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Kinematic analysis of handwriting movements in Schizophrenic patients
Kinematic Analysis of Handwriting Movements in Schizophrenic Patients Robyn M. Gallucci, James G. Phillips, John L. Bradshaw, Krishna S. Vaddadi, and Christos Pantelis K e y W o r d s : Schizophrenia, basal ganglia, laterality, P a r k i n s o n ' s disease, H u n t i n g t o n ' s disease BIOL PSYCHIATRY 1997;41:830--833
Introduction Any motor dysfunction in schizophrenia could provide insights into underlying functional disturbance. Motor incoordination in schizophrenia could reflect disturbed subcortical function (Pantelis et al 1992; Sandyk and Kay 1990). We have previously kinematically documented handwriting of patients with basal ganglia (BG) diseases known to affect the speed and size of handwriting strokes (Phillips et al 1991 1994). Chorea reduces consistency of handwriting (Phillips et al 1994), and bradykinesic movements are inefficient, sometimes requiring prolonged periods of acceleration (Phillips et al 1989). Alternatively, schizophrenic motor incoordination could be a soft sign, with reduced preferred/nonpreferred hand differences indicating abnormalities of hemispheric specialization (Crow 1990). Since writing hand preference is an important test of handedness, we asked whether patients with schizophrenia exhibit extrapyramidal signs or altered functional asymmetries, by kinematically analyzing their handwriting movements.
Methods Twenty schizophrenic patients diagnosed under DSM-IV criteria (12 male and 8 female) had a mean age of 31.1 (range 18-46, SD 8.0) years and a mean illness duration of 9.9 (SD 7.3) years. From the Department of Psychology, Monash University,Clayton, Australia (RMG, JGP, JLB); Adult Psychiatry, Monash Medical Centre, Clayton, Australia(KSV);and CognitiveNeuropsychiatryUnit,MentalHealthResearch Instituteof Victoria.Parkville,Australia(CP). Address reprint requests to Dr. J.G. Phillips,PsychologyDepartment. Monash University,ClaytonVIC 3168, Australia. Received April 8, 1996;revisedDecember4. 1996. © 1997 Societyof BiologicalPsychiatry
Patients had minimal abnormal involuntary movements, being screened by referring psychiatrists using the abnormal involuntary movement scale (AIMS) examination technique. Patients were either unmedicated (2) or medicated with clozapine (9), risperidone (3), thioridazine (1), or "typical" antipsychotics (5; haloperidol, flupenthixol, trifluoperazine, and fluphenazine). Of those 5 patients on "typical" antipsychotics, 4 were also on anticholinergics (benztropine). Eighteen patients were right- and 2 were left-handed (determined by handedness questionnaire; Bradshaw et al 1990). Controls were matched to patients for age, gender, and handedness. A WACOM SD 420 graphics tablet sampled position of a noninking pen (every 5 msec) as x and y coordinates. Participants wrote, with the preferred and nonpreferred hand, four continuous loops (variations of cursive 'T's) to a height of approximately 16 mm. To ensure homologous muscle groups were used and to control biomechanical differences (direction of rotation): the nonpreferred hand performed movements mirror image to those of the preferred hand; participants rested their lower forearm on the edge of the tablet; and clockwise and anticlockwise movements were sampled. There were four conditions involving hand (preferred/nonpreferred) and rotation (guirland/arcade; Sovik and Arntzen 1991) in the 2 x 2 x 2 design (see Figure 1). Conditions were counterbalanced, each being practised on lined paper (inking pen) and then upon the graphics tablet (noninking pen), maintaining stroke size and comfortable speed. The last 10 complete trials in each condition were analyzed. Vertical components of handwriting strokes were selected using interactive computer graphics, filtered, and features of interest then extracted by automatic algorithms (Phillips et al 1991, 1994). The average stroke duration (msec) provided a measure of 0006-3223/97/$17.00 PII S0006-3223(96)00544-6
Brief Reports
BIOL PSYCHIATRY 1997;41:830-833
t $
831
t $
16 mm
16 mm
4 Guirlands - Preferred hand
Mirrored Guirlands (M-Guirlands) - Non-preferred hand
1' $
t $
16 mm
16 mm
Mirrored Arcades (M-Arcades) - Non-preferred hand
Arcades - Preferred hand
Figure 1. The four conditions employed in the study. In accordance with the handwriting literature, guirlands refer to preferred hand "counterclockwise movements" and arcades refer to preferred hand "clockwise movements" (Sovik and Arntzen 1991, p 78). Arrows indicate the direction of the movement.
