Brain (1991), 114, 2203-2233
THE NEUROLOGY OF OBSESSIONAL SLOWNESS by N. HYMAS, 1 A. LEES, 2 D. BOLTON, 3 K. EPPS 3 and D. HEAD3 (From 'Fulbourn Hospital, Cambridge, the 2National Hospital for Nervous Diseases, Queen Square, London, and the ^Institute of Psychiatry, London, UK)
SUMMARY
INTRODUCTION
Obsessions are recurrent, persistent ideas, thoughts, images or impulses that are experienced as involuntary, senseless or repugnant. Attempts are made to ignore or suppress them. Compulsions are repetitive and seemingly purposeful behaviours that are performed according to certain rules or in a stereotyped fashion. The act is performed with a sense of subjective compulsion often coupled with a desire to resist the compulsion. The individual usually recognizes the senselessness of the behaviour and does not derive pleasure from carrying out the activity, although it often provides a release of tension (American Psychiatric Association, 1980). This is theme from which are woven all those many variations of individual psychopathology to be found under the general rubric of Obsessive-Compulsive Disorder (OCD). Common obsessions concern violent urges towards the self or others, fears of contamination of self or others, or doubts about past actions or events. Common compulsive rituals involve cleaning, counting, checking, touching or avoidance (Dowson, 1977; Stern and Cobb, 1978; American Psychiatric Association, 1980). In recent decades it has not been customary to try to understand such symptoms and behaviour as manifestations of cerebral dysfunction. Indeed, in systems of psychiatric nosology such as DSM-III (American Psychiatric Association, 1980) or ICD-9 (World Health Organization, 1978), the absence of demonstrable brain disease was a criterion by which the syndrome of OCD was defined. Classified as a 'neurosis', it took its place alongside a variety of other disorders which, according to contemporary usage of the term, were often thought to be best approached primarily with the languages and concepts of dynamic psychology or sociology and with little reference to those of physiology or clinical neurology. Correspondence to: Dr Nigel Hymas, Fulbourn Hospital, Cambridge CB1 5EF, UK. © Oxford University Press 1991
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Seventeen of 59 patients admitted to hospital for treatment of Obsessive-Compulsive Disorder (OCD) were found to have significant slowness, mainly due to difficulty in initiating goal-directed action and suppressing intrusive and perseverative behaviour. In this subgroup subtle neurological abnormalities were found more frequently than in healthy controls and included loss of motor fluency, hesitancy of initiation of limb movements, speech and gait abnormalities, cogwheel rigidity, complex repetitive movements and tics. Difficulties in cognitive set-shifting and complex spatial-and-shifting abilities were found on neuropsychological testing, but no correlation was found between these disturbances and either the degree of obsessionality or the severity of motor dysfunction. These results suggest that patients with obsessional slowness may have a dysfunction in the frontal-basal-ganglia loop system.
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However, since Esquirol in 1838 described a patient under his care who displayed some of those particular features of behaviour and experience which subsequently came to be termed 'obsessive-compulsive disorder' (Esquirol, 1838), there has existed a current of observation, thought and speculation which has always sought to convey, alongside descriptions of a purely psychological nature, the relevance of neurological mechanisms (Hymas and Prasad, 1989). Pierre Janet, for example, whose descriptions of the syndrome must remain unsurpassed in their comprehensiveness, elegant clarity and attention to psychological nuance, nevertheless perceived the provisional and partial nature of his psychological formulations, and believed them to be paving the way to a future anatomical understanding (Janet, 1903). Janet's awareness and acknowledgement of the importance of the biological and neurological aspects of the syndrome, and the similar awareness shown by contemporaries such as Tuke (1894) or Jackson (1895), perhaps reflected the shared concepts of neurology and psychiatry, and the easy commerce of ideas which existed between their practitioners, in the latter half of the 19th century (Bynum, 1985; Dowbiggin, 1985). The subsequent impact of Freudian ideas led to, or at least was an expression of, a divergence of viewpoints which increasingly persuaded psychiatrists to divorce mental illnesses such as obsessive-compulsive disorder from the neurological context of earlier understanding. The 'neuroses' assumed an autonomy as 'functional' psychological disorders (Berrios, 1985) and became freed from those connotations of central nervous system disease which had been implicit in earlier conceptions of the term (Hunter, 1973; Bynum, 1985; Rogers, 1987). The literature on OCD tended, thereafter, to remain predominantly psychological in emphasis. However, in the first half of this century, speculations concerning the cerebral basis of the syndrome continued. Such ideas were especially fuelled by the observation of obsessive-compulsive phenomena in patients suffering from neurological disorders. The outbreaks of epidemic encephalitis which had swept Europe and North America at the end of the First World War and throughout the following decade (Greenfield, 1976) had been of particular importance in yielding many reports of obsessions and compulsions associated with the syndrome of post-encephalitic parkinsonism (e.g. von Economo, 1931). Obsessions and compulsions associated with epilepsy (e.g. Brickner et al., 1940) and tic-disorder (e.g. Creak and Guttman, 1935) were also reported, and within the limits of contemporary knowledge attempts were made to interpret both the neurological and the psychiatric disturbances in terms of shared cerebral mechanisms. Schilder, for example, in his study of 1938 referred to the association of obsessivecompulsive phenomena with epidemic encephalitis earlier in the century and argued for a close relationship between the neurologically-based disturbances of motility seen in these patients and their particular psychiatric symptoms (Schilder, 1938). He estimated from his clinical experience that in obsessional patients, without any history suggestive of encephalitis, 'organic' signs could be found in about a third of cases, and that in a further third the symptomatology aroused the suspicion of an organic background. The signs that Schilder observed included: rigidity of the face, flexor rigidity of the arms, tremor, impaired eye convergence, great urge to talk and propulsive features in speech, and what he called 'motor urges of a higher degree'. A renewed interest in the importance of these earlier observations to the study of
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obsessive-compulsive disorder can be discerned in some recent publications (Laplane etal., 1981, 1984; Yaryura-Tobias and Neziroglu, 1983; Cummings and Frankel, 1985; Ward, 1988). Furthermore, some more recent studies have attempted to generate 'biological markers' of the disorder, or of subgroups within it. However, few investigations have proceeded from coherent hypotheses concerning brain-behaviour relationships, and few have attempted to explain the phenomena of OCD in terms of phenomena displayed by patients, or experimental animals, suffering from cerebral disorders whose mechanisms may be better understood (Hymas and Prasad, 1989). Against this background, the comparatively recently described phenomenon of 'obsessional slowness' gains particular interest. Many patients with obsessive-compulsive disorder complain of slowness in carrying out their ordinary, day-to-day activities, a slowness which may sometimes be profoundly incapacitating (Marks, 1978). It is commonly thought to be the result of the performance of rituals and has attracted little attention in its own right. Indeed, in standard textbook descriptions of the disorder, for example, those by Slater and Roth (1969), Ey et al. (1974) or Rado and Monroe (1974), it receives no explicit mention. In 1974 Rachman described what he termed 'primary obsessional slowness' (Rachman, 1974). His report was based on the characteristics of 10 patients who showed severe slowness in the execution of the simple tasks of daily living, such as dressing, bathing or eating. His descriptions, however, leave some uncertainty about the precise phenomenon he was attempting to identify. On the one hand, he notes that particular care was taken to exclude patients 'in whom slowness was plainly a secondary consequence of extensive checking or other rituals', yet elsewhere states that 'needless to say, all 10 of the patients were carrying out some checking behaviour'. On the one hand, he describes that the patients resembled a 'slow motion movie', yet on the other that 'slow motion of the limbs seemed to play no part in their overall slowness'. Rachman explains the slowness psychologically in terms of 'meticulousness', and without reference to the brain. Our own interest in obsessional slowness was kindled by the close observation of a patient who demonstrated the phenomenon to a marked degree. This 25-yr-old man, who suffered from a compulsion to touch things and repeat actions, would take hours over the most ordinary of activities such as having a bath or dressing. His slowness seemed to derive from a difficulty in initiating simple movements, in shifting between and sequencing different patterns of movement, and in performing more than one movement simultaneously; his goal-directed behaviour was continually disrupted by the perseveration of unwanted movements and by an extreme distractability to random visual stimuli; a further striking feature was the inefficacy of his verbal monitoring in modifying and directing his behaviour. The patient, therefore, showed a number of deficits of motor performance and control reminiscent of some of those seen in, for example, frontal lobe disorders, or Parkinson's disease in which a dysfunction of basal ganglia and possibly also of frontal lobe mechanisms is believed to be important. This background was felt to justify a prospective investigation of a series of prominently slow obsessive-compulsive patients using a design which would expose some of those motor and cognitive deficiencies seen in patients suffering from dysfunction of the frontal lobes of the brain and their subcortical connections.
