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Original Paper

Neuropsychobiology 2009;60:8086

DOI: 10.1159/000236448

Quantitative Motor ActivityDifferentiates Schizophrenia Subtypes

Sebastian Walther Helge Horn Nadja Razavi Philipp Koschorke

Thomas J. Mller Werner Strik

University Hospital of Psychiatry, University of Bern, Bern, Switzerland

quantitative motor activity. The increased duration of im-

mobility appears to be the special feature of catatonic

schizophrenia. Copyright 2009 S. Karger AG, Basel

Introduction

The quality and frequency of motor symptoms in

schizophrenia have been accorded importance in the di-agnosis of subtypes and were described in detail in clas-sical psychopathology [1, 2]. Today, their prevalence andthus the diagnosis of catatonia appears to be decreasing,and their clinical distinction from neuroleptic side effectsis unreliable [3, 4].

Motor symptoms, however, occur frequently in schizo-phrenia. In fact, 50% of a schizophrenia group were foundto present at least 1 motor symptom during the acutestage [5]. Further, motor symptoms are still part of thediagnostic criteria for schizophrenia in DSM-IV andICD-10. They are necessary for the diagnosis of the cata-

tonic subtype of schizophrenia even if the mere presenceof motor symptoms is not sufficient in either classifica-tion system. Instead, a predominance of motor symptomsis required to allow the diagnosis of catatonia.

Research interest in motor symptoms of schizophreniahas increased within the past 2 decades, and several stud-ies suggest an important role for the motor system in thisdisorder. The development of motor abilities has been re-

Key Words

Actigraphy Catatonia Psychosis Motor retardation

Negative syndrome Antipsychotics

Abstract

Background:Motor symptoms are frequent in schizophre-

nia and relevant to the diagnosis of subtypes. However, the

assessment has been limited to observations recorded in

scales and experimental designs. The aim of this study wasto use wrist actigraphy to obtain motor activity data in 3

schizophrenia subtypes. Methods: In total, 60 patients

with schizophrenia (35 paranoid, 12 catatonic, 13 disorga-

nized) were investigated using continuous wrist actigraphy

over 24 h in an inpatient setting on average 38 days after

admission. Data of the wakeful hours of the day were ana-

lyzed. Results: The activity level was predicted by schizo-

phrenia subtype and by the type of antipsychotic medica-

tion. The movement index and mean duration of

uninterrupted immobility were found to be predicted only

by the schizophrenia subtype. Age, gender, duration of ill-

ness and chlorpromazine equivalents did not contribute tothe variance of the activity data. A MANOVA demonstrated

the significant differences in the 3 parameters between

schizophrenia subtypes (p = 0.001). Patients with catatonic

schizophrenia had lower activity levels, a lower movement

index and a longer duration of immobility than those with

paranoid schizophrenia. Conclusions: Schizophrenia sub-

types can be differentiated using objective measures of

Received: January 27, 2009

Accepted after revision: June 23, 2009

Published online: September 10, 2009

Sebastian Walther, MDUniversity Hospital of PsychiatryBolligenstrasse 111

CH3060 Bern (Switzerland)Tel. +41 31 930 9111, Fax +41 31 930 9404, E-Mail [email protected]

2009 S. Karger AG, Basel0302282X/09/06020080$26.00/0

Accessible online at:www.karger.com/nps

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Motor Activity in SchizophreniaSubtypes

Neuropsychobiology 2009;60:8086 81

peatedly shown to be delayed in children who later sufferfrom schizophrenia [68]. A body of evidence supportsimpaired motor control and motor sequencing in schizo-phrenia [911]. Reduced volume in the cerebellum inschizophrenia was reported [8, 12] and thought to relate todisturbances of the motor system. Gait disturbances have

been observed in patients with schizophrenia [13] as wellas bradykinesia in 818% of the neuroleptic-nave patients[14]. Parkinsonism and dyskinesia were demonstrated tobe related to psychopathology in neuroleptic-nave first-episode patients [15]. In addition, several studies on neu-rological soft signs have reported motor disturbances inboth treated and untreated schizophrenia [1619].

