Research reportStructural brain correlates of defective gesture performance in schizophrenia
Introduction
Hand gestures are important for nonverbal communication (Cartmill, Beilock, & Goldin-Meadow, 2012). In addition, gestures allow studying cerebral action representation in health and disease, such as apraxia (Steele, Ferrari, & Fogassi, 2012). Gesturing can be elicited either by a verbal command that specifies the content of the gesture or by demonstration and subsequent imitation of the gesture. The gesture may be meaningful or meaningless. Meaningful gestures may either have a conventionally agreed meaning (e. g., thumbs up for “okay”) or refer to tools and their actions (e. g., the typical movement of hammering). Out of the possible combinations of mode of elicitation (verbal command vs imitation) and content (meaningless, tool use, conventional meaning) we concentrate on imitation of meaningless gestures on the one hand and production of meaningful gestures on verbal command on the other. To facilitate the comparison with other studies using different nomenclature we note that gestures referring to tool use have also been classified “pantomime of tool use” and “transitive gestures”, whereas gestures with a conventional meaning have been termed “emblems” and “intransitive” gestures.
Action planning and its neuroanatomical representation are lively debated in behavioral and neuroimaging studies. Two action systems are currently discussed, including a ventro-dorsal stream running from primary visual cortex to middle temporal gyrus (MTG) to the inferior parietal lobe (IPL) to the ventral premotor cortex (PMv) – and a dorso-dorsal stream connecting primary visual cortex, V6, intraparietal sulcus (IPS), superior parietal lobe (SPL) and dorsal premotor cortex (PMd) (Binkofski and Buxbaum, 2013, Buxbaum and Kalenine, 2010, Rizzolatti and Matelli, 2003). The ventro-dorsal stream is thought to store long-term action knowledge critical for object use and pantomime of object use, while the dorso-dorsal stream is used for immediate online control of motor acts (Binkofski & Buxbaum, 2013). However, studies on cerebral action representation are not entirely conclusive across patient groups and controls.
Functional MRI (fMRI) studies in healthy subjects support the general functional distinction in ventro-dorsal stream for meaningful gestures on verbal command and dorso-dorsal stream for imitation, albeit the distinction is not strict. Particularly, fMRI studies demonstrated a bilateral but left lateralized fronto-temporo-parietal network engaged in planning of meaningful gestures on command (Bohlhalter et al., 2009, Fridman et al., 2006, Johnson-Frey et al., 2005, Kroliczak and Frey, 2009, Vry et al., 2015). Performance of both intransitive and transitive gestures on verbal command has elicited brain activation in overlapping brain areas with some studies reporting less lateralization in transitive gestures (Bohlhalter et al., 2009, Fridman et al., 2006). Furthermore, the contrast transitive versus intransitive gestures demonstrated activation within the left inferior part of the inferior frontal gyrus (IFG) (Fridman et al., 2006), the left PMd and inferior parietal cortex (Kroliczak & Frey, 2009). Results of a combined fMRI and fiber tracking study suggest that performance of transitive gestures on command engages the ventro-dorsal route and additionally the ventral route via IFG (Vry et al., 2015). In healthy controls the imitation of hand gestures is associated with neural activity in bilateral IFG, PMd, IPL and SPL (Horan et al., 2014, Menz et al., 2009, Muhlau et al., 2005, Vry et al., 2015). Even though these fMRI studies have been informative on neural action representation under normal conditions, they do not allow inferences on the nature of the disturbances seen in abnormal gesturing, such as apraxia.
Lesion mapping studies of predominantly left hemisphere stroke patients revealed that poor imitation performance was associated with lesions in parietal and posterior temporal cortices (Buxbaum et al., 2014, Hoeren et al., 2014, Mengotti et al., 2013), less often with lesions in the IFG or insula (Weiss et al., 2016), which have been suggested to incorporate specificity of body parts (Goldenberg & Karnath, 2006). Most studies tested imitation of meaningless gestures, but some also investigated imitation of tool related (transitive) gestures. Buxbaum and colleagues proposed that the kinematics of imitative gestures relied on IPL and SPL, the tool related knowledge in transitive gestures instead relied on posterior temporal cortex integrity (Buxbaum et al., 2014).
Lesion mapping studies also focused on transitive gestures on verbal command. Impaired performance of such tool-related gestures was linked to lesions in left IFG, insula, premotor cortex, hippocampus, IPL and lateral occipitotemporal cortex (Goldenberg et al., 2007, Hoeren et al., 2014, Manuel et al., 2013, Weiss et al., 2014). However, some reports suggested specific contributions, e.g., content errors and IFG lesions, spatial errors and IPL lesions (Manuel et al., 2013) or posture in tool use and lesions in MTG and inferior temporal gyrus (ITG) (Buxbaum et al., 2014). Lesion mapping studies have not attempted to investigate performance of meaningless or intransitive gestures on verbal command.