bradykinesia. The average stroke length (mm) provided a measure of micrographia or macrographia. The consistency of stroke length and duration were indicated by the ratio of the mean to its standard deviation. High values reflect consistent control of movement patterns, whereas low values reflect inconsistency. Force inefficiency was indicated by the ratio of the number of zero crossings in the acceleration function to the number of zero crossings in the velocity function. The skewness coefficient, the ratio of the time from zero to peak velocity (acceleration phase) to the total movement time, described the relative proportion of time spent in acceleration during the writing stroke. Additional
writing strokes over those required (see Figure 1) were considered perseverations.
Results The dependent variables were submitted to a mixed model 2 X 2 × 2 analysis of variance (ANOVA) to compare between groups (patients, controls) with repeated measures upon hand (preferred, nonpreferred) and rotation (guirland, arcade) (see Table 1). Altered functional asymmetries were indicated by
Table 1. Mean Handwriting Indices for Patients and Controls
Stroke duration (msec) Stroke length (ram) Duration consistency Length consistency Force inefficiency Skewness coeffÉcient ~Trend,p = .06. ~'p < .01. 'p < .05.
Patients [mean (SD)]
Controls [mean (SD)]
466 (97) 23.48 (5.83) 5.62 ( 1.03) 7.88 ( 1.87) 2.92 (0.92) .496 (.024)
436 (84) 20.61 (3.33) 7.08 (1.10) 10.18 (2.11 ) 2.18 (0.71 ) .491 (.026)
Group effect F(1,38) = F(1,38) = F( 1,38) = F( 1,38) = F( 1,38) = F(1,38) =
1.06 3.66" 18.94~ 13.36b 7.95b 0.38
Group by hand interaction F(1,38) = /=(1,38) = F( 1,38) = F(1,38) = F(1,38) = F(1,38) =
0.18 0.90 4.87c 0.40 0.56 1.64
832
BIOL PSYCHIATRY 1997;41:830-833
group by hand interactions. Extrapyramidal signs were indicated by group main effects. Overall, schizophrenic patients exhibited similar differences between preferred and nonpreferred hands to controls, indicating normal functional asymmetries. Although the handwriting of patients was not bradykinesic (slow), it was significantly less efficient and consistent, and there was a trend toward macrographic (bigger) strokes. In addition, significantly more perseverative responses were observed in the patient group (8% of all recorded trials) than the controls (0.25%) (z = 9.55, p < .01). Anomalous functional asymmetries only occurred for stroke duration consistency. Whereas controls' movements were of more consistent duration with preferred (7.82) than nonpreferred (6.34) hands, this was less appreciable for the preferred (5.87) and nonpreferred (5.37) hands of patients. Post hoc analysis examined contributions of medication. Patients were ordered by medication type for any expected increase in extrapyramidal symptoms [i.e., unmedicated (n = 2), atypical (n = 9), borderline (neither typical or atypical-risperidone and thioridazine; n = 4), typical neuroleptics (n = 5)]. The Jonckheere statistic (Siegel and Castellan 1988) showed that medication did not affect force inefficiency (J* = 1.1468, p > .05, two tailed) or length consistency (J* = 1.807, p > .05, two tailed), but did affect duration consistency (J* = 2.05, p < .05). Movement duration consistency in unmedicated (mean = 5.38) and atypical (mean = 5.01) patients improved for "borderline" (mean = 6.71) and typical neuroleptic (mean = 5.93) patients.