The assessment of motor symptoms, however, is chal-lenging and often limited to clinical observation and spe-cific rating scales. On the other hand, studies relying onquantitative measurements usually depended on labora-tory settings [11, 20, 21]. To obtain information about the

motor behavior of schizophrenic patients in naturalisticenvironments, objective quantitative measurements areneeded.

Actigraphy is a validated tool in sleep medicine and hasbecome important for motion analysis in psychiatric re-search [22]. However, only few studies on quantitative mo-tor activity during wakefulness have been conducted inschizophrenia using actigraphy [2325]. Farrow et al. [23,24] reported a negative correlation of the cumulated activ-ity counts with avolition. We have reported higher motoractivity levels (AL) in cycloid psychoses as compared toparanoid schizophrenia [26] and poor correlation between

objective motor activity and expert ratings [27]. In addi-tion, disturbances of the sleep-wake cycle as measured byactigraphy were reported in schizophrenia [2830].

We were interested whether DSM-IV schizophreniasubtypes would differ with regard to quantitative motoractivity as measured by actigraphy. In particular, we hy-pothesized that specific motor features of catatonicschizophrenia could be identified compared to the otherschizophrenic subtypes. Further, based on the fact thatthe clinical distinction between catatonic and drug-induced movement disorders is unreliable, we exploredthe possibility whether objective movement parameters

would be more reliable to discriminate them.

Subjects and Methods

SubjectsStudy participants were recruited during the f irst 3 weeks after

admission to the inpatient department of the University Hospitalof Psychiatry Bern, Switzerland. The inclusion criterion was a

DSM-IV diagnosis of schizophrenia based upon clinical inter-views and review of al l records available, taking into account thelongitudinal course of the disorder. The exclusion criteria were ahistory of or concomitant neurological or medical disorder, orsubstance abuse (except for nicotine). Participation was unpaid.Sixty-three patients were included in the study with an overlapwith the sample reported earlier [27]. Three of the patients re-

ceived anticholinergic drugs which may inf luence motor activityand were excluded from the f inal analyses.Chlorpromazine equivalents were calculated according to Rey

et al. [31] and Woods [32]. In addition, 14 patients were also treatedwith antidepressants for the negative syndrome in schizophrenia.Seven received a selective serotonin reuptake inhibitor, 1 a selectivenoradrenaline reuptake inhibitor , 3 a selective serotonin and nor-adrenaline reuptake inhibitor, and 3 patients were on tricyclic anti-depressants. No difference in antidepressant prescription was de-tected between the schizophrenia subgroups (2 = 5.515; d.f. = 8; p= 0.773). The demographic and clinical variables are displayed intable 1. After a complete explanation of the aims and procedures ofthe study, the patients provided written informed consent. The pro-cedures are in accordance with the declaration of Helsinki and hadbeen approved by the local ethics committee (KEK No. 208/06).

MeasuresThe patients were interviewed and assessed using the Positive

and Negative Syndrome Scale (PANSS) [33]. In addition, theywore an actigraph (Actiwatch, Cambridge NeurotechnologyInc., UK) on the wrist of the nondominant arm for 24 consecutivehours for the continuous recording of motor activity. Handednesswas determined by asking the patients about the preferred handwhen writing, brushing teeth and eating with a spoon.

Motor Activity ParametersMovement counts of the actigraph were stored in 2-second in-

tervals, allowing continuous recording for a maximum of 36 h onthe 64-kB memory. We chose the smallest possible interval to

achieve maximum temporal resolution. The nondominant armwas chosen because it ref lects average movement during day- andnighttime, while actigraphy in the dominant arm represents max-imum movements that are strongly related to manual work oractivities [34]. The start of measurement varied between 10: 00and 15: 00, but for the analyses we included the whole 24-hourcycle, so each hour of the day was covered. In 3 participants (1 ofeach subtype), however, we failed to record complete 24-hour da-tasets as these patients removed their actigraphs during sleep.