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Assessments Assessments consisted of an initial screening procedure followed by the further study of patients showing slowness. Initial screening All patients were asked to complete the Maudsley Obsessional-Compulsive Inventory (MOCI) (Hodgson and Rachman, 1977), and the self-administered written form of the Leyton obsessional inventory (LOI) (Cooper, 1970; Snowdon, 1980). These are two widely used methods of assessing the existence and extent of obsessive-compulsive complaints. In order to simplify the administration of the questionnaires, the questions relating to resistance and interference in the Leyton inventory were omitted. All patients were also asked to complete a slowness questionnaire which had been devised for the study. Slowness questionnaire. This self-administered questionnaire is shown in Fig. 1. It lists 20 common items of behaviour. The subject is asked to rate the speed of his or her own performance of each item in comparison with an average person. The scoring method is shown on the questionnaire. The maximum possible score is 60, corresponding to the maximum severity of subjective slowness. A pilot study was conducted to establish the score above which 'slowness' would be defined as present. The questionnaire was administered to 6 obsessive-compulsive patients in whom slowness in day-to-day activities was a prominent and disabling feature. Patients in this group often complained of having to take several hours over such routine tasks as dressing, eating a meal, washing or bathing. Their results were compared with a group of 11 other obsessive-compulsive patients not showing this feature to a marked degree. The mean score of the slow group was 38.3 (SD 7.2, range 30-47), and that of the non-slow group 12.2 (SD 8.8, range 3—29). A score of 30, which lay approximately 2 standard deviations above the mean of the non-slow group, was chosen as the criterion score above which a significant degree of slowness in day-to-day activities was to be defined as present for the purpose of the study.
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Subjects Patients. Patients were recruited from the Behaviour Therapy Unit of the BethJem and Maudsley Hospital, London. Between November 1985 and April 1988 all patients referred to the unit for inpatient assessment and/or treatment of obsessive-compulsive symptoms and behaviour were screened at the time of their first attendance or admission. In all cases the diagnosis of OCD was made according to DSM-111 guidelines (American Psychiatric Association, 1980). However, in view of the potential interest of patients who might show a conjunction of this particular psycho-syndrome and a 'neurological' disorder, the exclusion criteria of the presence of Gilles de la Tourette syndrome or 'organic mental disorder' were ignored. This matches the subsequent revision of DSM-111 (DSM-111-R, American Psychiatric Association, 1987). In all cases the obsessive-compulsive symptoms and behaviours constituted the leading feature of the psychiatric picture and formed the principal reasons for the patient's referral. Fifty-nine patients were screened of whom 32 were men, with a mean age of 35.2 yrs (range 17 — 73, SD 14.49), and 27 were women, with a mean age of 33.5 yrs (range 2 1 - 6 5 , SD 11.5). Two other patients who fulfilled this study's diagnostic criteria for obsessional slowness (see below) were also included. The first was the 25-yr-old man mentioned in the Introduction (see also Appendix, case A), and the second was a 36-yr-old woman (case L) who was currently under the inpatient care of one of us (A.L.) at the National Hospital for Nervous Diseases. In addition to the obsessions, compulsions and slowness which dominated the clinical picture and were the main reasons for her admission, she also carried a diagnosis of Gilles de la Tourette syndrome. Controls. For the neuromotor examination of those patients displaying 'slowness' (see below) a control group was recruited from hospital staff and employees. The controls and patients were matched pairwise with the patients for age, sex and IQ as judged by the National Adult Reading Test (NART) (Nelson, 1982). The pairs were completely matched for sex and the majority were matched within 3 yrs of age and 3 IQ points. For the neuropsychological assessments, controls matched by group for age and sex, were selected from a population recruited for an earlier study. No control had a history of psychiatric or physical illness. Informed consent was obtained from all patients and controls for the procedures of the study.
NEUROLOGY OF OBSESSIONAL SLOWNESS
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Instructions. The following is a list of activities which people with your kind of problem have difficulty with. Please answer each question by putting a tick under the appropriate number. Then for each activity give an estimate of the time it takes you.
0
Ih.ive no problem with this activit y-it takes me about the same time as the a verage person.
1
This activity takes me about twice as long as most people
2
This activity takes me about three times as lone as most people This,activity takes me more than three times as Iong as most people ACTIVITY Having a bath or shower Washing hands and face Care of hair (combing, washing, etc) Brushing teeth Dressing Undressing Using the toilet to urinate Using the toilet to defaecate Getting out of bed in the morning Eating a meal Cleaning a room in the house Making a bed Opening a door by the handle Switching a light or a tap on or off Locking or closing a door or window Writing a letter to a friend Putting a letter in the post-box Walking from one room to another Walking 100 yards down the street Crossing the road
TIME TAKEN
FIG. 1. Slowness questionnaire.
Further study of patients showing significant slowness Standard neurological examination. All patients were seen and examined independently by a psychiatrist (N.H.) and a neurologist (A.L.), and a standard neurological examination performed. In addition, the neurologist assessed each patient for asynkinesia using a test similar to that devised by Schwab et al. (1954). The subject was required to draw a triangle with the dominant hand whilst simultaneously pressing the bulb of a sphygmomanometer with the other to cause a rise in the column of mercury. Performance was assessed for ease and fluency of simultaneous movement, and rated as either normal or impaired.
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,.