Discussion There was little evidence of reduced hemispheric specialization in schizophrenia with only one measure (consistency of stroke duration) demonstrating altered functional asymmetries of handwriting movements. Functional asymmetries observed in schizophrenia were otherwise similar to those of neurologically healthy adults. Thus although altered structural asymmetries have been reported (Crow 1990), there was little indication here of altered functional asymmetry. Perhaps altered asymmetry is only a marker for underlying pathology, having a correlational, rather than a causal, role in schizophrenia. Instead, schizophrenic patients' handwriting exhibited similar motor disturbances to those of BG disorders (Pantelis et al 1992).
Brief Reports
Table 2. Kinematic Characterization of Handwriting (Relative to Age-Matched Controls), for Patients with Parkinson's Disease (PD), Huntington's Disease (HD), and Schizophrenia PD
HD
Stroke characteristics Duration Longer ",b ?Longer c.a Length ?Shorter" ?Longeff/normal c'd Stroke consistency Duration Norma( Lessd Length Normal/ Less (trend)d Stroke trajectory Efficiency Less/ Less d Skew '~ Acceleration b ?Normal" Perseveration None b.j More,t.e
Schizophrenia Normal ?Longer Less Less Less Normal More
aMargolin and Wing 1983. t'Phillips et al 1989. ~Phillips et al 1995. aphillips et al 1994. ePodoll et al 1988. /Phillips et al 1991. Table 2 compares the present results to previously observed BG disorders (Parkinson's disease, PD; Huntington's disease, HD). As some patients were on typical neuroleptics (25%), we might expect extrapyramidal side effects and similarities to PD. Considering differences between PD and HD patients and their age-matched controls in such handwriting tasks, patients with schizophrenia resembled PD but especially HD patients. These similarities are not simply extrapyramidal side effects, since there was no apparent effect of medication upon our measure of extrapyramidal symptoms (force inefficiency), with instead an improvement on a measure (consistency of duration) previously sensitive to chorea (Phillips et al 1994). Conversely, since clozapine patients had been off typical neuroleptics for months (mean = 8.2 months, SD = 3.0 months), this was probably not withdrawal dyskinesia. Although drug-naive patients, and patients with predominantly positive or negative symptomatology should also be considered, the present findings do suggest a disturbance at some level in frontal-subcortical circuitry in schizophrenia (Pantelis et al 1992).
We gratefully acknowledge the assistance of Dr. David Leonard, Dr. Geoff Stuart, Deirdre Smith, and Mornington Peninsula Hospital.
References Bradshaw JL, Bradshaw JA, Nettleton NC (1990): Abduction, adduction and hand differences in simple and serial movements. Neuropsychologia 28:917-931.
Phillips JG, Stelmach G, Teasdale N (1989): Preliminary assessment of spatiotemporal control of handwriting in parkinsonians. In Plamondon R, Suen CY, Simner ML (eds), Com-
Crow TJ (1990): Temporal lobe asymmetries as the key to the etiology of schizophrenia. Schizophr Bull 16:433-444.
puter Recognition and Human Production of Handwriting.
Margolin DI, Wing AM (1983): Agraphia and micrographia: Clinical manifestations of motor programming and wrformance disorders. Acta Psychol (Amst) 54:263-283.
Phillips JG, Stelmach G, Teasdale N (1991): What can indices of handwriting quality tell us about parkinsonian handwriting? Hum Mov Sci 10:301-314.
Pantelis C, Barnes TRE, Nelson HE (1992): Is the concept of frontal-subcortical dementia relevant to schizophrenia? Br J Psychiatry 160:442-460.
Phillips JG, Bradshaw JL, Chiu E, Bradshaw JA (1994): Characteristics of handwriting of patients with Huntington's disease. Mov Disord 9:521-539.
Singapore: World Scientific, pp 317-331.
Brief Reports
BIOL PSYCHIATRY
833
1997:41:830-833
Phillips JG, Chiu E, Bradshaw JL, Iansek R (1995): Impaired movement sequencing in patients with Huntington's disease: A kinematic analysis. Neuropsychologia 33:365-369. Podoll K, Caspary P, Lange HW, Noth J (1988): Language functions in Huntington's disease. Brain 111:1475-1503. Sandyk R, Kay SR (1990): Is negative schizophrenia a variant of parkinsonism? Int J Neurosci 53:235-240.