Motor activity is subject to circadian rhythms. By investigatinginpatients of 1 large psychiatric university hospital we had thechance to normalize external and socia l rhythms. The patients onall wards get up around 7: 00, have breakfast at 07: 30, lunch at11: 30 and dinner at around 18: 00. Also, they are engaged in sev-

eral group activities during the day and have social contact until22: 00, when the l ights are usual ly turned off. Measurements wereperformed exclusively during weekdays to assure that there wasequal impact of group therapies across the participants. At the endof the recording, the patients were asked to provide sleep log in-formation and to fill in the Pittsburgh Sleep Quality Index [35].

Data AnalysisThe data were analyzed using Sleep Analysis 5 (Cambridge

Neurotechnology) and EXCEL templates for further analyses.

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Walther/Horn/Razavi/Koschorke/Mller/Strik


Using the sleep log information, we removed data collected dur-ing sleep. We chose to extract 3 parameters from the data that hadpreviously been descr ibed [34] and used in schizophrenia [26, 27].AL is the mean number of activity counts per hour. The move-ment index (MI) is the percentage of periods with an activitycount 10, reflecting the proportion of 2-second periods with ac-tivity or immobility. The mean duration of uninterrupted immo-bility periods (MIP) provides a global measure of the distribution

and number of immobility periods. Further analyses were per-formed using SPSS 15.0.General linear models (GLM) were computed for AL, MI and

MIP as dependent variables using Wald 2. The main effects of thefollowing predictors were compared: schizophrenia subtype, age,gender, type of antipsychotic medication, chlorpromazine equiva-lents, number of episodes and duration of illness. Afterwards, aMANOVA using Wilks with AL, MI and MIP as dependent

variables and schizophrenia subtype as between-subject variablewas performed. Bonferroni correction was applied for multiplecomparisons. Differences between groups in the descriptive sta-tist ics were tested using 1-way ANOVAs or2 tests when appropri-ate. Correlations of activity parameters were performed usingPearsons correlation. All levels of signif icance are 2-tailed.

Results

Motor Activity during WakefulnessFor each of the motor activity parameters a GLM was

computed with the predictors schizophrenia subtype,chlorpromazine equivalents, type of antipsychotic drugs

used (none, atypical, typical or both), age, gender, num-ber of episodes and duration of illness. The GLM of ALdemonstrated a significant main effect for schizophreniasubtype (2 = 6.055, p = 0.014) and type of antipsychotictreatment (2 = 3.861, p = 0.049). However, an ANOVAfor AL with schizophrenia subtype and type of antipsy-chotic failed to detect an interaction of both factors

(F5, 60 = 0.984, p = 0.437).When we performed an independent t test on AL, we

found a nonsignificant trend towards higher AL in thepatients treated with atypical antipsychotic drugs only(T40 = 1.853, d.f. = 38, p = 0.072). However, the type ofantipsychotic drug used was comparable between theschizophrenia subtypes (see table 1).

The GLM of MI found a significant main effect onlyfor schizophrenia subtype (2 = 5.968, p = 0.015). Simi-larly, the GLM of MIP showed a significant main effectonly for the predictor schizophrenia subtype (2 = 11.563,p !0.001). None of the other predictors had a signif icant

main effect on any of the activity parameters.As the GLMs revealed schizophrenia subtype to have

a main effect on motor activity parameters, these 3 pa-rameters were entered as dependent variables into aMANOVA with schizophrenia subtype as between-sub-ject factor. Schizophrenia subtype demonstrated a signif-icant overall effect (Wilks : F6, 60 = 4.320, p = 0.001).Significant differences between schizophrenia subtypes

Table 1. Characteristics of the schizophrenia subtypes

Characteristic Schizophrenia subtype Comparison

paranoid (n = 35) catatonic (n = 12) disorganized (n = 13) 2 d.f. p

n % n % n %

Male gender 18 51.4 6 50.0 9 69.2 1.365 2 0.523Antipsychotic treatment

None 2 5.3 0 0 1 7.7 7.151 6 0.236Typical 2 5.7 2 16.7 2 15.4Atypical 24 68.6 5 41.7 5 38.5Both 7 20.0 5 41.7 5 38.5

