Congenital Mirror Movements

J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

Journal of Neurology, Neurosurgery, and Psychiatry, 1981. 44, 586-599

Congenital mirror movements

G D SCHOTT AND MARIA A WYKE From the National Hospitals for Nervous Diseases, Queen Square and Maida Vale, London

S U MM AR Y In this report are described seven patients assessed clinically and neuropsycho- logically in whom mirror movements affecting predominantly the hands occurred as a congenital disorder. These mirror movements, representing a specific type of abnormal synkinesia, may arise as a hereditary condition, in the presence of a recognisable underlying neurological abnormality, and sporadically, and the seven patients provide more or less satisfactory examples of each of these three groups. Despite the apparent uniformity of the disorder, the heterogeneity and variability may be marked, examples in some of our patients including the pronounced increase in tone that developed with arm movement, and the capacity for modulation of the associated movement by alteration of neck position and bio-feedback. Various possible mechanisms are considered; these include impaired cerebral inhibition of unwanted movements, and

functioning of abnormal motor pathways. Emphasis has been placed on the putative role of the Protected by copyright. direct, crossed corticomotoneurone pathways and on the unilateral and bilateral cerebral events that precede movement.

Of the many forms of associated movements, presence of a neurological disorder-either con- mirror movements are those characterised by in- genital or acquired, and (3) that occurring spor- voluntary movements executed by one side of the adically in otherwise normal individuals.5 In this body which are mirror reversals with respect to paper, we wish to confine our observations to the intended movements. The term "mirror move- patients whose mirror movements date from ment" appears first to have been used by early childhood and in whom therefore the Bauman,' probably being derived from an analogy phenomenon appears to be congenital. with mirror writing.2 3 Certain mirror movements In 1977, we observed a 15-year-old otherwise such as smiling and blinking are obvious in every- healthy boy, who had throughout life shown in- day life; they are also features of normal child- voluntary mirror movements of the limbs. At hood motor function, as seen in the symmetrical that time it appeared that the movements he http://jnnp.bmj.com/ Moro response and in the posturing of the arms executed were similar to the apparently uniform that can be observed in children at around the descriptions of previous cases reported in the fifth month of life.4 literature. Since then, we have been able to study From the various types of pathological mirror six further patients who represent more or less movements, a particular group can be delineated satisfactory examples from each of the three which has the following characteristics: pre- groups referred to above. The purpose of the dominant or exclusive involvement of the hands, present report, in which these patients are pre- partial suppressibility, increase in the associated sented together with a resume of our earlier case, on September 29, 2021 by guest. movement with effort, and lack of progression is to draw attention to the hitherto unrecognised after childhood. We have classified this condition heterogeneity of the clinical features and to con- of obligatory bimanual associated movements into sider afresh possible mechanisms that may sub- three groups: (1) that occurring as a hereditary serve these rare bimanual synkinesias. disorder, usually with an autosomal dominant pattern of inheritance, (2) that occurring in the Patients and methods Address for reprint requests: Dr GD Schott, The National Hospital for Nervous Diseases, Queen Square, London WCIN 3BG. The case histories of the patients are given below, and Accepted 18 May 1981 summarised in tables 1 and 2. Patients were investi- 586 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

Congenital mirror movements 587 Table 1 Summary of clinical features

Case Sex Age (yr) Condition Investigations GROUP l-Familial I JG M 39 ? Recessive inheritance Normal GROUP 2-Congenital underlying disorder 2 DH M 41 Agenesis of corpus callosum CT scan-features of agenesis of corpus callosum 3 CW F 34 Klippel-Feil syndrome Radiographs-large foramen magnum, blocks of fused cervical vertebrae; myelogram-wide cervical canal, posterior arachnoid pouches 4 SA F 31 Usher's syndrome Abnormal electro-oculogram and electro-retinogram; audiogram -severe sensorineural deafness and loudness recruitment 5 SK F 17 Unidentified cranio-cervical anomaly Radiographs-spina bifida occulta of Cl, fused neural arches of Cl and 2, fused bodies of C5 and 6. (Normal myelogram) 6 LE F 30 Multiple cervical and thoracic Radiographs-malformed bodies and arches of C6 and 7, arches spinal anomalies of D2-5, and right 3rd and 6th and left 2nd, 3rd and 4th ribs GROUP 3-Sporadic 7 DC M 15 Normal Normal

Table 2 Mirror movements

Case Involvement Amplitude Mirror movements Alteration Otherfeatures on passive movement in tone

1 JG hands+ + arms+ L=R - + + + Partially suppressible with bio-feedback Protected by copyright. 2 DH hands + + arms+ L>R - eyes+ mouth+ 3 CW hands+ + arms+ R>L - - Movements influenced by neck position 4 SA hands+ + arms+ L=R - - eyes+ 5SK hands++toes± R>L - - Clumsyrighthand 6 LE hands+ + eyes+ L=R - + + Partially suppressible with bio-feedback toes+ 7DC hands++arms+ R>L + legs+ toes+ gated with radiographs of the skull and spine, com- Table 3 Neuropsychological Assessment puted tomography (CT) of the head, electroencephal- ography (EEG), and spinal and cortical sensory evoked Case Handedness Full scale Psychomotor performance potentials6 recorded over the ipsilateral and contra- IQ (WAIS) lateral scalp. The last tWo investigations were normal 1 JG Right 131 Normal in all patients; abnormalities detected and the results 2 DH Predominantly 72 Low normal http://jnnp.bmj.com/ right of additional abnormal investigations are included in 3 CW Right 102 Normal table 1. The patients were also given a neuropsycho- 4 SA Right 48 Clumsy and slow logical evaluation which included a handedness 5 SK Left 75 Clumsy and slow 6 LE Right 114 Normal questionnaire,7 tests of intelligence (WAIS), and tests 7 DC 83 of motor proficiency (cutting with scissors, maze trac- Left Normal ing, placing coins and matchsticks in a box, and drawing lines) taken from the Oseretsky Scale;8 psy- writing, but no definite mirror writing could be seen chomotor skills were evaluated using tests of rapidity when wtiting with the preferred hand alone. The of movemen'ts9 and the Perdue Dexterity Test.'0 The patients were also asked to perform "complementary" on September 29, 2021 by guest. results are sutnmarised in table 3. bimanual movements, that is tasks which required In assessing the movements, each hand was tested the simultaneous use of the two hands, as in winding independently and observations made concerning the thread onto a spool and threading a nut onto a bolt. direction of the associated mbvement (that is mirror In no patient was any associated or interfering move- or homologous, see reference 5). Most of the associ- ment noted. ated movements were mirror forms of the intended Two patients (JG and LE) attempted to control the movements, but at times they were less easy to involuntary movements using bio-feedback. The tech- characterise-as indicated in the case histories below. nique employed EMG feedback from the extensor When writing simultaneously with both hands, four muscles of the forearm showing the associated move- patients produced occasional and fragmentary mirror ment; feedback was both auditory using a tone of J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