Brain lesions due to ischemic stroke cover a wide range of affected brain tissue, including gray and white matter. Lesion mapping studies are therefore limited in their specificity. Even though the gesture deficit is clear, misattributions of the causes are possible, as the brain lesions include more areas than those critical for correct gesturing. Furthermore, in contrast to most fMRI investigations in healthy subjects, lesion studies suggest that gesture performance was exclusively linked to left hemispheric networks.
While fMRI studies in healthy subjects have informed on particular brain regions they failed to mimic defective gesturing. In contrast, lesion mapping studies provide precise information on the gesture deficit but lesion mapping is less specific and contaminated by the anatomical boundaries of ischemic stroke. The neural correlates of defective gesturing may be investigated in a model disorder combining subtle structural brain and gestural deficits.
Schizophrenia is characterized by poor social interaction, which contributes to the devastating functional outcome (Schmidt, Mueller, & Roder, 2011). Particularly, nonverbal communication is disturbed, both during perception and expression of socially relevant information (Green et al., 2012, Lavelle et al., 2013, Pinkham, 2014). Gesture is particularly interesting to understand social cognitive deficits in schizophrenia (Walther & Mittal, 2016). Patients are impaired in action imitation, particularly imitation of finger and hand gestures (Matthews et al., 2013, Park et al., 2008). These deficits have been linked to aberrant function of the mirror neuron system (Thakkar, Peterman, & Park, 2014). The accuracy of hand gestures is severely impaired in schizophrenia, particularly when performed on verbal command, but less impaired during imitation (Walther et al., 2015, Walther et al., 2013a, Walther et al., 2013b). Indeed, 40–60% of patients are impaired in gesture performance on verbal command, while 23–33% present defective imitation of hand gestures (Walther et al., 2013a, Walther et al., 2013b). The most frequent errors occur when performing meaningless gestures on verbal command (Walther et al., 2013a). Poor performance was linked to frontal lobe dysfunction, impaired working memory and motor abnormalities (Walther et al., 2013b, Walther et al., 2015).
Gray matter (GM) alterations have been demonstrated in schizophrenia patients in meta-analyses also in praxis relevant brain areas, including the bilateral IFG and insula, superior temporal gyrus (STG) and parietal lobe (Bora et al., 2011, Haijma et al., 2013). Furthermore, aberrant white matter (WM) ultrastructure was reported in long association fibers such as the superior longitudinal fasciculus and uncinate fasciculus as well as in interhemispheric and projection fibers of the frontal lobe (Bora et al., 2011, Peters et al., 2010, Walther et al., 2011a).
Schizophrenia may present both, a behavioral gesture deficit as well as brain alterations in gray and white matter within the praxis relevant network. Thus, the disorder may serve as a neuropsychiatric model of defective pantomime without macroanatomic brain lesions. As imitation of gestures is less affected in schizophrenia, the model will be confined to deficits in pantomime. Patients with apraxia usually suffer from impairments in tool use, gesturing, fine and gross motor function due to structural brain lesions. Hand gesture performance is impaired during both imitation and pantomime; errors include spatial and temporal errors as well as content errors (e.g., body part as object) (Vanbellingen et al., 2010). In apraxia impairments in action planning are multimodal as indicated by altered visual scanning and perception of action-related sounds (Pazzaglia et al., 2008, Vanbellingen et al., 2015). Schizophrenia patients share the same type of gesture errors, but the extent of the impairment is less pronounced than in apraxia (Vanbellingen et al., 2010, Walther et al., 2013a). In addition, schizophrenia is associated with subtle fine and gross motor impairments, frontal lobe dysfunction and impaired social cognition (Walther et al., 2013a, Walther et al., 2015).
To investigate the structural brain correlates of defective gesturing in schizophrenia, we focused on group differences in GM volume according to gesture performance, i.e., the difference between patients with gesture deficits versus patients without gesture deficits versus healthy controls. We expected reduced GM volume within the ventro-dorsal stream (particularly in the left IFG) in schizophrenia patients with apparent impairments of gesture performance on verbal command compared to patients with intact gesture performance and healthy subjects. Likewise, we hypothesized reduced GM volume within the parietal cortex in schizophrenia patients with defective gesture imitation. Finally, we explored the association of impaired gesture performance on verbal command and GM volume in patients for each category of meaningful gestures, i.e., intransitive (conventional meaning) and transitive (tool use). We hypothesized that impaired performance of intransitive gestures would be related to GM volume reduction in brain areas processing language/semantic content such as MTG and STG. Furthermore, impaired performance of transitive gestures on verbal command would be related to reduced GM volume in IFG and SPL.