Mean SD Mean SD Mean SD F d.f. p

Age, years 39.60 9.64 45.50 12.19 36.23 10.26 2.602 2 0.083Duration of illness, years 10.97 8.84 6.34 5.70 14.85 10.50 2.967 2 0.059Episodes 7.31 6.21 4.25 2.96 9.38 3.55 3.049 2 0.055Chlorpromazine equivalents 488.45 350.35 566.13 537.62 718.46 659.00 1.143 2 0.326PANSS positive score 17.60 5.53 14.92 4.03 15.85 5.44 1.377 2 0.261

PANSS negative score 17.06 5.43 20.00 7.66 20.77 5.54 2.353 2 0.104PANSS total score 75.51 15.51 79.92 17.60 84.46 18.68 1.439 2 0.246

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were detected in each of the dependent variables: AL(F2, 60 = 4.629, p = 0.014), MI (F2, 60 = 3.615, p = 0.033) andMIP (F2, 60 = 10.397, p ! 0.001). The post hoc t-tests re-vealed differences between patients with catatonic andparanoid schizophrenia (see fig. 1ac). Indeed, in para-noid schizophrenia the highest AL and MI were found,while patients with catatonic schizophrenia displayed thelongest duration of immobility.

AL correlated negatively with the PANSS negativesubscore. On the other hand, the PANSS positive sub-score correlated positively with MI and negatively withMIP (see table 2). Therefore, stronger negative syndrome

severity was associated with less activity, while strongerpositive syndrome scores indicated shorter immobilityand a higher proportion of active periods.

The PANSS item score for motor retardation was high-est among catatonia patients (2 = 19.337, d.f. = 10, p =0.008). However, motor retardation to some extent wasrated frequently in each subtype (paranoid 37%, cataton-ic 91%, disorganized 47%). As expected, specific symp-

toms such as mannerism were most frequent among pa-

tients with catatonic schizophrenia (92%; 2 = 28.880,d.f. = 12, p! 0.001), while other items of the negative syn-drome were equally rated between the groups (socialavoidance: p = 0.237; lack of spontaneity: p = 0.427; blunt-ed affect: p = 0.499). Likewise, the PANSS items distur-bance of volition and depression were not rated differ-ently between the groups (p = 0.147 and p = 0.518).

SleepThe actual sleep time differed between the groups (see

table 3). No variations were identified in terms of sleepquality and motor activity during sleep.

Discussion

The results demonstrate differences in motor activityduring wakefulness in schizophrenia subtypes and sup-port our hypothesis. In fact, they diverge in terms of themagnitude of activity (AL), the relative amount of activeperiods (MI) and the mean duration of immobility (MIP).Patients with catatonic schizophrenia had a lower overallAL, lower MI and longer immobility periods as com-pared to patients with paranoid schizophrenia. No post

hoc differences were found between the disorganized andother subtypes. Even though the type of antipsychoticmedication had some unspecific effect on AL, there wasno interaction of antipsychotic and subtype associatedwith AL. All other factors presumably influencing motoractivity, such as age, gender, chlorpromazine equivalentsand duration of illness, had no effect on the parameterstested.

Table 2. Correlation of motor activity parameters and PANSS

PANSSpositive score

PANSSnegative score

PANSStotal score

r p r p r p

AL, counts/h 0.181 0.167 0.351 0.006* 0.225 0.084MI, % 0.286 0.027* 0.204 0.118 0.087 0.507MIP, s 0.286 0.027* 0.025 0.848 0.111 0.398

* p < 0.05.