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Motor examination. This structured and detailed examination was performed by the psychiatrist (N.H.), but in 15 cases the complete procedure was audio- and videotaped. These tapes were then independently examined by the neurologist (A.L.), and agreement on the various features which had been rated was estimated in 12 cases {see below). The neuromotor control group was then examined by one of us (N.H.). The 10 items of this examination, in order of administration, are listed below. Care was first taken to put each subject at ease by full explanation of the procedure. In each case the subject had met the doctor performing the examination on many previous occasions and a rapport of willingness and cooperation was readily established. Each item was rated for a variety of features using the following numerical scale: 0 = no abnormality, 1 = slight abnormality, 2 = moderate abnormality, and 3 = marked abnormality. (1) Speech. A structured interview was administered and responses recorded to obtain a sample of speech. All questions concerned 'neutral* factual demographic detail, for example, the subject's age, place of birth, nationality, parents' occupations, etc., and tasks such as counting from 0 to 50, or saying the days of the week, were also given. The features rated were hesitancy of reply, slowness of speech, low volume of voice and reduced pitch-variation. (2) Posture. During the above interview the subject was filmed in a seated posture both frontally and laterally. Following the interview the subject was asked to stand with arms first by the side and then held outstretched and in front of the body. The features rated were the degree of spontaneous facial movement, the genera] level of spontaneous bodily movement, and any degree of postural flexion. (3) Head, neck and face elicited movement. The subject was asked to shake the head from side to side, put the tongue in and out of the mouth, put the tongue out of the mouth and move it quickly from side to side, open and close the eyes and finally to bare the teeth. Frontal close-up recordings of the head and neck were made. Each movement was demonstrated three times by the examiner. Hesitancy of initiation, fluency and slowness were the features rated. (4) Upper limb rapid alternating movements. The subject was asked to hold out one hand in the shape of a fist and to make, on the back of the fist, rapid alternating supination-pronation movements with the flat of the other hand, followed by rapid, light tapping movements with the finger-tips of this hand on the back of the fist. The procedure was then repeated with the hands reversed. The subject was then asked to perform rapid open-and-close movements of the tips of the forefinger and thumb of one hand, separating these digits as much as possible between each opposition, followed by rapid opposition movements between the tips of the thumb and each finger in turn. Each movement was demonstrated by the examiner three times, and performance in both hands assessed. The features rated were hesitancy of initiation, slowness, fluency, decay of amplitude and decay of speed. (5) Upper limb sequential movements. Ozeretski's test was used (Luria, 1976). With the subject in a seated position, both hands are placed in a pronated position in the lap, one in the shape of a fist and the other with fingers extended; using simultaneous movements of the hands, the subject is asked to rapidly alternate their positions. Fist-ring test: using the dominant arm and hand, first the hand shaped into a fist is held out and withdrawn, followed by the hand with forefinger and thumb shaped into a ring; these movements being alternated several times. Fist-edge test: using the dominant hand, the hand is placed on the lap, first pronated in the shape of a fist, and then semi-prone with the fingers extended and the medial edge resting on the lap. These movements are alternated several times. Fist-edge-palm test: this is similar to the movements of the fist-edge test but with the addition to the sequence of a third movement in which the hand is moved from the 'edge' position to full pronation of the extended hand in the lap. The three-movement sequence is repeated several times. All the above movements are demonstrated three times by the examiner. The features rated were hesitancy of initiation, slowness and fluency. (6) Test-tube task. For this task the subject was seated at a table immediately in front of a row of 24 plastic test-tubes, each measuring 10.5 cm in length and 1.5 cm in diameter, and aligned perpendicularly to the table's leading edge. At a further distance of 15 cm was placed a rigid wire test-tube rack measuring 14 cm in width, 9.5 cm in depth and 9.5 cm in height, and containing 24 slots corresponding to the test-tubes. The subject, using the dominant hand, was required to place each test-tube in the rack as quickly and as accurately as possible. A practice placement of three test-tubes was allowed before beginning the task to ensure full understanding of instructions. The features of performance rated consisted of hesitancy of initiation, slowness and fluency. (7) Writing. The subject was seated at a table before a pen and a piece of plain A4 paper and asked to pick up the pen and write the word 'sunshine' as many times as possible for 1 min. The features rated were hesitancy of initiation, slowness, fluency and abnormal writing posture.
NEUROLOGY OF OBSESSIONAL SLOWNESS
2209
(8) Foot tap. In a seated position, the subject was asked to lightly tap each foot on the floor as quickly as possible. The features rated were hesitancy of initiation, slowness and fluency. (9) Whole-body movements. Starting from a seated position with both feet placed firmly on the floor, the subject was asked to alternately rise to a standing position and sit down again as many times as possible for 15 s. The subject, from a standing position, was then asked to balance first on one leg for 10 s, and then on the other. The features rated for whole-body movements were hesitancy of initiation and slowness. (10) Gait. The subject was asked to walk briskly on the flat along a concreted pavement for a distance of approximately 15 m to the bottom of a series of 6 stone steps, climb the steps, turn round and return to the starting point. The features of gait which were rated were hesitancy of initiation, slowness, pace-length, degree of right arm-swing, degree of left arm-swing and abnormality of turn.
Neuropsychology The following tests were employed, based on the rationale described by Head and colleagues (Head el al., 1989): National adult reading test (Nelson and O'Connell, 1978; Nelson, 1982; Crawford et al., 1987, 1988; O'Carroll et al., 1987). Wisconsin card sorting test (Grant and Berg, 1948; Milner, 1963). Verbal fluency tests (Milner, 1964; Borkowski et al., 1967; Benton, 1968, 1976; Newcombe, 1969). Stylus maze test (Milner, 1964). The subject is seated before a board on which is mounted an array of 100 nail-heads, and required to trace with a stylus a predetermined route across the board. The stylus is wired to the nails in such a way that contact with any nail-head outside the correct route produces a noise from a buzzer to inform him of his error. The subject is not informed of the route and must proceed by trial and error using the buzzer as a guide. He is not allowed to retrace his steps, retrace the correct path, or move diagonally. Testing proceeds until 3 error-less runs are achieved. Money road map test of directional sense (Butters et al., 1972). The subject is shown a street map on which are traced two routes, one involving 3 right or left turns, the other involving 32 such turns. The subject is asked to imagine walking each route and to indicate at each street intersection whether he would turn right or left. He is not allowed to turn the map or his body in order to facilitate his answers. The short route is followed first as a practice task to ensure full understanding of the rules of the test. The number of correct responses is scored. Personal orientation test (Semmes et al., 1963). The subject is shown a series of 5 cards each of which carries 2 diagrams of the human body, 1 in anterior and 1 in posterior view. On each diagram 4 areas on the right or left side of the body are numbered. The subject is required to point on his own body, in the order of the numbers, to the parts numbered in the diagrams. Line orientation test (Benton et al., 1978). The subject is shown a series of 15 cards each carrying a fan-shaped array of 11 lines of equal length, numbered 1 to 11 and separated by angles of 18°. Above each of these reference diagrams are 2 stimulus-lines corresponding in orientation to 2 of the lines in the reference diagram below, and of half the length. The subject is required to detect which reference lines the 2 stimulus-lines correspond to, a correct response being scored if both stimulus-lines are correctly identified. The test is free of any sequencing or switching of rules or mental images, and thus reflects a relatively 'pure' spatial ability. It is reported to be sensitive to posterior right hemisphere dysfunction. Block design. This was taken from Wechsler's adult intelligence scale tests (Wechsler, 1958).
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Inter-rater reliability Video-tapes of 12 patients were assessed independently by the 2 raters (A.L. and N.H.) on each of the 10 items of the above examination. For each item a 4-point global score of severity was derived and reliability estimated using the Weighted Kappa Coefficient as described by Cohen (1968). The maximum weight of 8 was given to the most serious disagreement where 1 rater scored no abnormality (0) and the other scored marked abnormality (3). Where 1 rater scored no abnormality (0) and the other scored slight (1) or moderate (2) the weights assigned were 2 and 4 respectively. If both raters observed an abnormality but differed in their rating by 1 deg of severity the weight assigned was 1. Relatively low coefficients were achieved for foot-tap (0.446) and writing (0.573), though others were in an acceptable range of 0.629-0.938.