Siegel S, Castellan NJ (1988): Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Sovik N, Arntzen O (1991): A developmental study of the relation between movement patterns in letter combinations (words) and writing. In Wann J, Wing AM, Sovik N (eds), Development of Graphic Skills. San Diego, CA: Academic Press, pp 77-90.
Introduction Any motor dysfunction in schizophrenia could provide insights into underlying functional disturbance. Motor incoordination in schizophrenia could reflect disturbed subcortical function (Pantelis et al 1992; Sandyk and Kay 1990). We have previously kinematically documented handwriting of patients with basal ganglia (BG) diseases known to affect the speed and size of handwriting strokes (Phillips et al 1991 1994). Chorea reduces consistency of handwriting (Phillips et al 1994), and bradykinesic movements are inefficient, sometimes requiring prolonged periods of acceleration (Phillips et al 1989). Alternatively, schizophrenic motor incoordination could be a soft sign, with reduced preferred/nonpreferred hand differences indicating abnormalities of hemispheric specialization (Crow 1990). Since writing hand preference is an important test of handedness, we asked whether patients with schizophrenia exhibit extrapyramidal signs or altered functional asymmetries, by kinematically analyzing their handwriting movements.
Methods Twenty schizophrenic patients diagnosed under DSM-IV criteria (12 male and 8 female) had a mean age of 31.1 (range 18-46, SD 8.0) years and a mean illness duration of 9.9 (SD 7.3) years. From the Department of Psychology, Monash University,Clayton, Australia (RMG, JGP, JLB); Adult Psychiatry, Monash Medical Centre, Clayton, Australia(KSV);and CognitiveNeuropsychiatryUnit,MentalHealthResearch Instituteof Victoria.Parkville,Australia(CP). Address reprint requests to Dr. J.G. Phillips,PsychologyDepartment. Monash University,ClaytonVIC 3168, Australia. Received April 8, 1996;revisedDecember4. 1996. © 1997 Societyof BiologicalPsychiatry
Patients had minimal abnormal involuntary movements, being screened by referring psychiatrists using the abnormal involuntary movement scale (AIMS) examination technique. Patients were either unmedicated (2) or medicated with clozapine (9), risperidone (3), thioridazine (1), or "typical" antipsychotics (5; haloperidol, flupenthixol, trifluoperazine, and fluphenazine). Of those 5 patients on "typical" antipsychotics, 4 were also on anticholinergics (benztropine). Eighteen patients were right- and 2 were left-handed (determined by handedness questionnaire; Bradshaw et al 1990). Controls were matched to patients for age, gender, and handedness. A WACOM SD 420 graphics tablet sampled position of a noninking pen (every 5 msec) as x and y coordinates. Participants wrote, with the preferred and nonpreferred hand, four continuous loops (variations of cursive 'T's) to a height of approximately 16 mm. To ensure homologous muscle groups were used and to control biomechanical differences (direction of rotation): the nonpreferred hand performed movements mirror image to those of the preferred hand; participants rested their lower forearm on the edge of the tablet; and clockwise and anticlockwise movements were sampled. There were four conditions involving hand (preferred/nonpreferred) and rotation (guirland/arcade; Sovik and Arntzen 1991) in the 2 x 2 x 2 design (see Figure 1). Conditions were counterbalanced, each being practised on lined paper (inking pen) and then upon the graphics tablet (noninking pen), maintaining stroke size and comfortable speed. The last 10 complete trials in each condition were analyzed. Vertical components of handwriting strokes were selected using interactive computer graphics, filtered, and features of interest then extracted by automatic algorithms (Phillips et al 1991, 1994). The average stroke duration (msec) provided a measure of 0006-3223/97/$17.00 PII S0006-3223(96)00544-6
Brief Reports
BIOL PSYCHIATRY 1997;41:830-833
t $
831
t $
16 mm
16 mm
4 Guirlands - Preferred hand
Mirrored Guirlands (M-Guirlands) - Non-preferred hand
1' $
t $
16 mm
16 mm
Mirrored Arcades (M-Arcades) - Non-preferred hand
Arcades - Preferred hand
Figure 1. The four conditions employed in the study. In accordance with the handwriting literature, guirlands refer to preferred hand "counterclockwise movements" and arcades refer to preferred hand "clockwise movements" (Sovik and Arntzen 1991, p 78). Arrows indicate the direction of the movement.