0

Activ

ity

leve

l(c

ounts

/h)

Paranoid

5,000

10,000

15,000

20,000

n = 35

Catatonic

n = 12

p = 0.016

Disorganized

n = 130

Movemen

tin

dex

(%)

Paranoid

10

20

30

40

n = 35

Catatonic

n = 12

p = 0.045

Disorganized

n = 13

50

Schizophrenia type Schizophrenia type

0

Mean

durationo

f

un

interrupte

dimmo

bility

(s)

Paranoid

2

4

6

n = 35

Catatonic

n = 12

p < 0.001

Disorganized

n = 13

Schizophrenia typea b c

Fig. 1. Quantitative motor activity in schizophrenia subtypes. Bars display means + 1 SD. Post hoc comparisonsusing Bonferroni correction.

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As in an earlier study [27], reduced magnitude of motoractivity (AL) was associated with higher PANSS negativesyndrome scores. In contrast, with higher PANSS positivesyndrome scores we found a shorter duration of immobil-ity (MIP) and a higher proportion of active periods (MI).Both correlations indicated less rest during marked posi-tive syndromes. Some single PANSS items might be morerelevant to motor activity than others. As expected, motorretardation and mannerisms were rated most frequentlyin catatonic schizophrenia. Depression, lack of spontane-ity, disturbance of volition and social avoidance displayedno differences between the subtypes.

In the GLMs we found no impact of chlorpromazineequivalents on the motor activity parameters, nor could weobserve an impact of the type of antipsychotic adminis-tered on MIP and MI. In AL, however, there was a differ-ence between the types of antipsychotic administered. Onthe other hand, we failed to find specific differences in thepost hoc tests. In addition, there was no interaction of thefactors antipsychotic medication and subtype of schizo-phrenia. A nonsignificant trend towards higher activitywas observed in AL when we compared atypical versus typ-ical antipsychotics. This ambiguous result is in line withthe finding that atypical antipsychotic drugs vary substan-

tially in their ability to induce extrapyramidal side effects[36]. However, there were no differences between the groupsin terms of the prescription of antipsychotic drugs.

The most prominent difference between the subtypeswas found in the duration of immobility. Thus, our re-sults suggest that the duration of immobility could ref lectspecific catatonic symptomatology, the intrinsic motordisturbances in schizophrenia [15] or both.

Catatonic patients exhibit an irregular pattern of activ-ity with longer periods of immobility followed by activephases. This could also explain the low average AL becauselonger immobility would contribute to lower AL. Similar-ly, longer duration of immobility would decrease the pro-portion of active periods in favor of inactive periods andthereby lead to a lower MI. Our results suggest that motoractivity in catatonic schizophrenia is characterized by in-termittent inhibitions preventing the patients from regu-lar, fluent movement patterns. These phenomena, interest-ingly, are usually not perceived by clinical observation andlack operationalization in standard psychopathological

scales and diagnostic systems. In fact, no significant dif-ference in the negative syndrome was detected between thesubgroups. Motor retardation as a PANSS item was fre-quent in all subgroups, even though the scores in catatoniawere higher. Therefore, the categorization of single pa-tients as catatonic simply by the observation of reducedmotor activity is imprecise. Employing actigraphic mea-sures such as the duration of immobility could increase thequality of diagnosis, adding an objective parameter to theclinical observation of rather complex catatonic move-ment patterns like mannerisms, stereotypy, echophenom-ena, perseveration and automatic obedience.

Patients with catatonic schizophrenia were shown tohave specific deficits in decision making and set shifting,neuropsychological measures associated with ventralprefrontal cortical function [37]. Indeed, the medial pre-frontal cortex is critical to the evaluation of the relevanceof cognitive goals and motor acts [38]. Findings fromneuroimaging studies in catatonic schizophrenia report-ed a reduced cerebral blood f low in the parietal lobe [39,