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Assessment of depression Patients were asked to complete the Beck depression inventory (BDI) (Beck et al., 1961; Metcalfe and Goldman, 1965). RESULTS
TABLE 1. CHARACTERISTICS OF PATIENTS AND CONTROLS Whole group
Non-slow group
Slow group
Adjusted slow group
Neuromotor controls
Neuropsychological controls
Males
32
22
10
1
10
8
Females
27
20
7
4
6
7
Age (yrs)
34.5 (13.1)
33.4 (12.43)
Verbal IQ (NART)
36.9 (14.8)
34.7 (16.7)
36.7 (14.0)
32.9 (10.5)
114.6 (8.5)
113.5 (7.87)
116.4 (6.68)
114.2 (7.7)
Slowness questionnaire
19.5 (16.5)
10.5 (8.2)
41.7 (8.4)
43.4 (8.83)
Leyton—Total Symptoms Traits
37.5 (12.9) 26.0 (9.4) 11.5 (4.3)
35.2 (13.4) 24.1 (9.5) 11.2 (4.5)
43.3 (9.7) 30.9 (7.2) 12.4 (3.7)
45.1 (8.53) 32.4 (6.7) 12.7 (3.2)
MOCI—Total
15.6 (5.9)
14.3 (5.9)
18.8 (4.7)
21 (3.9)
Comparison of slow and non-slow subgroups. The slow subgroup did not differ significantly from the non-slow subgroup either in sex distribution (x2 = 0.2, df = 1, P > 0.05) or age (f = 0.93, df = 57, P > 0.05). The slow subgroup differed significantly from the non-slow subgroup in the total LI score (symptoms+traits) (Mann-Whitney U = 210, Z = 2.00, P < 0.05, two-tailed), the LI symptom score (Mann-Whitney U = 190, Z = 2.35, P < 0.02, two-tailed) and the MOCI total obsessionality score (Mann-Whitney U = 236.5, Z = 2.43, P < 0.02, two-tailed), the slow subgroup
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Initial screening All 59 consecutive patients completed the slowness questionnaire (SQ). Seventeen (29%) scored greater than 30, the criterion at or above which slowness was to be defined as present for the purpose of the study. Two patients in the consecutive non-slow subgroup failed to return the Leyton inventory (LI) and 1 patient in the slow subgroup refused to complete it. One patient in the non-slow subgroup returned an incomplete Maudsley Obsessive-Compulsive Inventory (MOCI) which was excluded from the analysis. Some characteristics of the patient and control groups are summarized in Table 1. With the measures of obsessionality used in this study the initial group of 59 consecutive patients was comparable with previously reported populations of adults with obsessivecompulsive disorder (Cooper, 1970; Hodgson and Rachman, 1977; Murray et al., 1979).
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showing greater obsessionality as judged by these measures. There was no significant difference between the subgroups on the LI trait score (Mann-Whitney U = 328, Z = 0.54, P > 0.05). Further study of the slow subgroup Two of the 17 consecutive patients in this group refused to participate further. Two other patients (cases A and L) who were comparable in their scores on the slowness questionnaire and obsessional inventories were substituted as described in Methods. Reanalysis of all the slow vs non-slow comparisons showed no effect of the substitution on the results. The group of 17 slow patients subjected to the further studies described below therefore comprises these 2 patients and the remaining 15 consecutive patients. Vignettes of these patients are provided in the Appendix.
TABLE 2. CLINICAL FEATURES OF PATIENTS WITH SLOWNESS (n =
17)
Case code A Observable behaviour Simple actions repeated, e.g. switches, taps, doors Simple action] preceded or interrupted by hesitation Simple actions 'ritualistic' Increased touching of environment Decreased touching/avoidance of environment Increased response to random visual stimuli Visual checking or searching behaviour Increased response to random auditory stimuli Repetitive cleaning/washing of self Repetitive cleaning/washing of personal environment Difficulty going through doorways Rigid routines and order for simple
B
C
D
+ +
E
F
G
+
+ +
+
+
H
I
K
L
++ +
+
+
M
N
O
+
+
+
+
+
+
P
+
Q +
+
+
+
+
+
+
+
+
+
(65)
+
(18) (18) (47)
+
+
+ +
+
(12)
+
+ +
+
+
+
+
+ +
++
+
+ +
+
+ +
(59)'
+
+
++
+
J
+
(35) (12)
+ + +
+
+
+
+ +
+ +
(53) (12) (41) (35)
+
actions
Subjective experiences Fear of harming others, e.g. by contamination Fear of being harmed, e.g. by contamination Ruminations Doubts Feeling of incompktion of action Counting to self Perfectionism Indecision
+ +
+
+
+ +
+
+
+
+
+
+
+
+
'
+
+
+ +
+ +
+
+
+
+
(29)
+
+
(71)
+ +
+
+
+ +
+ +
+ + +
+
'Numbers in parentheses show the percentage of the group displaying each feature.
(35) (12) +(41) (12) (18) (12)
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Clinical features of the slow group The leading obsessive-compulsive features were classified into objective behaviour and subjective symptoms. These are summarized in Table 2.
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N. HYMAS AND OTHERS
Motor examination Motor abnormalities. Comparisons between patients and controls are given in Table 3. Two analyses were performed: firstly, the slow patient group as a whole was compared with controls; secondly, an 'adjusted slow group' was compared by excluding 6 cases with features in addition to their OCD which could have been independently associated with motor disorder, and could have been biasing the findings in favour of the hypothesis being examined. These were the 4 cases in whom an additional 'neurological' diagnosis could be sustained (Gilles de la Tourette syndrome in cases J and L, and a parkinsonian syndrome in cases F and O), and the 2 cases (H and N) who were taking neuroleptic medication at the time of examination. In the slow patient group as a whole, motor abnormalities were seen in all of the 10 categories of the examination but were most common on examination of upper-limb rapid alternating movements, of upper-limb sequential movements and of gait. In the controls, abnormalities were observed only on examination of head, neck and facial movements, of upper limb rapid alternating movements, of upper limb sequential movement and of gait. Using Wilcoxon's signed-ranks test (two-tailed), comparison with the control group showed significantly more abnormalities in the patients for all
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In addition to the diagnosis of OCD, which was the principal psychiatric feature in every case and the reason for the patient's referral, another psychiatric diagnosis could be sustained in 1 case where the obsessive-compulsive features arose in a setting of probable Asperger's syndrome. The group mean score on the Beck depression inventory was 17.3 (SD 10.4, range 4—44). Twelve patients scored 18 or below corresponding to the responses of a 'mildly depressed' population in the original study by Beck and colleagues (Beck et al., 1961). Four patients (cases J, N, O and P) scored 2 2 - 2 8 corresponding to 'moderate' depression; 1 patient (case D) scored 44 corresponding to 'severe' depression though a diagnosis of major depression was not sustained on examination. In addition to the psychiatric diagnosis, a neurological diagnosis could be sustained in 4 cases. Cases F and O had a parkinsonian syndrome. In 1 case this probably began in childhood, there was no tremor, and no disturbance of pace-length or handwriting. In the other the development of classical Parkinson's disease was preceded by many years of a typical OCD with contamination fears and repetitive hand-washing. The patient commented that for years she had moved slowly and carefully in order to avoid touching objects which might contaminate her and regarded it as ironic that now she wished to move more quickly she was unable to do so. Cases J and L had motor and vocal tics. Case P had received a course of ECT 2 wks prior to examination and was receiving imipramine at the time of assessment. Case L had received tranylcypromine until 2 wks before examination. Case K had received phenelzine until 2 wks before assessment. At the time of examination case D was taking 20 mg of diazepam and 100 mg dothiepin daily, case H was receiving zuclopentixol 16 mg daily, and case N was receiving depot flupenthixol 40 mg monthly. No other case had been taking medication for several weeks before examination. Four patients, but also 4 controls, gave histories of an abnormal birth. All patients had normal CT brain scans.
