai plexus injury have been recently described (Albe-Fessard et al. 1990; Procacci and Maresca 19901, who bit and mutilated their finger tips during sleep and complained of painful dysesthesias during wakefulness. The DREZ lesion has been particularly successful for the relief of the human pains of brachial plexus avulsion (Nashold and Ostdahl iY79; Friedman et al. 1988). That surgical lesion was also found to abolish the pains of brachial plexus *‘aversion” in one of the patients who committed autotomy (Procacci and Maresca 1990). Unfortunately, no specific comment was made regarding the probable effect of DREZ surgery on autotomy. We have found that autotomy was markedly attenuated or prevented by DREZ surgery in rats which were totally deafferented by ganglionectomies (Gvelmen-Levitt et al. 1991; Rossitch et al. 1992). Thus, experiences with surgical relief of human deafferentation pains provided a testable hypothesis regarding the prevention of deafferentation autotomy in rats, and that hypothesis was confirmed. Eventually we expect that studies of autotomy will provide testable hypotheses regarding treatment of human deafferentation pains, and these hypotheses will be upheld. Such an event will provide the ultimate validation of autotomy. Hence, our assessment of unambiguous evidence leads us to conclusions which are contrary to some of those reached by Kruger. The total syndrome of behavioral response to certain sensorineural lesions reflects signs of spontaneous and peripherally induced dysesthesias. Acral self-mutilation is a special element of the larger syndrome and it likely signifies the spontaneous dysesthesias which are referred to territories of reduced peripheral sensibilities. The validity of this assertion receives impressive support from the fact that lesions in sensory components of the peripheral or central nervous system which originate autotomy are essentially the same as those which are known to originate dysesthesias in humans. Moreover, additional support for this validity was provided by the prophylactic effect of the DREZ lesion in deafferented rats. inasmuch as such abnormal disturbing sensations are among the most poorly understood, we must question the wisdom which urges cessation of inquiry into autotomy. In addition, we find it disconcerting to consider that such censorship might be fostered by fear of a radical terrorist movement. A rational expectation would envisage great encouragement for the scientific study of autotomy (and the totality of the syndrome).

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