Table 3. Sleep data

Schizophrenia type F d.f. p

paranoid catatonic disorganized

mean SD mean SD mean SD

PSQI 6.50 3.57 8.00 2.66 5.83 3.10 1.393 2 0.257Sleep efficiency, % 84.40 6.71 86.22 7.66 79.56 8.37 2.724 2 0.075Sleep latency, hh:mm:ss 00:28:32 00:31:06 00:27:11 00:17:41 00:41:30 00:45:16 0.775 2 0.466Actual sleep time, hh:mm:ss 07:41:38 01:36:42 08:55:05 01:28:16 06:09:45 03:21:06 5.008 2 0.010*Immobile time percent, % 91.95 5.08 91.95 7.28 88.21 8.25 1.603 2 0.211Sleep AL, counts/h 1,814.91 1,449.91 1,440.07 1,023.58 1,763.93 1,671.15 0.284 2 0.754Sleep MI, % 4.65 3.26 4.52 3.31 5.46 4.34 0.285 2 0.753Sleep MIP, s 78.55 60.05 79.33 54.24 53.23 33.75 1.034 2 0.363

* p = 0.008 (catatonic > disorganized; post hoc t test, Bonferroni correction).

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40], structural alterations in frontoparietal areas [41] andfunctional deficits in the ventromedial prefrontal cortex[42]. Another explanation for reduced motor activity incatatonia stems from the association of negative symp-toms and motor activity. In fact, negative symptoms cor-relate highly with catatonia [43] and some authors attri-

bute this to a higher vulnerability of catatonic schizo-phrenia to neuroleptic-induced negative symptoms [44].

At the current state of research, it is not possible to at-tribute quantitative motor activity to a state or trait phe-nomenon in schizophrenia subtypes. From the historicalview of schizophrenia subtypes we would conclude thatdisturbances of motor activity are stable over time andover different periods of the disorder [1, 2]. Neurologicalsoft signs, however, seem to vary with the course of thedisorder to some extent, while some symptoms remainstable after antipsychotic treatment [15, 19].

Slight differences between the groups were also docu-

mented for the actual sleep time, with disorganizedschizophrenia displaying the shortest duration. However,our data on sleep measures are only of descriptive value.They must be interpreted with caution, since longer re-cording periods are recommended for actigraphic esti-mates of sleep [29, 45].

The strength of our study is the objective motor activ-ity assessment during the wake period of a day in a patientgroup with comparable social and circadian rhythms. Inaddition, we ruled out the impact of age, gender, chlor-promazine equivalents and duration of illness on our ac-tivity data. Also, we excluded patients on anticholinergic

medication. Limitations of the study are the small num-ber of subjects with catatonic and disorganized subtypes,due to the lower prevalence. Since we did not control forthe intrinsic parkinsonism and dyskinesia reported alsoin unmedicated schizophrenia [15], patients receiving an-ticholinergic drugs against extrapyramidal side effects

were excluded. We did not, however, control for the smok-ing status, which might also inf luence motor behavior.

At entry, diagnoses were established according toDSM-IV after thorough clinical interview and review ofthe available records. However, no structured diagnosticinterview was performed. Further, it cannot be excluded

that ambidextrous patients, who use their nondominantarm more frequently than right-handed subjects, mighthave been included. Another problem is the correct inter-pretation of immobility. In sleep research, strongly re-duced activity or immobility during the day as measuredby actigraphy is defined as daytime napping (i.e. sleep)[46, 47]. Higher activity scores in short-term actigraphyare associated with signs of arousal in EEG of healthycontrols [48]. In psychiatric conditions, however, it is pos-sible to be awake and akinetic. The participants wereasked to report daytime napping in their sleep logs. Dataduring sleep periods were removed from the analysis of

the main results on activity during wakefulness (seemethods). However, we cannot rule out that some of theinformation provided by the patients was inaccurate.

To the best of our knowledge, this study is the first toreport differences in schizophrenia subtypes regarding thequantitative motor activity by objective means. The majorfinding is the increased duration of immobility periods asa specific feature of catatonic schizophrenia. Still, furtherresearch should address the specific activity pattern in dis-organized schizophrenia as well as the underlying patho-physiology of motor activity in schizophrenia subtypes. Inaddition, the duration of immobility and the MI were

found to be independent of the type and dosage of antipsy-chotic drugs and therefore may reflect intrinsic motor fea-tures of schizophrenia. Actigraphy does not distress pa-tients and may help better understand schizophrenia-spe-cific movement disorders and evaluate the treatmentoutcome, as has been previously shown in dementia [49].

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