NEUROLOGY OF OBSESSIONAL
2213
SLOWNESS
•4INATION—COMP.ARISON OF PATIENTS AND CONTROLS Group means (±SD) Item1
Patients
W2
P
2.00±2.3 [1.73±1.7
Posture
1.75±2.1 [1.27±1.2
0 0]
0 [0
< 0.005
THE NEUROLOGY OF OBSESSIONAL SLOWNESS by N. HYMAS, 1 A. LEES, 2 D. BOLTON, 3 K. EPPS 3 and D. HEAD3 (From 'Fulbourn Hospital, Cambridge, the 2National Hospital for Nervous Diseases, Queen Square, London, and the ^Institute of Psychiatry, London, UK)
SUMMARY
INTRODUCTION
Obsessions are recurrent, persistent ideas, thoughts, images or impulses that are experienced as involuntary, senseless or repugnant. Attempts are made to ignore or suppress them. Compulsions are repetitive and seemingly purposeful behaviours that are performed according to certain rules or in a stereotyped fashion. The act is performed with a sense of subjective compulsion often coupled with a desire to resist the compulsion. The individual usually recognizes the senselessness of the behaviour and does not derive pleasure from carrying out the activity, although it often provides a release of tension (American Psychiatric Association, 1980). This is theme from which are woven all those many variations of individual psychopathology to be found under the general rubric of Obsessive-Compulsive Disorder (OCD). Common obsessions concern violent urges towards the self or others, fears of contamination of self or others, or doubts about past actions or events. Common compulsive rituals involve cleaning, counting, checking, touching or avoidance (Dowson, 1977; Stern and Cobb, 1978; American Psychiatric Association, 1980). In recent decades it has not been customary to try to understand such symptoms and behaviour as manifestations of cerebral dysfunction. Indeed, in systems of psychiatric nosology such as DSM-III (American Psychiatric Association, 1980) or ICD-9 (World Health Organization, 1978), the absence of demonstrable brain disease was a criterion by which the syndrome of OCD was defined. Classified as a 'neurosis', it took its place alongside a variety of other disorders which, according to contemporary usage of the term, were often thought to be best approached primarily with the languages and concepts of dynamic psychology or sociology and with little reference to those of physiology or clinical neurology. Correspondence to: Dr Nigel Hymas, Fulbourn Hospital, Cambridge CB1 5EF, UK. © Oxford University Press 1991
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Seventeen of 59 patients admitted to hospital for treatment of Obsessive-Compulsive Disorder (OCD) were found to have significant slowness, mainly due to difficulty in initiating goal-directed action and suppressing intrusive and perseverative behaviour. In this subgroup subtle neurological abnormalities were found more frequently than in healthy controls and included loss of motor fluency, hesitancy of initiation of limb movements, speech and gait abnormalities, cogwheel rigidity, complex repetitive movements and tics. Difficulties in cognitive set-shifting and complex spatial-and-shifting abilities were found on neuropsychological testing, but no correlation was found between these disturbances and either the degree of obsessionality or the severity of motor dysfunction. These results suggest that patients with obsessional slowness may have a dysfunction in the frontal-basal-ganglia loop system.
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N. HYMAS AND OTHERS
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However, since Esquirol in 1838 described a patient under his care who displayed some of those particular features of behaviour and experience which subsequently came to be termed 'obsessive-compulsive disorder' (Esquirol, 1838), there has existed a current of observation, thought and speculation which has always sought to convey, alongside descriptions of a purely psychological nature, the relevance of neurological mechanisms (Hymas and Prasad, 1989). Pierre Janet, for example, whose descriptions of the syndrome must remain unsurpassed in their comprehensiveness, elegant clarity and attention to psychological nuance, nevertheless perceived the provisional and partial nature of his psychological formulations, and believed them to be paving the way to a future anatomical understanding (Janet, 1903). Janet's awareness and acknowledgement of the importance of the biological and neurological aspects of the syndrome, and the similar awareness shown by contemporaries such as Tuke (1894) or Jackson (1895), perhaps reflected the shared concepts of neurology and psychiatry, and the easy commerce of ideas which existed between their practitioners, in the latter half of the 19th century (Bynum, 1985; Dowbiggin, 1985). The subsequent impact of Freudian ideas led to, or at least was an expression of, a divergence of viewpoints which increasingly persuaded psychiatrists to divorce mental illnesses such as obsessive-compulsive disorder from the neurological context of earlier understanding. The 'neuroses' assumed an autonomy as 'functional' psychological disorders (Berrios, 1985) and became freed from those connotations of central nervous system disease which had been implicit in earlier conceptions of the term (Hunter, 1973; Bynum, 1985; Rogers, 1987). The literature on OCD tended, thereafter, to remain predominantly psychological in emphasis. However, in the first half of this century, speculations concerning the cerebral basis of the syndrome continued. Such ideas were especially fuelled by the observation of obsessive-compulsive phenomena in patients suffering from neurological disorders. The outbreaks of epidemic encephalitis which had swept Europe and North America at the end of the First World War and throughout the following decade (Greenfield, 1976) had been of particular importance in yielding many reports of obsessions and compulsions associated with the syndrome of post-encephalitic parkinsonism (e.g. von Economo, 1931). Obsessions and compulsions associated with epilepsy (e.g. Brickner et al., 1940) and tic-disorder (e.g. Creak and Guttman, 1935) were also reported, and within the limits of contemporary knowledge attempts were made to interpret both the neurological and the psychiatric disturbances in terms of shared cerebral mechanisms. Schilder, for example, in his study of 1938 referred to the association of obsessivecompulsive phenomena with epidemic encephalitis earlier in the century and argued for a close relationship between the neurologically-based disturbances of motility seen in these patients and their particular psychiatric symptoms (Schilder, 1938). He estimated from his clinical experience that in obsessional patients, without any history suggestive of encephalitis, 'organic' signs could be found in about a third of cases, and that in a further third the symptomatology aroused the suspicion of an organic background. The signs that Schilder observed included: rigidity of the face, flexor rigidity of the arms, tremor, impaired eye convergence, great urge to talk and propulsive features in speech, and what he called 'motor urges of a higher degree'. A renewed interest in the importance of these earlier observations to the study of
NEUROLOGY OF OBSESSIONAL SLOWNESS
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obsessive-compulsive disorder can be discerned in some recent publications (Laplane etal., 1981, 1984; Yaryura-Tobias and Neziroglu, 1983; Cummings and Frankel, 1985; Ward, 1988). Furthermore, some more recent studies have attempted to generate 'biological markers' of the disorder, or of subgroups within it. However, few investigations have proceeded from coherent hypotheses concerning brain-behaviour relationships, and few have attempted to explain the phenomena of OCD in terms of phenomena displayed by patients, or experimental animals, suffering from cerebral disorders whose mechanisms may be better understood (Hymas and Prasad, 1989). Against this background, the comparatively recently described phenomenon of 'obsessional slowness' gains particular interest. Many patients with obsessive-compulsive disorder complain of slowness in carrying out their ordinary, day-to-day activities, a slowness which may sometimes be profoundly incapacitating (Marks, 1978). It is commonly thought to be the result of the performance of rituals and has attracted little attention in its own right. Indeed, in standard textbook descriptions of the disorder, for example, those by Slater and Roth (1969), Ey et al. (1974) or Rado and Monroe (1974), it receives no explicit mention. In 1974 Rachman described what he termed 'primary obsessional slowness' (Rachman, 1974). His report was based on the characteristics of 10 patients who showed severe slowness in the execution of the simple tasks of daily living, such as dressing, bathing or eating. His descriptions, however, leave some uncertainty about the precise phenomenon he was attempting to identify. On the one hand, he notes that particular care was taken to exclude patients 'in whom slowness was plainly a secondary consequence of extensive checking or other rituals', yet elsewhere states that 'needless to say, all 10 of the patients were carrying out some checking behaviour'. On the one hand, he describes that the patients resembled a 'slow motion movie', yet on the other that 'slow motion of the limbs seemed to play no part in their overall slowness'. Rachman explains the slowness psychologically in terms of 'meticulousness', and without reference to the brain. Our own interest in obsessional slowness was kindled by the close observation of a patient who demonstrated the phenomenon to a marked degree. This 25-yr-old man, who suffered from a compulsion to touch things and repeat actions, would take hours over the most ordinary of activities such as having a bath or dressing. His slowness seemed to derive from a difficulty in initiating simple movements, in shifting between and sequencing different patterns of movement, and in performing more than one movement simultaneously; his goal-directed behaviour was continually disrupted by the perseveration of unwanted movements and by an extreme distractability to random visual stimuli; a further striking feature was the inefficacy of his verbal monitoring in modifying and directing his behaviour. The patient, therefore, showed a number of deficits of motor performance and control reminiscent of some of those seen in, for example, frontal lobe disorders, or Parkinson's disease in which a dysfunction of basal ganglia and possibly also of frontal lobe mechanisms is believed to be important. This background was felt to justify a prospective investigation of a series of prominently slow obsessive-compulsive patients using a design which would expose some of those motor and cognitive deficiencies seen in patients suffering from dysfunction of the frontal lobes of the brain and their subcortical connections.