bradykinesia. The average stroke length (mm) provided a measure of micrographia or macrographia. The consistency of stroke length and duration were indicated by the ratio of the mean to its standard deviation. High values reflect consistent control of movement patterns, whereas low values reflect inconsistency. Force inefficiency was indicated by the ratio of the number of zero crossings in the acceleration function to the number of zero crossings in the velocity function. The skewness coefficient, the ratio of the time from zero to peak velocity (acceleration phase) to the total movement time, described the relative proportion of time spent in acceleration during the writing stroke. Additional
writing strokes over those required (see Figure 1) were considered perseverations.
Results The dependent variables were submitted to a mixed model 2 X 2 × 2 analysis of variance (ANOVA) to compare between groups (patients, controls) with repeated measures upon hand (preferred, nonpreferred) and rotation (guirland, arcade) (see Table 1). Altered functional asymmetries were indicated by
Table 1. Mean Handwriting Indices for Patients and Controls
Stroke duration (msec) Stroke length (ram) Duration consistency Length consistency Force inefficiency Skewness coeffÉcient ~Trend,p = .06. ~'p < .01. 'p < .05.
Patients [mean (SD)]
Controls [mean (SD)]
466 (97) 23.48 (5.83) 5.62 ( 1.03) 7.88 ( 1.87) 2.92 (0.92) .496 (.024)
436 (84) 20.61 (3.33) 7.08 (1.10) 10.18 (2.11 ) 2.18 (0.71 ) .491 (.026)
Group effect F(1,38) = F(1,38) = F( 1,38) = F( 1,38) = F( 1,38) = F(1,38) =
1.06 3.66" 18.94~ 13.36b 7.95b 0.38
Group by hand interaction F(1,38) = /=(1,38) = F( 1,38) = F(1,38) = F(1,38) = F(1,38) =
0.18 0.90 4.87c 0.40 0.56 1.64
832
BIOL PSYCHIATRY 1997;41:830-833
group by hand interactions. Extrapyramidal signs were indicated by group main effects. Overall, schizophrenic patients exhibited similar differences between preferred and nonpreferred hands to controls, indicating normal functional asymmetries. Although the handwriting of patients was not bradykinesic (slow), it was significantly less efficient and consistent, and there was a trend toward macrographic (bigger) strokes. In addition, significantly more perseverative responses were observed in the patient group (8% of all recorded trials) than the controls (0.25%) (z = 9.55, p < .01). Anomalous functional asymmetries only occurred for stroke duration consistency. Whereas controls' movements were of more consistent duration with preferred (7.82) than nonpreferred (6.34) hands, this was less appreciable for the preferred (5.87) and nonpreferred (5.37) hands of patients. Post hoc analysis examined contributions of medication. Patients were ordered by medication type for any expected increase in extrapyramidal symptoms [i.e., unmedicated (n = 2), atypical (n = 9), borderline (neither typical or atypical-risperidone and thioridazine; n = 4), typical neuroleptics (n = 5)]. The Jonckheere statistic (Siegel and Castellan 1988) showed that medication did not affect force inefficiency (J* = 1.1468, p > .05, two tailed) or length consistency (J* = 1.807, p > .05, two tailed), but did affect duration consistency (J* = 2.05, p < .05). Movement duration consistency in unmedicated (mean = 5.38) and atypical (mean = 5.01) patients improved for "borderline" (mean = 6.71) and typical neuroleptic (mean = 5.93) patients.
Discussion There was little evidence of reduced hemispheric specialization in schizophrenia with only one measure (consistency of stroke duration) demonstrating altered functional asymmetries of handwriting movements. Functional asymmetries observed in schizophrenia were otherwise similar to those of neurologically healthy adults. Thus although altered structural asymmetries have been reported (Crow 1990), there was little indication here of altered functional asymmetry. Perhaps altered asymmetry is only a marker for underlying pathology, having a correlational, rather than a causal, role in schizophrenia. Instead, schizophrenic patients' handwriting exhibited similar motor disturbances to those of BG disorders (Pantelis et al 1992).