588 G D Schott and Maria A Wyke varying pitch and visual using a calibrated meter. particularly the left, some associated closure move- TIhese patients were able to suppress the involuntary ments of the other eye also occurred. There was movements for a few minutes after continuous train- neither motor nor sensory deficit in the limbs, the ing for periods lasting up to 20 minutes. One patient reflexes were normal, and tone at rest, co-ordination (JG) was able to control the involuntary movements and fine and discrete finger movements were also of both the left and right hands; the other (LE) could normal. On movements of one arm, however, and only control the movements of the preferred hand. even even on anticipation of movement, striking in- Additional investigations were carried out on patient crease in tone in the opposite arm appeared, this DH (agenesis of the corpus callosum) in order to assess hypertonicity appearing poorly localised in the opposite possible impairment of inter-hemispheric transfer of limb. Discrete movements of the fingers of either information." The assessment disclosed no such im- hand produced mirror movements of the contralateral pairment; for instance, with eyes closed, objects fingers, whether the movements were made individu- actively explored with one hand could be recognised ally or in combination in more complex tasks such as by the other. writing and manipulating fine objects. Mirroring also occurred on movement of the hand and wrist, and to Case histories a small extent on movement of the forearm and even upper arm. The mirror movement was often less in Case 1, JG amplitude than the in'tended one, and could be par- This 39-year-old consultant for an electronics firm tially suppressed, usually being associated with further first recalled "clumsiness" of the hands when playing increase in tone. All synkinetic movements were en- with mechanical toys as a child. He was aware of hanced when the intended movement was carried out having difficulty carrying out intricate manoeuvres with effort. There was no n'oticeable asymmetry be- and his fingers appeared to move clumsily. By the tween the two sides, passive movements did not cause age of 8 years he recalled that his two hands in- mirroring, and there was no abnormality of the legs. voluntarily tended to move simultaneously. At the Protected by copyright. age of 14 years he started to learn to play the piano, Case 2, DH and whilst his problems probably did not progress, This 41-year-old waiter had three brief epileptic they became more obtrusive and the bimanual move- seizures, and at that time mirror movements first ments seriously interfered with this activity. As he attracted medical attention. Enquiry, however, re- became older, he became aware that many or most vealed that the patient had had mirror movements for of the movements performed with one hand were as long as he could recall. As a chlild he remembered faithfully copied in mirror fashion by the other- his mother encouraging him to sit on one hand to stop for example, putting his hand in his pocket, writing the other hand moving. He was almost illiterate, and and turning knobs. Finger and wrist movements were had little recollection of making mirror movements mainly affected with slight involvement of the fore- when trying to write. Everyday tasks proved difficult arms. Other than an irnability to play the piano, there on account of these movements: for instance lifting had been no interference with everyday activities in- a teapot with one hand resulted in the other hand cluding sport. The amplitude of the movements may becom'ing lifted up and making gripping movements. have increased during childhood and were enhanced Similar problems occurred holding jugs and beer mugs by stress and anxiety, but he had always partly been -a source of embarrassment in his occupation. Com- able to suppress the unwanted activity, albeit with bing his hair resulted in similar movements of the effort, and this appeared to impose a "strain" on other arm, also when he manipulated nuts and bolts http://jnnp.bmj.com/ both arms. It is possible that he involuntarily used and used a screwdriver. These fine, gripping and this increase in tone in an attempt to control the turning movements had been the most troublesome, mirrored movements. The face and legs were un- especially when effort was required, whilst no prob- involved. lems had been encountered with grosser movements He learnt to write at around the age of 4 years, such as hammering; he had been unable to control talked well at 3 and walked at 18 months. His his symptoms voluntarily. There was a greater ten- general health remained excellent. His only sibling, dency for mirroring to occur in the left hand with a brother, also exhibited mirror movements although intended movements of the righit, than vice versa. unfortunately details remain anecdotal since he There had been no progression and his legs and face on September 29, 2021 by guest. died aged 27 years in an accident. Throughout life were uninvolved. His previous and family history he had had difficulty in manipulating fine objects were unremarkable. on account of "stiffness" and "clumsiness" of the Examination was normal except for the presence fingers, and he showed non-progressive but very of mirror movements. These affected individual marked mirror movements affecting both hands. His finger movements-such as flexion and extension- parents and other relatives were unaffected and there and also more complex movements such as serial op- was no consanguinity. position of the thumb to each finger. There were Examination of JG showed slight synkinetic move- some mirror movements on opening and closing the ment upwards of the ipsilateral corner of the mouth fist, also seen with activities such as doing up buttons, on closing each eye; on voluntarily closing each eye, turning knobs and winding a watch. On forceful J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