2206
N. HYMAS AND OTHERS METHODS
Assessments Assessments consisted of an initial screening procedure followed by the further study of patients showing slowness. Initial screening All patients were asked to complete the Maudsley Obsessional-Compulsive Inventory (MOCI) (Hodgson and Rachman, 1977), and the self-administered written form of the Leyton obsessional inventory (LOI) (Cooper, 1970; Snowdon, 1980). These are two widely used methods of assessing the existence and extent of obsessive-compulsive complaints. In order to simplify the administration of the questionnaires, the questions relating to resistance and interference in the Leyton inventory were omitted. All patients were also asked to complete a slowness questionnaire which had been devised for the study. Slowness questionnaire. This self-administered questionnaire is shown in Fig. 1. It lists 20 common items of behaviour. The subject is asked to rate the speed of his or her own performance of each item in comparison with an average person. The scoring method is shown on the questionnaire. The maximum possible score is 60, corresponding to the maximum severity of subjective slowness. A pilot study was conducted to establish the score above which 'slowness' would be defined as present. The questionnaire was administered to 6 obsessive-compulsive patients in whom slowness in day-to-day activities was a prominent and disabling feature. Patients in this group often complained of having to take several hours over such routine tasks as dressing, eating a meal, washing or bathing. Their results were compared with a group of 11 other obsessive-compulsive patients not showing this feature to a marked degree. The mean score of the slow group was 38.3 (SD 7.2, range 30-47), and that of the non-slow group 12.2 (SD 8.8, range 3—29). A score of 30, which lay approximately 2 standard deviations above the mean of the non-slow group, was chosen as the criterion score above which a significant degree of slowness in day-to-day activities was to be defined as present for the purpose of the study.
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Subjects Patients. Patients were recruited from the Behaviour Therapy Unit of the BethJem and Maudsley Hospital, London. Between November 1985 and April 1988 all patients referred to the unit for inpatient assessment and/or treatment of obsessive-compulsive symptoms and behaviour were screened at the time of their first attendance or admission. In all cases the diagnosis of OCD was made according to DSM-111 guidelines (American Psychiatric Association, 1980). However, in view of the potential interest of patients who might show a conjunction of this particular psycho-syndrome and a 'neurological' disorder, the exclusion criteria of the presence of Gilles de la Tourette syndrome or 'organic mental disorder' were ignored. This matches the subsequent revision of DSM-111 (DSM-111-R, American Psychiatric Association, 1987). In all cases the obsessive-compulsive symptoms and behaviours constituted the leading feature of the psychiatric picture and formed the principal reasons for the patient's referral. Fifty-nine patients were screened of whom 32 were men, with a mean age of 35.2 yrs (range 17 — 73, SD 14.49), and 27 were women, with a mean age of 33.5 yrs (range 2 1 - 6 5 , SD 11.5). Two other patients who fulfilled this study's diagnostic criteria for obsessional slowness (see below) were also included. The first was the 25-yr-old man mentioned in the Introduction (see also Appendix, case A), and the second was a 36-yr-old woman (case L) who was currently under the inpatient care of one of us (A.L.) at the National Hospital for Nervous Diseases. In addition to the obsessions, compulsions and slowness which dominated the clinical picture and were the main reasons for her admission, she also carried a diagnosis of Gilles de la Tourette syndrome. Controls. For the neuromotor examination of those patients displaying 'slowness' (see below) a control group was recruited from hospital staff and employees. The controls and patients were matched pairwise with the patients for age, sex and IQ as judged by the National Adult Reading Test (NART) (Nelson, 1982). The pairs were completely matched for sex and the majority were matched within 3 yrs of age and 3 IQ points. For the neuropsychological assessments, controls matched by group for age and sex, were selected from a population recruited for an earlier study. No control had a history of psychiatric or physical illness. Informed consent was obtained from all patients and controls for the procedures of the study.
NEUROLOGY OF OBSESSIONAL SLOWNESS
2207
Instructions. The following is a list of activities which people with your kind of problem have difficulty with. Please answer each question by putting a tick under the appropriate number. Then for each activity give an estimate of the time it takes you.
0
Ih.ive no problem with this activit y-it takes me about the same time as the a verage person.
1
This activity takes me about twice as long as most people
2
This activity takes me about three times as lone as most people This,activity takes me more than three times as Iong as most people ACTIVITY Having a bath or shower Washing hands and face Care of hair (combing, washing, etc) Brushing teeth Dressing Undressing Using the toilet to urinate Using the toilet to defaecate Getting out of bed in the morning Eating a meal Cleaning a room in the house Making a bed Opening a door by the handle Switching a light or a tap on or off Locking or closing a door or window Writing a letter to a friend Putting a letter in the post-box Walking from one room to another Walking 100 yards down the street Crossing the road
TIME TAKEN
FIG. 1. Slowness questionnaire.
Further study of patients showing significant slowness Standard neurological examination. All patients were seen and examined independently by a psychiatrist (N.H.) and a neurologist (A.L.), and a standard neurological examination performed. In addition, the neurologist assessed each patient for asynkinesia using a test similar to that devised by Schwab et al. (1954). The subject was required to draw a triangle with the dominant hand whilst simultaneously pressing the bulb of a sphygmomanometer with the other to cause a rise in the column of mercury. Performance was assessed for ease and fluency of simultaneous movement, and rated as either normal or impaired.
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,.