Brief Reports
Table 2. Kinematic Characterization of Handwriting (Relative to Age-Matched Controls), for Patients with Parkinson's Disease (PD), Huntington's Disease (HD), and Schizophrenia PD
HD
Stroke characteristics Duration Longer ",b ?Longer c.a Length ?Shorter" ?Longeff/normal c'd Stroke consistency Duration Norma( Lessd Length Normal/ Less (trend)d Stroke trajectory Efficiency Less/ Less d Skew '~ Acceleration b ?Normal" Perseveration None b.j More,t.e
Schizophrenia Normal ?Longer Less Less Less Normal More
aMargolin and Wing 1983. t'Phillips et al 1989. ~Phillips et al 1995. aphillips et al 1994. ePodoll et al 1988. /Phillips et al 1991. Table 2 compares the present results to previously observed BG disorders (Parkinson's disease, PD; Huntington's disease, HD). As some patients were on typical neuroleptics (25%), we might expect extrapyramidal side effects and similarities to PD. Considering differences between PD and HD patients and their age-matched controls in such handwriting tasks, patients with schizophrenia resembled PD but especially HD patients. These similarities are not simply extrapyramidal side effects, since there was no apparent effect of medication upon our measure of extrapyramidal symptoms (force inefficiency), with instead an improvement on a measure (consistency of duration) previously sensitive to chorea (Phillips et al 1994). Conversely, since clozapine patients had been off typical neuroleptics for months (mean = 8.2 months, SD = 3.0 months), this was probably not withdrawal dyskinesia. Although drug-naive patients, and patients with predominantly positive or negative symptomatology should also be considered, the present findings do suggest a disturbance at some level in frontal-subcortical circuitry in schizophrenia (Pantelis et al 1992).
We gratefully acknowledge the assistance of Dr. David Leonard, Dr. Geoff Stuart, Deirdre Smith, and Mornington Peninsula Hospital.
References Bradshaw JL, Bradshaw JA, Nettleton NC (1990): Abduction, adduction and hand differences in simple and serial movements. Neuropsychologia 28:917-931.
Phillips JG, Stelmach G, Teasdale N (1989): Preliminary assessment of spatiotemporal control of handwriting in parkinsonians. In Plamondon R, Suen CY, Simner ML (eds), Com-
Crow TJ (1990): Temporal lobe asymmetries as the key to the etiology of schizophrenia. Schizophr Bull 16:433-444.
puter Recognition and Human Production of Handwriting.
Margolin DI, Wing AM (1983): Agraphia and micrographia: Clinical manifestations of motor programming and wrformance disorders. Acta Psychol (Amst) 54:263-283.
Phillips JG, Stelmach G, Teasdale N (1991): What can indices of handwriting quality tell us about parkinsonian handwriting? Hum Mov Sci 10:301-314.
Pantelis C, Barnes TRE, Nelson HE (1992): Is the concept of frontal-subcortical dementia relevant to schizophrenia? Br J Psychiatry 160:442-460.
Phillips JG, Bradshaw JL, Chiu E, Bradshaw JA (1994): Characteristics of handwriting of patients with Huntington's disease. Mov Disord 9:521-539.
Singapore: World Scientific, pp 317-331.
Brief Reports
BIOL PSYCHIATRY
833
1997:41:830-833
Phillips JG, Chiu E, Bradshaw JL, Iansek R (1995): Impaired movement sequencing in patients with Huntington's disease: A kinematic analysis. Neuropsychologia 33:365-369. Podoll K, Caspary P, Lange HW, Noth J (1988): Language functions in Huntington's disease. Brain 111:1475-1503. Sandyk R, Kay SR (1990): Is negative schizophrenia a variant of parkinsonism? Int J Neurosci 53:235-240.
Siegel S, Castellan NJ (1988): Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Sovik N, Arntzen O (1991): A developmental study of the relation between movement patterns in letter combinations (words) and writing. In Wann J, Wing AM, Sovik N (eds), Development of Graphic Skills. San Diego, CA: Academic Press, pp 77-90.