Congenital mirror movements 589 movement against resistance, mirror movements affect- taps cause enhanced mirroring, and also a sense of ing shoulder abduction and adduction and also elbow diffuse strain mainly in the forearm muscles, as re- flexion and extension could be demonstrated; similar ferred to above. Forearm mirror movements particu- mirror movements could be brought out with gross larly occur when she stirs a cooking pot. Certain arm movements, for instance when insctibing circles activities have proven more difficult: when writing in the air with the outstretched arm or even with the she has developed the habit of making a fist with hand alone. When drawing in rungs of a ladder in a the left hand to prevent the unwanted movements. centrifugal direction, there resulted some slight mirror Some larger movements of the arm also tend to movements of the contralateral hand, and with at- cause mirroring-for instance catching a ball. Learn- tempts at writing with either hand, some low ampli- ing to play the piano had to be abandoned due to the tude involuntary movements were visible in the considerable difficulties encountered, and as a nurse, contralateral hand. There was some asymmetry of she tended to drop a vial held in one hand, when response, the right hand tending to mirror those the other hand was drawing-up fluid into a syringe. movements mtade with the left hand to a lesser Examination revealed a very short neck with low extent compared with when the right hand made the hair line, cervical kyphosis, restriction of all neck intended movement. In the face, whilst closure of movements to about 15 degrees, and webbing at the the right eye caused associated closure of the left shoulders. There was first degree horizontal nystag- eye, only slight associated movements of the right mus in both eyes on lateral gaze in either direct'ion; eye occurred when closing the left. Elevation of the in the left arm, there was slight weakness affecting left corner of the mouth caused some elevation of left shoulder abduction and elbow, wrist and finger the right side, whilst vice versa, more synkinetic extension. The arm reflexes were reduced bilaterally. movements occurred. The feet were unaffected. Tone There was neither sensory loss nor ataxia, and no remained normal throughout testing and passive move- signs of a foramen magnum lesion or spinal cord in- ments did not cause synkinetic movements. volvement. There were obvious mirror movements of

the fingers with particular involvement of the little Protected by copyright. Case 3, CW and ring fingers. The movements were not always This 34-year-old lady was born with a short neck but precisely mirrored and symmetrical: particularly remained asymptomatic until the age of 23 years. noticeable was that movement of a finger of the She then complained of episodes of tingling in the right h-and tended to produce some diffuse synkinetic left arm and leg, intermittent burning in the left movements affecting at times several fingers of the arm and slight impairment of grip of the left hand. left hand. Mirroring affected wrist movements, and Her family history was unremarkable. The findings also to a slight extent more gross movements of the on examination were similar to those currently ob- whole arm-such as when making circles in the air served. Although not having sought medical attention with the outstretched arm. Usually the amplitude of for this, mirror movements had been present for as mirroring produced by the right hand was greater than long as she could remember, and according to her that of the left. A striking finding was the increase mother had been present even during infancy. Thus and slowing of the mirror movements with forward when she had reached for an object with one hand, flexion of the neck, at a time when there was no the other hand would make a similar movement. The other demonstrable change in neurological function. patient remembered as a child mirror movements Synkinetic movements of the face and legs were not occurring, for instance when she did up buttons or seen. turned knobs; in one instance, she recalled that when http://jnnp.bmj.com/ scratching the side of her head with one hand, the Case 4, SA other produced a curious partial mirrored movement. This 31-year-old lady, the product of a pregnancy When aged 10 years, she tried to suppress the un- complicated by antepartum haemorrhage, was born wanted movement, although suppression caused con- uneventfully weighing 51b 10oz. Whilst the perinatal siderable and rather diffuse "strain" in the arm period was unremarkable, her developmental mile- showing the mirror movements. Over the years, she stones were markedly delayed. She crawled at 9 had unconsciously partly been able to control the mon'ths, walked at 2 years, and was slow to talk: her movements, although certain activities she still finds speech was almost unintelligible by the age of 5. At difficult-for instance plaiting her child's hair which 7 years she was noted to be deaf, and at 8 to be on September 29, 2021 by guest. involves different but simultaneous activity of the two partially sig'hted and bilateral cataracts were found. hands. Activities involving co-operative bimanual She had three grand mal seizures between the ages movements-such as sewing or manipulating nuts and of 5 and 23 years. She had never been able to read bolts, cause no difficulties. Affected movements are or write and had attended special schools; for a time mainly those of the fingers and wrist; over the years, she mianaged a simple assembly job in a factory. Her control has been executed predominantly over the family history was unremarkable and there was no thumb, index and middle fingers, and mirroring in parental consanguinity. Througout the patient's life, everyday life now particularly affects the little and her mother had been aware of the presence of mirror ring fingers. There is no asymmetry. Movements re- movements affecting the arms. The patient herself quiring effort such as undoing tight bottle tops or was able to recall few details of these movemen'ts J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

