Elsevier

Cortex

Volume 49, Issue 2, February 2013, Pages 520-527
Cortex

Research report
Impaired pantomime in schizophrenia: Association with frontal lobe function

https://doi.org/10.1016/j.cortex.2011.12.008Get rights and content

Abstract

Introduction

Gestures are important for nonverbal communication and were shown to be impaired in schizophrenia. Two categories of gestures can be differentiated: pantomime on verbal command and imitation of seen gestures. There is evidence that the neural basis of these domains may be distinct, pantomime being critically dependent on prefrontal cortex function. The aim of the study was to investigate gestural deficits in schizophrenia and their association with frontal lobe function and motor performance.

Methods

In 30 schizophrenia patients, gesture performance was assessed by the comprehensive Test of Upper Limb Apraxia (TULIA) using previously determined cut-off scores. The ratings of videotaped gesture performance were blinded. In addition, a battery of rating scales on frontal lobe function, parkinsonism, dyskinesia, catatonia and instrumental measures of gross and fine motor performance were assessed.

Results

Pantomime deficits were found in 40% and imitation deficits in 23% of the patients. Patients with gestural deficits had poorer frontal cortex function, more catatonic symptoms, and more severe psychopathology. Furthermore, trends indicated an association with a more chronic course of the illness. Pantomime was linked to frontal lobe function whereas imitation was associated with catatonic symptoms and gross motor performance.

Conclusions

Pantomime is frequently impaired in chronic schizophrenia and may critically depend on motor planning, reflecting a further example of brain disconnectivity in schizophrenia.

Introduction

Schizophrenia is characterized by symptom dimensions including positive and negative symptoms, disorganized thought, motor signs, mood symptoms, and cognition (Tandon et al., 2009). The nature of some of these symptoms has been attributed to disturbed brain connectivity (Catani and ffytche, 2005, Friston, 1998, Penzes et al., 2011).

Gestures are important for nonverbal communication as they may substitute or support language (Obermeier et al., 2012). Schizophrenia patients are impaired in nonverbal communication perception (Toomey et al., 2002) and more specifically in the perception of incidental movements as gestures (Bucci et al., 2008). Furthermore, patients show deficits in emotion recognition demonstrated by defective imitation and pantomime for facial expressions (Park et al., 2008, Schwartz et al., 2006, Tremeau et al., 2005). These deficits in nonverbal communication and emotion processing were linked to negative symptoms and poor social functioning (Bellack et al., 1990, Dickinson et al., 2007, Park et al., 2008). Schizophrenia patients were shown to produce fewer gestures during speech, which was related to affective flattening and avolition (Troisi et al., 1998). Likewise, in unmedicated patients with schizophrenia spectrum disorders spontaneous gesturing is reduced (Mittal et al., 2006).

Gesture performance on command is different from spontaneous gesturing and can be tested in two categories: imitation (production following seen gesture) and pantomime (production on verbal command). The gestures may be meaningful (symbolic) or meaningless (non-symbolic) and engage left parieto-premotor networks, particularly their inferior parts (Bohlhalter et al., 2009, Bohlhalter et al., 2011, Fridman et al., 2006, Hermsdörfer et al., 2007, Johnson-Frey et al., 2005, Kroliczak and Frey, 2009). Left lateralization for planning of gestures was found for both hands (Bohlhalter et al., 2009, Johnson-Frey et al., 2005, Kroliczak and Frey, 2009). Planning of gestures involves the left inferior frontal gyrus (BA44), inferior parts of the precentral gyrus (BA6) and the anterior cingulate, while execution engages predominantly anterior parts of the posterior parietal cortex (Fridman et al., 2006). The findings of left hemisphere specialization in gesture production of healthy subjects have been corroborated by lesion studies (Goldenberg et al., 2007).

Impaired imitation of simple motor tasks and facial expression has been reported in schizophrenia (Park et al., 2008). The impairments in imitation of hand gestures, mouth movements and facial expressions were found to be strongly correlated to poor social competence and negative symptoms. Therefore it was concluded, that the imitation deficit is due to prefrontal cortex dysfunction either linked to the negative syndrome or to impaired mirror movements (Park et al., 2008). In a subsequent study of the same group, impaired imitation of hand gesture in schizophrenia was related to working memory function (Matthews et al., in press). Again, negative symptoms were associated with poor performance in a task of higher working memory demand.