2208
N. HYMAS AND OTHERS
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Motor examination. This structured and detailed examination was performed by the psychiatrist (N.H.), but in 15 cases the complete procedure was audio- and videotaped. These tapes were then independently examined by the neurologist (A.L.), and agreement on the various features which had been rated was estimated in 12 cases {see below). The neuromotor control group was then examined by one of us (N.H.). The 10 items of this examination, in order of administration, are listed below. Care was first taken to put each subject at ease by full explanation of the procedure. In each case the subject had met the doctor performing the examination on many previous occasions and a rapport of willingness and cooperation was readily established. Each item was rated for a variety of features using the following numerical scale: 0 = no abnormality, 1 = slight abnormality, 2 = moderate abnormality, and 3 = marked abnormality. (1) Speech. A structured interview was administered and responses recorded to obtain a sample of speech. All questions concerned 'neutral* factual demographic detail, for example, the subject's age, place of birth, nationality, parents' occupations, etc., and tasks such as counting from 0 to 50, or saying the days of the week, were also given. The features rated were hesitancy of reply, slowness of speech, low volume of voice and reduced pitch-variation. (2) Posture. During the above interview the subject was filmed in a seated posture both frontally and laterally. Following the interview the subject was asked to stand with arms first by the side and then held outstretched and in front of the body. The features rated were the degree of spontaneous facial movement, the genera] level of spontaneous bodily movement, and any degree of postural flexion. (3) Head, neck and face elicited movement. The subject was asked to shake the head from side to side, put the tongue in and out of the mouth, put the tongue out of the mouth and move it quickly from side to side, open and close the eyes and finally to bare the teeth. Frontal close-up recordings of the head and neck were made. Each movement was demonstrated three times by the examiner. Hesitancy of initiation, fluency and slowness were the features rated. (4) Upper limb rapid alternating movements. The subject was asked to hold out one hand in the shape of a fist and to make, on the back of the fist, rapid alternating supination-pronation movements with the flat of the other hand, followed by rapid, light tapping movements with the finger-tips of this hand on the back of the fist. The procedure was then repeated with the hands reversed. The subject was then asked to perform rapid open-and-close movements of the tips of the forefinger and thumb of one hand, separating these digits as much as possible between each opposition, followed by rapid opposition movements between the tips of the thumb and each finger in turn. Each movement was demonstrated by the examiner three times, and performance in both hands assessed. The features rated were hesitancy of initiation, slowness, fluency, decay of amplitude and decay of speed. (5) Upper limb sequential movements. Ozeretski's test was used (Luria, 1976). With the subject in a seated position, both hands are placed in a pronated position in the lap, one in the shape of a fist and the other with fingers extended; using simultaneous movements of the hands, the subject is asked to rapidly alternate their positions. Fist-ring test: using the dominant arm and hand, first the hand shaped into a fist is held out and withdrawn, followed by the hand with forefinger and thumb shaped into a ring; these movements being alternated several times. Fist-edge test: using the dominant hand, the hand is placed on the lap, first pronated in the shape of a fist, and then semi-prone with the fingers extended and the medial edge resting on the lap. These movements are alternated several times. Fist-edge-palm test: this is similar to the movements of the fist-edge test but with the addition to the sequence of a third movement in which the hand is moved from the 'edge' position to full pronation of the extended hand in the lap. The three-movement sequence is repeated several times. All the above movements are demonstrated three times by the examiner. The features rated were hesitancy of initiation, slowness and fluency. (6) Test-tube task. For this task the subject was seated at a table immediately in front of a row of 24 plastic test-tubes, each measuring 10.5 cm in length and 1.5 cm in diameter, and aligned perpendicularly to the table's leading edge. At a further distance of 15 cm was placed a rigid wire test-tube rack measuring 14 cm in width, 9.5 cm in depth and 9.5 cm in height, and containing 24 slots corresponding to the test-tubes. The subject, using the dominant hand, was required to place each test-tube in the rack as quickly and as accurately as possible. A practice placement of three test-tubes was allowed before beginning the task to ensure full understanding of instructions. The features of performance rated consisted of hesitancy of initiation, slowness and fluency. (7) Writing. The subject was seated at a table before a pen and a piece of plain A4 paper and asked to pick up the pen and write the word 'sunshine' as many times as possible for 1 min. The features rated were hesitancy of initiation, slowness, fluency and abnormal writing posture.
NEUROLOGY OF OBSESSIONAL SLOWNESS
2209
(8) Foot tap. In a seated position, the subject was asked to lightly tap each foot on the floor as quickly as possible. The features rated were hesitancy of initiation, slowness and fluency. (9) Whole-body movements. Starting from a seated position with both feet placed firmly on the floor, the subject was asked to alternately rise to a standing position and sit down again as many times as possible for 15 s. The subject, from a standing position, was then asked to balance first on one leg for 10 s, and then on the other. The features rated for whole-body movements were hesitancy of initiation and slowness. (10) Gait. The subject was asked to walk briskly on the flat along a concreted pavement for a distance of approximately 15 m to the bottom of a series of 6 stone steps, climb the steps, turn round and return to the starting point. The features of gait which were rated were hesitancy of initiation, slowness, pace-length, degree of right arm-swing, degree of left arm-swing and abnormality of turn.
Neuropsychology The following tests were employed, based on the rationale described by Head and colleagues (Head el al., 1989): National adult reading test (Nelson and O'Connell, 1978; Nelson, 1982; Crawford et al., 1987, 1988; O'Carroll et al., 1987). Wisconsin card sorting test (Grant and Berg, 1948; Milner, 1963). Verbal fluency tests (Milner, 1964; Borkowski et al., 1967; Benton, 1968, 1976; Newcombe, 1969). Stylus maze test (Milner, 1964). The subject is seated before a board on which is mounted an array of 100 nail-heads, and required to trace with a stylus a predetermined route across the board. The stylus is wired to the nails in such a way that contact with any nail-head outside the correct route produces a noise from a buzzer to inform him of his error. The subject is not informed of the route and must proceed by trial and error using the buzzer as a guide. He is not allowed to retrace his steps, retrace the correct path, or move diagonally. Testing proceeds until 3 error-less runs are achieved. Money road map test of directional sense (Butters et al., 1972). The subject is shown a street map on which are traced two routes, one involving 3 right or left turns, the other involving 32 such turns. The subject is asked to imagine walking each route and to indicate at each street intersection whether he would turn right or left. He is not allowed to turn the map or his body in order to facilitate his answers. The short route is followed first as a practice task to ensure full understanding of the rules of the test. The number of correct responses is scored. Personal orientation test (Semmes et al., 1963). The subject is shown a series of 5 cards each of which carries 2 diagrams of the human body, 1 in anterior and 1 in posterior view. On each diagram 4 areas on the right or left side of the body are numbered. The subject is required to point on his own body, in the order of the numbers, to the parts numbered in the diagrams. Line orientation test (Benton et al., 1978). The subject is shown a series of 15 cards each carrying a fan-shaped array of 11 lines of equal length, numbered 1 to 11 and separated by angles of 18°. Above each of these reference diagrams are 2 stimulus-lines corresponding in orientation to 2 of the lines in the reference diagram below, and of half the length. The subject is required to detect which reference lines the 2 stimulus-lines correspond to, a correct response being scored if both stimulus-lines are correctly identified. The test is free of any sequencing or switching of rules or mental images, and thus reflects a relatively 'pure' spatial ability. It is reported to be sensitive to posterior right hemisphere dysfunction. Block design. This was taken from Wechsler's adult intelligence scale tests (Wechsler, 1958).
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Inter-rater reliability Video-tapes of 12 patients were assessed independently by the 2 raters (A.L. and N.H.) on each of the 10 items of the above examination. For each item a 4-point global score of severity was derived and reliability estimated using the Weighted Kappa Coefficient as described by Cohen (1968). The maximum weight of 8 was given to the most serious disagreement where 1 rater scored no abnormality (0) and the other scored marked abnormality (3). Where 1 rater scored no abnormality (0) and the other scored slight (1) or moderate (2) the weights assigned were 2 and 4 respectively. If both raters observed an abnormality but differed in their rating by 1 deg of severity the weight assigned was 1. Relatively low coefficients were achieved for foot-tap (0.446) and writing (0.573), though others were in an acceptable range of 0.629-0.938.