590 G D Schott and Maria A Wyke although she did remember their occurrence when particularly right sided weakness of both deltoids and she turned knobs on a radio; the movements had not spinati, triceps, wrist and finger extensors and the been progressive and caused no disability. small muscles of the hands. Movements of the hands On examination of this retarded girl, her visual were carried out slowly but there was neither ataxia acuity was 6/60 in the right eye and 6/36 in the left, nor disturbance of tone. The legs were normal. and there was tunnel vision, attenuated fundal vessels, Whilst the biceps and brachioradialis reflexes were retinal pigment epithelial degeneration and cataracts well preserved, the triceps and leg reflexes were in both eyes. There was severe bilateral deafness. In sluggish; the abdominal responses were absent but the the limbs there was neither weakness nor alteration plantar responses flexor. Sensory testing revealed in tone but slowness in executing fine finger and toe slightly impaired postural sense in the fingers bilater- movements bilaterally. There was no ataxia. Sen- ally. Mirror movements were also apparent. Active sation was normal, as were the tendon reflexes, and use of the left hand produced mirror movements of the plantar responses were flexor. A diagnosis of the right; thus tapping with a single finger, abduction Usher's syndrome'2 13 had been made. The face of the fingers, and pill-rolleing movements of the showed no abnormal associated movements, except fingers as well as gripping, pronation and supination of that she was unable to close either eye independently. the wrist, and more complex tasks such as undoing Mirror movements were evident in the upper limbs tops and turning knobs all produced symmetrical and especially the hands, and were particularly strik- movements of the right side. Attempting these move- ing on lateral finger movements and when more ments with the right hand produced less mirror move- complicated tasks were undertaken such as sequential ments of the left, and movements executed with the opposition of the thumb to each finger. There was a right hand frequently showed diffuse dispersal of the tendency for spread of discrete finger movements to mirror movements produced by the left hand. She involve adjacent fingers-for example, flexion of an had difficu'lty holding a pen, but writing with the index finger often caused flexion of the adjacent left hand produced marked mirror movements of

thumb as well as mirror movements of both these the right. Mirroring was not detected proximally in the Protected by copyright. fingers of the opposite hand. Attempts at writing upper arms but there was a suggestion of occasional, produced some synkinetic movements of the fingers slight and variable toe movements of the contralateral of the left hand. Slight mirroring also occurred proxi- great and second toes when rapid flexion-extension mally, particularly in the forearms when rotational movements of the toes of one foot were performed. movements were made. The legs were uninvolved. There was no alteration in tone on executing arm Case 6, LE movements nor with change in posture of the head. This 30-year-old-lady was born with a mis-shapen and shorter left foot and leg. This had caused little func- Case 5, SK tional disability but she had come under medical care This 17-year-old girl had had weak and clumsy hands as a result of some local pain in that foot. Her since birth; there had been a suggestion of progression family history was negative. Her parents had noted in recent years, probably attributable to increasing mirror movements since her birth, and as a young awareness as she started employment. The symptoms chiild, she recalled that when waving to people in the had always predominantly affected the right arm, street the other hand would make similar but less which she found difficult to elevate, and marked im- marked movements. As she learnt to write, she be- pairment in function of the right hand resulted in came aware of mirror movements of the left hand, almost exclusive use of the left. She had noticed and in particular releasing the grip of one hand http://jnnp.bmj.com/ longstanding difficulty in carrying out fine tasks such caused similar release movements of the other. Num- as writing, typing and in doing up and undoing erous activities were associated With mirror move- buttons. Born in India, she came to England at the ments, including turning door knobs, sewing, using a age of 5 years, started school a year later and after screwdriver and catching a ball. These movements leaving at the age of 16, she took up work as a shop resulted in embarrassment rather than functional assistant. Her family history was unremarkable. She disability. had been aware of mirror movements throughout life, Examination revealed slight weakness of neck although they caused her no concern. She had noticed flexion, elevation of the right shoulder, flattening of some asymmetry, with a greater tendency when using the interscapular region, thoracic scoliosis and marked on September 29, 2021 by guest. the left hand for the right hand to imitate movements pes cavus deformity of the left foot. There was slight than vice versa. weakness of all movements of the left hand and arm, Examination of this left handed girl revealed three which although causing no functional impairment, cafe-au-lait patches on the skin, and a small m'idline she had been aware of throughout life. There was pit in the back of the neck; the latter had apparently severe weakness of left ankle dorsiflexion and eversion been noted at birth. The cranial nerves were normal. and also toe dorsiflexion. Sensory examination was There was slight thinning of the muscles of the normal. The arm reflexes were normal and sym- shoulder girdle and small muscles of the hands, metrical, whilst the reflexes in the left leg were clawing of the fingers bilaterally but particularly the exaggerated, the left plantar response was extensor right, WVinging of the scapulae, and bilateral but and the left sided abdominal responses were reduced. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