The only prior study of gesture pantomime in schizophrenia applied an apraxia test covering the relevant semantic categories of meaningless and meaningful gestures in 21 patients (Martin et al., 1994). Movements of patients were “more clumsy, coarse and less extensive in space and time” compared to controls. Still, no clear-cut apraxic syndrome was found. The study found frequent impairments in gestures associated with tool use in schizophrenia, namely the body part as object errors. This error occurs for instance, when a patient uses the index finger like a toothbrush instead of indicating a hand position as if holding a toothbrush. Patients presenting with body part as object errors had longer duration of illness. However, the methods applied in this study were not validated.

Schizophrenia has been conceptualized as a disconnection syndrome, in which complex interaction of distinct brain areas is disturbed, leading to inefficient or erroneous higher order brain functions (Friston, 1998, Stephan et al., 2009, Walterfang et al., 2006). As gesture production critically depends on a fronto-parietal network (Catani and ffytche, 2005, Goldenberg, 2009), schizophrenic patients may be especially prone to gestural deficits of underlying network dysfunction. Structural and functional alterations have been reported for motor and premotor cortices in schizophrenia (Exner et al., 2006, Schröder et al., 1995, Walther et al., 2011b). Furthermore, motor symptoms such as parkinsonism, catatonia and abnormal involuntary movements are frequently observed in both medication naïve and medicated patients with schizophrenia (Ismail et al., 2001, Janno et al., 2004, Peralta et al., 2010, Peralta and Cuesta, 2011, Ungvari et al., 2005, Whitty et al., 2009). These motor abnormalities may confound gesture production (Grossman et al., 1991, Vanbellingen et al., 2011). Given that gesture production depends on an intact fronto-parietal network function, we aimed to test whether gestural deficits in schizophrenia were related to frontal cortex dysfunction, clinical variables or motor performance.

To measure gesture performance, the recently developed Test of Upper Limb Apraxia (TULIA) (Vanbellingen et al., 2010) was applied in schizophrenia patients. In order to elucidate the impact of impairments of fine and gross motor deficits on the gesture performance, we additionally used the coin rotation task (CR) (Gebhardt et al., 2008, Quencer et al., 2007) and wrist actigraphy on the same day. A set of clinical and motor rating scales was further used to explore any association with gesture production. We hypothesized that a considerable proportion of schizophrenia patients were impaired in gesturing. Furthermore, we expected gesture performance to be related to frontal function, illness duration, negative syndrome scores and motor performance.

Section snippets

Patients

Participants were inpatients of the University Hospital of Psychiatry at the time of study. Inclusion criteria were DSM-IV diagnosis of schizophrenia or schizoaffective disorder, age 18–65 years, sufficient German language skills for participation and right handedness. Exclusion criteria were substance abuse or dependence other than nicotine, history of head injuries with subsequent loss of conscience, medical or neurological impairments that would interfere with motor or praxis testing.

Predominant pantomime deficit in schizophrenia

Twelve of 30 patients (40%) displayed deficits in the TULIA. The proportion of patients with deficits was higher for pantomime (40%) than for imitation (23%). Every person with imitation deficits had pantomime deficits as well. Most frequent gestural errors observed were body-part-as-object, omissions and errors in spatial orientation. To a lesser extent content errors such as substitutions were detected. We compared clinical data, gross motor activity and coin rotation performance between the

Discussion

The present study aimed to objectively assess gesture performance in schizophrenia and to relate it to frontal lobe function and motor phenomena. We applied a validated test of gestural performance with blinded video-based ratings. According to previously determined cut-off scores (Vanbellingen et al., 2010), a considerable proportion of patients presented a gestural deficit (40%) being more impaired during pantomime than during imitation. Frequent errors were body-part-as-object errors,

Role of the funding source

There was no funding for this study.

Conflict of interest

The authors have no conflict of interest with this work.

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