2210
N. HYMAS AND OTHERS
Assessment of depression Patients were asked to complete the Beck depression inventory (BDI) (Beck et al., 1961; Metcalfe and Goldman, 1965). RESULTS
TABLE 1. CHARACTERISTICS OF PATIENTS AND CONTROLS Whole group
Non-slow group
Slow group
Adjusted slow group
Neuromotor controls
Neuropsychological controls
Males
32
22
10
1
10
8
Females
27
20
7
4
6
7
Age (yrs)
34.5 (13.1)
33.4 (12.43)
Verbal IQ (NART)
36.9 (14.8)
34.7 (16.7)
36.7 (14.0)
32.9 (10.5)
114.6 (8.5)
113.5 (7.87)
116.4 (6.68)
114.2 (7.7)
Slowness questionnaire
19.5 (16.5)
10.5 (8.2)
41.7 (8.4)
43.4 (8.83)
Leyton—Total Symptoms Traits
37.5 (12.9) 26.0 (9.4) 11.5 (4.3)
35.2 (13.4) 24.1 (9.5) 11.2 (4.5)
43.3 (9.7) 30.9 (7.2) 12.4 (3.7)
45.1 (8.53) 32.4 (6.7) 12.7 (3.2)
MOCI—Total
15.6 (5.9)
14.3 (5.9)
18.8 (4.7)
21 (3.9)
Comparison of slow and non-slow subgroups. The slow subgroup did not differ significantly from the non-slow subgroup either in sex distribution (x2 = 0.2, df = 1, P > 0.05) or age (f = 0.93, df = 57, P > 0.05). The slow subgroup differed significantly from the non-slow subgroup in the total LI score (symptoms+traits) (Mann-Whitney U = 210, Z = 2.00, P < 0.05, two-tailed), the LI symptom score (Mann-Whitney U = 190, Z = 2.35, P < 0.02, two-tailed) and the MOCI total obsessionality score (Mann-Whitney U = 236.5, Z = 2.43, P < 0.02, two-tailed), the slow subgroup
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Initial screening All 59 consecutive patients completed the slowness questionnaire (SQ). Seventeen (29%) scored greater than 30, the criterion at or above which slowness was to be defined as present for the purpose of the study. Two patients in the consecutive non-slow subgroup failed to return the Leyton inventory (LI) and 1 patient in the slow subgroup refused to complete it. One patient in the non-slow subgroup returned an incomplete Maudsley Obsessive-Compulsive Inventory (MOCI) which was excluded from the analysis. Some characteristics of the patient and control groups are summarized in Table 1. With the measures of obsessionality used in this study the initial group of 59 consecutive patients was comparable with previously reported populations of adults with obsessivecompulsive disorder (Cooper, 1970; Hodgson and Rachman, 1977; Murray et al., 1979).
NEUROLOGY OF OBSESSIONAL SLOWNESS
2211
showing greater obsessionality as judged by these measures. There was no significant difference between the subgroups on the LI trait score (Mann-Whitney U = 328, Z = 0.54, P > 0.05). Further study of the slow subgroup Two of the 17 consecutive patients in this group refused to participate further. Two other patients (cases A and L) who were comparable in their scores on the slowness questionnaire and obsessional inventories were substituted as described in Methods. Reanalysis of all the slow vs non-slow comparisons showed no effect of the substitution on the results. The group of 17 slow patients subjected to the further studies described below therefore comprises these 2 patients and the remaining 15 consecutive patients. Vignettes of these patients are provided in the Appendix.
TABLE 2. CLINICAL FEATURES OF PATIENTS WITH SLOWNESS (n =
17)
Case code A Observable behaviour Simple actions repeated, e.g. switches, taps, doors Simple action] preceded or interrupted by hesitation Simple actions 'ritualistic' Increased touching of environment Decreased touching/avoidance of environment Increased response to random visual stimuli Visual checking or searching behaviour Increased response to random auditory stimuli Repetitive cleaning/washing of self Repetitive cleaning/washing of personal environment Difficulty going through doorways Rigid routines and order for simple
B
C
D
+ +
E
F
G
+
+ +
+
+
H
I
K
L
++ +
+
+
M
N
O
+
+
+
+
+
+
P
+
Q +
+
+
+
+
+
+
+
+
+
(65)
+
(18) (18) (47)
+
+
+ +
+
(12)
+
+ +
+
+
+
+
+ +
++
+
+ +
+
+ +
(59)'
+
+
++
+
J
+
(35) (12)
+ + +
+
+
+
+ +
+ +
(53) (12) (41) (35)
+
actions
Subjective experiences Fear of harming others, e.g. by contamination Fear of being harmed, e.g. by contamination Ruminations Doubts Feeling of incompktion of action Counting to self Perfectionism Indecision
+ +
+
+
+ +
+
+
+
+
+
+
+
+
'
+
+
+ +
+ +
+
+
+
+
(29)
+
+
(71)
+ +
+
+
+ +
+ +
+ + +
+
'Numbers in parentheses show the percentage of the group displaying each feature.
(35) (12) +(41) (12) (18) (12)
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on October 3, 2014
Clinical features of the slow group The leading obsessive-compulsive features were classified into objective behaviour and subjective symptoms. These are summarized in Table 2.
2212
N. HYMAS AND OTHERS
Motor examination Motor abnormalities. Comparisons between patients and controls are given in Table 3. Two analyses were performed: firstly, the slow patient group as a whole was compared with controls; secondly, an 'adjusted slow group' was compared by excluding 6 cases with features in addition to their OCD which could have been independently associated with motor disorder, and could have been biasing the findings in favour of the hypothesis being examined. These were the 4 cases in whom an additional 'neurological' diagnosis could be sustained (Gilles de la Tourette syndrome in cases J and L, and a parkinsonian syndrome in cases F and O), and the 2 cases (H and N) who were taking neuroleptic medication at the time of examination. In the slow patient group as a whole, motor abnormalities were seen in all of the 10 categories of the examination but were most common on examination of upper-limb rapid alternating movements, of upper-limb sequential movements and of gait. In the controls, abnormalities were observed only on examination of head, neck and facial movements, of upper limb rapid alternating movements, of upper limb sequential movement and of gait. Using Wilcoxon's signed-ranks test (two-tailed), comparison with the control group showed significantly more abnormalities in the patients for all
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on October 3, 2014
In addition to the diagnosis of OCD, which was the principal psychiatric feature in every case and the reason for the patient's referral, another psychiatric diagnosis could be sustained in 1 case where the obsessive-compulsive features arose in a setting of probable Asperger's syndrome. The group mean score on the Beck depression inventory was 17.3 (SD 10.4, range 4—44). Twelve patients scored 18 or below corresponding to the responses of a 'mildly depressed' population in the original study by Beck and colleagues (Beck et al., 1961). Four patients (cases J, N, O and P) scored 2 2 - 2 8 corresponding to 'moderate' depression; 1 patient (case D) scored 44 corresponding to 'severe' depression though a diagnosis of major depression was not sustained on examination. In addition to the psychiatric diagnosis, a neurological diagnosis could be sustained in 4 cases. Cases F and O had a parkinsonian syndrome. In 1 case this probably began in childhood, there was no tremor, and no disturbance of pace-length or handwriting. In the other the development of classical Parkinson's disease was preceded by many years of a typical OCD with contamination fears and repetitive hand-washing. The patient commented that for years she had moved slowly and carefully in order to avoid touching objects which might contaminate her and regarded it as ironic that now she wished to move more quickly she was unable to do so. Cases J and L had motor and vocal tics. Case P had received a course of ECT 2 wks prior to examination and was receiving imipramine at the time of assessment. Case L had received tranylcypromine until 2 wks before examination. Case K had received phenelzine until 2 wks before assessment. At the time of examination case D was taking 20 mg of diazepam and 100 mg dothiepin daily, case H was receiving zuclopentixol 16 mg daily, and case N was receiving depot flupenthixol 40 mg monthly. No other case had been taking medication for several weeks before examination. Four patients, but also 4 controls, gave histories of an abnormal birth. All patients had normal CT brain scans.
NEUROLOGY OF OBSESSIONAL
2213
SLOWNESS
•4INATION—COMP.ARISON OF PATIENTS AND CONTROLS Group means (±SD) Item1
Patients
W2
P
2.00±2.3 [1.73±1.7
Posture
1.75±2.1 [1.27±1.2
0 0]
0 [0
< 0.005