Congenital mirror movements 591 Mirror movements were evident, and affected discrete and often bimanual movements which are not and fine finger movements of both hands, opposition necessarily strictly mirrored. Imitative, homo- movements of the thumb to each finger, and abduc- logous, and corresponding are alternative and less tion and adduction movements of the fingers. The restrictive terms sometimes used. 14 That this upper arms were not affected. When either arm was aspect is not merely semantic becomes evident used, marked increase in tone occurred in the contralateral arm, but this was not so striking as in JG. when considering that different mechanisms may There was no significant asymmetry. In the face, have to be invoked when considering explanations right eye closure was associated with involuntary for these movements. closure of the left eye, whilst left eye closure was Interest in associated movements in general first accompanied by only slight mirror movements of the developed during the 19th century (for historical right. There were some mirror movements of the toes review, see reference 14), but a century ago, of the right foot on flexion of the left toes. Passive Westphal15 delineated symmetrical synkinetic movements did not produce any mirror phenomena. movements as a specific group amongst these involuntary movements. The normal mirror move- Case 7, DC (Resume from Schott and Wyke5) ments of children and adults have been referred This 15-year-old boy had had involuntary mirror to earlier, but pathological mirror movements par- movements since infancy, his parents noticing that at ticularly affecting the hands are also seen both in the age of 3 years, picking up objects with one hand was associated with similar movements of the other. children'0 and in adults in many acquired dis- By the age of 7 years these movements were more orders of the nervous system, including cer- prominent and particularly affected gripping; the ebrovascular accidents,17 cerebral tumours,18 19 movements could only be suppressed partially and trauma,20 21 extrapyramidal disease22 23 and sub- were increased with effort. He found holding milk arachnoid haemorrhage.24 In this report, however, bottles in both hands was hazardous, since release of we have confined ourselves to a consideration of Protected by copyright. one bottle caused release of the other, and later rope some unusual patients whose bimanual mirror climbing, typewriting and piano playing had to be movements are congenital, and in some of whom abandoned. The mirrored movements when writing an underlying and relevant abnormality of the caused considerable embarrassment at school. There had been no progression over the years and medical nervous system has been detected. advice was only sought because difficulty was antici- Despite different underlying disorders, the seven pated in the boy's aspirations to become a diamond cases described here share the characteristic cutter. The family history was unremarkable. features that have long been recognised in this Examination was normal except for the presence condition: the movements affect solely or pre- of mirror movements, which spared the face. Indi- dominantly the hands and especially the fingers, vidual finger movements and more complex move- are present on active and rarely passive movements of the hands produced mirror movements of ments of one side, are noted during infancy and the contralateral side, although the mirrored movements were more evident when the left hand wvas show no significant progression, and are them- carrying out voluntary movements. Less mirroring selves associated with no other functional deficit occurred on more proximal movements of the arms. unless an underlying neurological disorder should Passive movements of the fingers and wrist, and pro- contribute additional handicaps. Often the mirror http://jnnp.bmj.com/ nation and supination of the forearm, especially when movement is of a lesser amplitude than the in- abruptly executed, sometimes produced similar tended one, and there is no doubt that some degree though small amplitude mirror movements. In the of voluntary control can be exerted over the legs, slight mirror movements were detected on vol- associated movement. These associated movements untary movement of the toes or ankle. All associated of the voluntary movements were enhanced when active movement was may often be only a fragment performed against resistance. movement and sometimes do not even resemble it; this explains for instance why when writing, mirror writing is not inevitably produced by the on September 29, 2021 by guest. Discussion non-dominant hand, and also demonstrates the lack of precision of the term "mirror movements" Although the term "mirror movements" is em- when applied to these patients. ployed to describe those involuntary movements The functional problems these movements cause executed by one side of the body which are are usually insignificant; curiously, typewriting mirror reversals with respect to the intended and playing the piano are often impossible,25 movements, usage has tended to lead to a less whereas sewing, manipulating nuts and bolts, and strict application of the meaning of the term, and other fine mechanical tasks appear to present few in many instances it is used to imply simultaneous difficulties. It may be that this is because activities c J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

592 G D Schott and Maria A Wyke such as piano playing demand independent and movements, and in four patients some associated separate activity of the two hands, whilst many of movements of the eyelids or mouth were noted. the other tasks require independent yet bimanually The latter as with many other associated facial co-ordinated ac'tivity. Other curious and predict- movements34 are commonly found in otherwise able problems have been noted-in one of our normal individuals and likely to be of little sig- patients (Case 7) difficulties were encountered nificance. As well as the various differences in when carrying bottles of milk in each hand, and the clinical features, the underlying conditions in the problems encountered by the sailor attempting some patients include a number of more or less to climb a rope can easily be envisaged.26 It is identifiable disorders, an aspect which needs to be noteworthy that only one of the seven cases des- accoun'ted for when attempting to construct any cribed here came to medical attention on account unifying hypothesis to explain these abnormal of these movements, which demonstrates the lack movements. of both progression and of the development of further neurological problems. CONSIDERATIONS OF UNDERLYING ABNORMALITIES Mirror movements have been investigated by Abnormalities of the cervical spine electromyograplhic (EMG) techniques for many The commonest condition recorded in association years,27-30 but detailed reports of patients with with congenital mirror movements has been the congenital mirror movements studied by current Klippel-Feil syndrome, in which numerous associ- EMG techniques are sparse. Regli, Filippa and ated developmental defects such as Sprengel's Wiesendanger31 analysed mirror movements in deformity, platybasia, and extradural spinal masses two brothers: EMG investigation of rapid flexion may occur, as also may defects of the cervical movement of the forearm revealed activity in the and thoracic cord.35 Mirror movements were first contralateral arm with coactivation of the antag- noted in this congenital cervical spine abnormality Protected by copyright. onistic muscle pair. Whilst the latency of the by Bauman,' who reported on their occurrence in activity was often the same on the two sides, on four out of six cases, and although the association average the latency of the mirror activity was has been questioned,36 several other confirmatory slightly longer, and Jelasic and Ott'9 reached reports have subsequently appeared (see reference similar conclusions studying patients with mirror 37). Mirror movements have also been described movements who were otherwise normal. Baird, in other congenital skeletal abnormalities of the Robinson and Buckler32 studied mirror movements craniocervical region, such as the Arnold-Chiari electromyographically in patients with the Klippel- malformation and basilar impression.38 The pro- Feil syndrome; although the association between pensity for mirror movements to occur in these the syndrome and mirror movements was highly conditions is unexplained. Of considerable im- significant, the presence of mirror movements portance are the pathological studies in two cases could not be correlated with any clinical or radio- of the Klippel-Feil syndrome associated with logical features. Notermans, Go and Boonstra33 mirror movements in which striking abnormalities have also studied mirror movements using EMG of the cervical cord have been demonstrated. In in a patient with the Klippel-Feil syndrome. Whilst the case described by Gunderson and Solitare,39 http://jnnp.bmj.com/ of interest, these reports have contributed rela- apart from the apparent absence of pyramidal de- tively little to an understanding of underlying cussation with defects of cord fusion, the corpus mechanisms, and when EMG studies were under- callosum was found to be abnormally thin. In taken on our patient DC, we were impressed by Avery and Rentfro's40 case, there was nearly com- the great variability of the response evoked in the plete division posteriorly of the cervical and upper contralateral muscles. thoracic cord, but unfortunately the brain was Despite the apparent uniformity of the clinical not examined. features, our cases demonstrate a heterogeneity A possible mechanism that has been considered on September 29, 2021 by guest. barely recognised in the literature on the subject. by many of these authors is that of impaired de- For instance, there was often asymmetry between cussation of the pyramidal tracts, perhaps with the movements of the two sides, in two of our consequent use of alternative, less specific and cases there was very pronounced increase in tone bilateral pathways. In the present report, two when the mirror movements were produced, in patients had unequivocal major skeletal abnor- three cases slight associated movements of the malities of the cervical and upper thoracic spine toes could be observed, in one patient the move- with a probable abnormality of the underlying ments were markedly affected by head posture, cord, and a further patient had clinical evidence in another passive movements induced mirror of a high cervical lesion with a congenital mid- J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

