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Allodynia: a sensory analogue of motor mirror neurons in a hyperaesthetic patient reporting instantaneous discomfort to another's perceived sudden minor injury?
  1. J L BRADSHAW
  1. Neuropsychology Research Unit, Department of Psychology, GPO Box 17, Monash University, Victoria 3800, Australia
  2. Department of Psychology, School of Behavioural Science, University of Melbourne, Parkville, Victoria 3010, Australia
  1. Professor J Bradshaw j.l.bradshaw{at}sci.monash.edu.au
  1. J B MATTINGLEY
  1. Neuropsychology Research Unit, Department of Psychology, GPO Box 17, Monash University, Victoria 3800, Australia
  2. Department of Psychology, School of Behavioural Science, University of Melbourne, Parkville, Victoria 3010, Australia
  1. Professor J Bradshaw j.l.bradshaw{at}sci.monash.edu.au

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Parietal injury may affect spatial cognition in at least three ways: right sided damage may cause left inattention (unilateral neglect), whereby the patient ignores or fails to attend to objects or events on the contralateral (left) side of extrapersonal space1; in a rare extension of this disorder, the patient may also experience the presence (often fluctuating) of an additional, supernumerary or phantom limb2—for example, a further arm at the midline in addition to a normal one on the right, and a paralysed, neglected, or “missing” one on the left. Finally, in the Gerstmann syndrome there may be, after left parietal damage, simultaneously, left-right disorientation, acalculia, agraphia, and problems with finger (or other body part) localisation or identification. Conversely, with amputation or loss (even congenital) of a limb in an otherwise healthy individual, a phantom limb may be experienced,3 with the vivid hallucinatory experience of the continued presence of that limb; parietal mechanisms have again been invoked.

The parietal cortex interconnects with the ventral premotor cortex which, as area F5 in monkeys, contains neurons that discharge both when an animal grasps or manipulates objects, and when it sees another individual making similar actions.4 These “mirror neurons” seem to represent a system that matches observed events to similar, internally generated actions, and thus forms a link, as the authors note, between observer and actor. In humans, areas in the left inferior frontal and right superior parietal cortex become active both when producing and when seeing finger movements in others.5 Could similar mirror activity arise in a purely sensory context, such that a person, due maybe to inhibitory failure, may experience pain in a finger or limb when seeing sudden trauma (for example, a blow) to a corresponding area in another person? We report the anecdotal account, from a widow, of her late husband's apparent experience of such “mirror pain” or, as we would suggest, “allodynia”.

The deceased, a long time smoker, died in late February 1993 with the diagnosis of “extensive metastatic carcinomatosis”, antecedent cause, “carcinoma of the right lung”. (The widow, however, questions the lung cancer diagnosis, and claims that symptoms of serious rheumatoid disease involving cervical spine and dysphagia were misinterpreted.) As a consequence of increasing pain and stiffness beginning in the neck and upper body, and chest symptoms, he underwent radiography of the cervical spine and chest in August 1990, disclosing opacity in the right lung and slight tracheal deviation; he had increasing difficulty swallowing with food inhalation. Unwillingly, he underwent radiotherapy in early November 1990 to alleviate dysphagia, although according to the widow subsequent gastroscopy indicated that this may have been unnecessary.

He was reported to be very sensitive to touch; even the slightest hand contact gave the impression of sharp fingernails. Of particular interest was his widow's recent observation that “If I slightly knocked my finger, spontaneously showing him, he would immediately grasp his own finger and say “don't do that” (meaning not to show him); He actually felt it. If I merely commented (that I had knocked my finger), there was no such reaction”. In interview, she recounted other similar events. The experience was suddenly immediate and intense, and, apparently, qualitatively similar to the hypersensitivity occasioned by actual contact. She had initially contacted one of us (JLB) after hearing a radio broadcast by him of phantom limb phenomena, and wondered whether an analogous mechanism of some kind may have been operating with her late husband.

Although mirror motor neurons may be fundamentally important in learning to act, an adaptive role is far less obvious for perceiving another's pain. Perhaps during infancy avoidance of noxious stimuli is facilitated by early recognition of pain in others. Alternatively the phenomenon may merely be adventitious consequence of disruption of convergent sensory systems. Thus hyperalgesia, where a light touch induces an unpleasant sensation in the same person, is typically attributed to dysfunction of convergent sensory neurons in the neuraxis, though any of several CNS levels may be involved. However where, as here, a separate person is implicated, there may be additional limbic involvement, given the rather intensely emotional aversive aspects of the sensory experience.

Unfortunately no CT or MRI seem to have been performed of the brain, but it is probable that there was fairly widespread CNS involvement. He had also, apparently, experienced head trauma in the war. It would be of interest to know whether similar “allodynia” has been seen after known damage that includes left inferior cortex (opercular region), or the rostralmost region of the right superior parietal lobule.5 It would also be interesting to get persons, normal or hyperalgesic, to note reactions to noxious stimuli in others while judging the intensity of mildly aversive tactual stimuli they receive themselves.

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