Congenital mirror movements 593 line cutaneous abnormality-the underlying defect a common basis for the occurrence of mirror remaining unidentified. In some instances, mirror movements. movements may be inherited (see below) and it In considering structural aspects, reference should be recalled that certain abnormalities in should be made to the apparently unrelated com- the region of the craniocervical junction may bination of mirror movements with hypogonado- themselves be inherited, including the Klippel-Feil tropic hypogonadism and anosmia. This triad has syndrome,41 basilar impression42 and the Arnold- recently been reported as a familial disorder by Chiari malformation.43 Conrad, Kriebel and Hetzel,37 and possible earlier examples cited. These authors proposed that hypo- Agenesis of the corpus callosum gonadism and anosmia (Kallman's syndrome) may Whether mirror movements take place via inter- arise from a developmental dysraphic state- hemispheric pathways has long been debated, but analogous to for example the Klippel-Feil syn- evidence on this is lacking. It is of interest, how- drome-and thus all the known structural dis- ever, that callosal section does not appear to orders seen with mirror movements appear to prevent at least those mirror movements acquired share a defect of midline structures, perhaps with through trauma.44 The occurrence of these move- attendant abnormalities of neural topography. ments in agenesis of the corpus callosum has attracted little attention even when noted." Our Mental retardation observation of a patient (Case 2) who presented It is well recognised that the bilateral associated fortuitously, whose callosal agenesis would have movements which are a normal feature of infancy remained undetected without computed tom- are more likely to persist in brain damaged chil- ography and in whom no other neurological ab- dren,47 48 and mirror writing is also more com- normalities were encountered, raises the question monly encountered among "defective" children.49 Protected by copyright. as to whether previously reported "normal" indi- Non-specific "brain damage" appears to allow viduals with mirror movements who were not mirror movements to persist indefinitely, and this investigated by such techniques, may have had an was recognised by von Fragstein50 who commented undetected abnormality of this kind. The associ- on these movements in "idiots"; the movements ation of the Klippel-Feil syndrome with an ab- have also been described in hereditary mental normally thin corpus callosum has been referred defectiveness,45 hereditary schizophrenia,5' and to above. Also pertinent is the agenesis of the "phenylpyruvic oligophrenia".52 In our patient corpus callosum detected in one member of a with Usher's syndrome, mirror movements ap- family with mirror movements, mental retarda- peared in a setting of multiple congenital defects tion and various skeletal abnormalities.45 of which mental retardation was one major mani- festation. There has been speculation that the Is it possible to link the two groups of patients disappearance of normal mirror movements might in whom an underlying defect can be demon- be related to the of strated, that is those with abnormalities of the development a hypothetical corpus callosum and of the cervical spine and "inhibitory" mec'hanism which would allow

separate, individual and non-mirror movements to http://jnnp.bmj.com/ cord? Apart from the necropsy findings referred occur. This hypothesis, and the possibility that to above, agenesis of the corpus callosum is ac- inhibition may fail to develop in patients with companied by a remarkably high incidence of mental retardation and aggression,53 are discussed associated anatomical abnormalities, and particu- later. larly striking is the study by Parrish, Roessmann and Levinsohn46 in which six of 11 patients with FAMILIAL AND SPORADIC CASES agenesis of the corpus callosum were found to In these two groups, patients with congenital have abnormalities involving the pyramidal sys- mirror movements have no detectable abnormality tem. In their review of the literature, associated of the nervous system. The inclusion of our case on September 29, 2021 by guest. pyramidal tract abnormalities were reported in JG as an example of familial mirror movements six of 47 other cases, which they considered to be must remain unsatisfactory, as we were unable an underestimate. It seems reasonable therefore to assess the reportedly affected brother. How- to suggest that as mirror movements may be ever there seems no reason to doubt that both associated both with agenesis of the corpus callo- brothers were similarly affected, and we are aware sum and with congenital cervical spine abnor- of 18 reports of familial mirror movements affect- malities, and as there is a high incidence of ing 86 individuals (see reference 37). The usual abnormalities of the pyramidal tracts in both dis- mode of inheritance is as an autosomal dominant, orders, abnormalities of these tracts may provide although Lackner54 described a family with a less J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

594 G D Schott and Maria A Wyke well defined pattern of inheritance, and Rasmussen clinical movements by various techniques, includ- and Waldenstrom55 reported a patient with mirror ing plethysmographyll and EMG.27 62 movements whose healthy parents were first cousins and where an autosomal recessive mode Inhibitory mechanisms of inheritance was postulated. It may be, there- Those early theories concerning inhibition and fore, that there is heterogeneity amongst the referred to above envisaged that with normal fanmilial cases, although inheritance as an auto- matura'tion, an inhibitory centre or mechanism somal dominant condition is the most common. develops which allows individual, separate and Of particular interest in our case is the striking non-synkinetic movements to occur. There is some hypertonicity developed by the limbs in the evidence for the presence of such a process. For presence of mirror movements; whether this example, left handers probably naturally write in characteristic is typical of familial cases is not mirror script from right to left, and it is edu- known, although it was a feature of one of cation and cultural influences which tend to cause Lackner's54 two cases. conventional script to supersede.63 Moreover, The familial incidence of a number of cranio- inhibition can apparently be overcome in right cervical abnormalities in which mirror movements handers, who when obligatorily taking up writing may occur has already been referred to, and and other activities with their left hand, may then these abnormalities are usually inherited as auto- transiently undertake mirror movements almost somal dominant conditions. Agenesis of the cor- unaware.64 Thus it seems that inhibitory mech- pus callosum may also be inherited, and both anisms may be continuously active but are capable autosomal dominant and recessive patterns have of being removed. been described.56 Whether there is a specifically There are two other aspects relevant to theories inherited abnormality of motor pathways is un- of inhibition which require comment. First, con- Protected by copyright. known; it is of interest, however, that at least in cerning movement-related cortical potentials, it the peripheral nervous system, familial patterns of has long been recognised that with unilateral hand anomalous innervation have been described, the movement, the first EEG activity prior to move- mode of inheritance again proebably being as an ment, the readiness potential or Bereitschafts- autosomal dominant.57 potential, is diffuse, bilateral and symmetrical, and Since the first obscure description by Thomayer the last pre-motor potential to be recorded is in 1887,58 59 nine patients have been reported in restricted to the contralateral hand area of the whom mirror movements occurred as a non- motor cortex (for references, see 65, 66). The familial condition in the absence of any identifiable intervening potentials are currently being evalu- associated neurological or skeletal abnormality.5 19 ated, and whilst controversial,62 these may include It should be emphasised that in the majority of an ipsilateral pre-motion potential ("P1") which these cases which we have termed sporadic, nor- it has been suggested may be related to inhibitory mality was assessed on clinical grounds. The case activity of ipsilateral pathways.67 Second, infor- (Patient 7) described by us and summarised above mation obtained from vascular studies indicates has been the only one in this group to have been that there is increased blood flow in both supple- http://jnnp.bmj.com/ investigated by modern techniques, now a pre- mentary motor areas during the programming and requisite for inclusion in the group of otherwise execution of individual finger movements, but in- normal individuals. creased regional blood flow in only the contralateral primary motor area.68 The parallel in- MECHANISMS OF CONGENITAL BIMANUAL MIRROR formation from these two different types of study MOVEMENTS raises the question as to whether some form of All theories which attempt to explain these move- inhibition or modulation may be occurring be- ments must account for why the movements affect tween early bilateral cerebral activity and later on September 29, 2021 by guest. solely or predominantly the hands and fingers, contralateral cerebral activity-inhibition which commence during early life and do not progress, could be abnormal in patients with mirror and may be partially suppressible. The theories movements. should also account for the fact that although the Functional considerations also point to the same bimanual synkinetic movements normally separation between diffuse bilateral and discrete occur in children and then disappear during the contralateral cerebral activity. In man, at least first or second decade,47 48 60 they may occasionally in respect of the limbs, focal stimulation of the be seen on extreme effort in healthy adults, and motor cortex results in purely contralateral move- can be demonstrated in normal people as sub- ments. This is evident in the normal subject J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

Congenital mirror movements 595 with stimulation through the intact skull,09 in Currier70 is of particular importance in this con- patients with focal motor epilepsy, and at surgery text. A patient with congenital and familial mirror on the exposed cortex;70 indeed, Penfield and movements sustained a cerebral infarction leading Jasper70 state "bilateral representation of move- to a right hemiplegia; mirror movements persisted ment of either extremity does not exist in man in the hand which'otherwise remained completely as far as our experience of Rolandic stimulation flacc'id and paralysed. It seems unlikely that these goes." (Unfortunately information at present is movements could be due to activity of the left lacking on the effect of percutaneous stimulation hand motor cortex and Haerer and Currier postu- of the motor cortex in patients with mirror move- lated that the movements of the right hand arose ments.) These abnormally-induced movements either from the right (ipsilateral) cortex or distant which follow direct stimulation of the motor subcortical structures, and that mirror movements cortex are, however, clearly different from the in general might be caused by distribution of normal, programmed and sometimes deliberate cortical motor neurones from each hemisphere to movements presumably generated deeply, diffusely each "cervical cord hand area" in association with and bilaterally and in which the supplementary incomplete pyramidal decussation. It should be motor areas become activated; which if either of emphasised that the nature of anatomical abnor- these mechanisms is pertinent to mirror move- malities in patients with mirror movements re- ments remains unknown. mains virtually unknown. It is difficult, however, These aspects leave unanswered why the ab- to envisage how the variability of the movements normal movements affect the hands and fingers, could occur in the presence of gross abnormalities usually in the absence of any defect of fine finger or lesions affecting motor pathways, particularly control or discrete finger movement. Theories of when impairment of motor function rarely occurs. inhibition also need to explain the heterogeneity, The relation between mirror movements and Protected by copyright. variability, and partial suppressibility of the move- position of the neck in our patient (case 3) is of ments, and the effect of passive movements in in- interest, since it suggests a possible mechanical ducing contralateral movements. Such passively- factor altering the function of motor pathways induced associated movements were present in specifically at that level. one of our cases, and have been described in other The complexity of the motor pathways needs no reports, for instance by Drinkwater7l and Gutt- emphasis. There is considerable anatomical vari- man, Maclay and Stokes.72 Presumably focal ation of these pathways in man,77 and of particular afferent impulses trigger contralateral motor path- importance is one of the conclusions reached from ways but there is no evidence, apart from the Nathan and Smith's78 later study: the lateral questionable73 case reported by Drinkwater,7' of corticospinal tract of each side has bilateral in- allocheiria or any other phenomena affecting the fluences. In the following section, some aspects sensory system in patients with mirror movements. related to specific corticospinal pathways will be The effect is presumably linked to localised sen- considered. sory pathways since only the contralateral part is activated following passive movement; the appli- A hypothesis combining mechanisms of inhibition http://jnnp.bmj.com/ cation of studies on cortical motor potentials fol- and abnormal pathways? lowing both voluntary and passive finger move- A satisfactory explanat'ion for congenital mirror ments74 to patients with mirror movements may movements may lie in an abnormality affecting prove revealing. the important direct, crossed corticomotoneurone pathways, w'hich-at least in primates-are now Abnormal pathways firmly established as being fairly specific for move-

A second major concept invoked has been that of ments of the hands and in particular for the on September 29, 2021 by guest. abnormal descending motor pathways. Abnormal- execution of fine finger movements.79 80 These ities of the corpus callosum and of pyramidal de- direct and crossed pathways develop relatively late cussation in the cervical region have been con- and coincide with the acquisition of motor skills8' sidered above; other theories involving neural -both crucial aspects when explaining congenital topography have also been considered, including mirror movements. In those of our patients whose inhibition of bilateral cerebral representation.20 mirror movements arose in a setting of recognis- loss of suppression of bilateral activity,75 impaired able abnormalities, a common factor might well inhibitory function of the parietal lobe,2' 24 and comprise an abnormality of these specific path- use of ipsilaterally projecting corticospinal pathways. Consistent with the use of the direct corti- ways.31 37 71 The case reported by Haerer and comotoneurone pathways is neuropsychological J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

596 G D Schott and Maria A Wyke evidence, which also suggests that abductive move- part of the movement disorder. It could even be ments-probably relevant for fine and individual that alterations of tone are relevant to the partial finger control-are subserved by the contralateral suppressibility of the mirror movements, and the hemisphere and may be mediated by these crossed influence of mood and relaxation on the fluctu- motor neurones.82 An abnormality affecting, for ation of discrete movements of the hands in dis- instance, decussation of these pathways in the orders such as writers' cramp will be recalled. brain or cervical cord must however remain In addition, whilst the mode of action of bio- speculative. feedback remains unclear, the technique has for If the direct, crossed corticomotoneurone path- long been used clinically to inhibit unwanted ways are implicated in mirror movements, can in- motor activity;85 it is of interest that two of our hibition of these pathways be demonstrated? It patients very rapidly learnt to diminish their is of interest that our patients were able to under- mirrored movements transiently utsing bio-feedback take everyday activities without difficulty when -which perhaps argues in favour of effects on the two hands were employed together, and simi- diffuse possibly subcortical mechanisms. larly we did not observe associated movements in That a disturbance or anomaly of higher cor- any of our patients when both hands were used tical function could play a part in bimanual move- co-operatively, which suggests that inhibition may ments also requires consideration but appears un- be occurring at least in these circumstances. In likely,86 and we believe can be dismissed. In our this respect the observations made by Jung and patients there was no close association between Dietz85 are of relevance. They found that whilst mirror movements and intellectual ability or motor there was a unilateral prolongation of motor skill. Finally, we do not consider handedness to be relevant; two of our seven cases were sinistrals latency in affected muscles of patients with dis- Protected by copyright. orders affecting one pyramidal pathway, this delay and the movements seen were no different in these in initiation of voluntary movements disappeared patients. when movements were made bilaterally. They considered the best explanation was the use of ipsi- We are grateful to Dr MFT Yealland, Dr KJ lateral projections of uncrossed pyramidal fibres Zilkha, Professor WI McDonald and Professor to the motor neurones. Recalling that the readiness CD Marsden for permission to publish details of potential and cerebral blood flow in the supple- patients under their care. We are also indebted mentary motor areas are bilateral, inhibition of to the Department of Clinical Neurophysiology these ipsilateral pathways perhaps usually occurs, for the somatosensory evoked potential studies. the inhibition only being removed or circumvented by bilateral movements. There is some further References evidence which might support this proposal. 1 Bauman GI. Absence of the cervical spine: Mention has already been made of the contro- Klippel-Feil syndrome. JAMA 1932; 98:129-32. versial movement-related pre-motion potential 2 Eilenmeyer A. Die Schrift: Grundzuge ihrer ("P1") which is ipsilateral to the voluntarily con- Physiologie und Pathologie. Stuttgart: A Bonz, http://jnnp.bmj.com/ tracting muscles; of interest is the observation 1879. that on bilateral movement of the thumb, Shi- 3 Critchley M. Mirror-writing. London: Kegan basaki and Kato67 could not record this ipsilateral Paul, Trench, Trubner & Cio, 1928. potential, and they suggested that it might indeed 4 Gesell A, Amatruda CS. Developmental Diag- be related to inhibition of imitative (mirror) nosis: Normal and Abnormal Child Development, movements. 2nd edition. New York: Paul B Hoeber 1947, Chapter 3:37; Chapter 11:190. The relevance of the alteration in tone noted in 5 Schott GD, Wyke MA. Obligatory bimanual

two of our patients is uncertain. Whilst clinical associated movements. J Neurol Sci 1977; 33: on September 29, 2021 by guest. disorders of the basal ganglia and cerebellum are 301-12. not typically accompanied by mirror movements, 6 Lecky BRF, Murray NMF, Berry RJ. Transient rormal movement is preceded by diffuse neuronal radiation myelopathy: spinal somatosensory activity in cerebellar structures, thalamus, and evoked responses following incidental cord ex- basal ganglia (for reviews, see references 65 and posure during radiotherapy. J Neurol Neurosurg 84). Whether the striking increase in tone pre- Psychiatry 1980; 43:747-50. 7 Harris AJ. Harris Tests of Lateral Dominance. ceding hand movement in our patients is related New York: The Psychological Corporation, 1974. to activity from these more diffuse extrapyramidal 8 Doll EA. (ed) The Oseretsky Tests of Motor Pro- pathways remains unknown, also whether the ficiency. Minnesota: American Guidance Service abnormality of tone results from or is an inherent Inc, 1946. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.44.7.586 on 1 July 1981. Downloaded from

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