Section snippets
Participants
In total, 45 patients with schizophrenia spectrum disorders according to DSM-5 criteria (schizophrenia n = 34, schizoaffective disorder n = 2, schizophreniform disorder n = 9) were recruited at the inpatient and outpatient departments of the University Hospital of Psychiatry, Bern. In addition, 44 healthy control subjects were recruited via advertisement and among staff and students. Controls were matched for age, gender, and duration of education. All participants were right-handed according
Behavioral and clinical data
Demographic and clinical data are given in Table 1. Schizophrenia patients performed poorer than controls in each TULIA domain and each TULIA gesture category. A repeated measures ANOVA of TULIA scores indicated significant effect of domain (F1, 89 = 22.0, p < .001) with superior imitation performance, category (F1.68, 89 = 50.4, p < .001), and group (F1, 89 = 22.5, p < .001), as well as interactions of domain × group (F1, 89 = 9.0, p = .003) and domain × category × group (F1.70, 89 = 5.0, p
Discussion
This study investigated the neural correlates of impaired performance of hand and finger gestures in schizophrenia. In fact, schizophrenia served as a model of apraxia with discrete cerebral abnormalities and distinct gesture impairments. This approach adds to fMRI studies in healthy controls that lack behavioral impairments. Furthermore, the study extends results of lesion studies that are limited to macroscopic brain damage. We investigated schizophrenia patients with deficits in gesture
Role of the funding source
This study was supported by grants from the Bangerter-Rhyner Foundation and the Swiss National Science Foundation (SNF, grant # 152619/1). The founding sources had no role in the study at any phase.
Conflict of interest
The authors have no conflict of interest with this work.
Acknowledgment
The authors would like to thank Dr. Corrado Bernasconi for statistical advice.
References (70)
- et al.
Voxel-based morphometry–the methods
NeuroImage
(2000) - et al.
Unified segmentation
NeuroImage
(2005) - et al.
Functional and structural brain correlates of theory of mind and empathy deficits in schizophrenia
Schizophrenia Research
(2009) - et al.
Two action systems in the human brain
Brain and Language
(2013) - et al.
Neuroanatomical abnormalities in schizophrenia: a multimodal voxelwise meta-analysis and meta-regression analysis
Schizophrenia Research
(2011) - et al.
Altered cortico-basal ganglia motor pathways reflect reduced volitional motor activity in schizophrenia
Schizophrenia Research
(2013) - et al.
Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T
NeuroImage
(2004) - et al.
Can we reconcile the declarative memory and spatial navigation views on hippocampal function?
Neuron
(2014) - et al.
The role of the dorsal stream for gesture production
NeuroImage
(2006) Apraxia and the parietal lobes
Neuropsychologia
(2009)
Shared neural substrates of apraxia and aphasia
Neuropsychologia
Self-reported empathy and neural activity during action imitation and observation in schizophrenia
Neuroimage Clinical
Mismatch and lexical retrieval gestures are associated with visual information processing, verbal production, and symptomatology in youth at high risk for psychosis
Schizophrenia Research
Left inferior parietal dominance in gesture imitation: an fMRI study
Neuropsychologia
The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
The sound of actions in apraxia
Current Biology
Diffusion tensor imaging in the early phase of schizophrenia: what have we learned?
Journal of Psychiatry Research
Search of multimodal neuroimaging biomarkers of cognitive deficits in schizophrenia
Biological Psychiatry
Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain
NeuroImage
Different visual exploration of tool-related gestures in left hemisphere brain damaged patients is associated with poor gestural imitation
Neuropsychologia
The ventral fiber pathway for pantomime of object use
NeuroImage
Psychomotor symptoms of schizophrenia map on the cerebral motor circuit
Psychiatry Research
Alterations of white matter integrity related to motor activity in schizophrenia
Neurobiology of Disease
Resting state cerebral blood flow and objective motor activity reveal basal ganglia dysfunction in schizophrenia
Psychiatry Research
Impaired gesture performance in schizophrenia: particular vulnerability of meaningless pantomimes
Neuropsychologia
Impaired pantomime in schizophrenia: association with frontal lobe function
Cortex
Definition and characterization of an extended social-affective default network
Brain Structure & Function
The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology
Archives of General Psychiatry
Cognitive approach to the assessment of limb apraxia
Clinical Neuropsychologist
Beat and metaphoric gestures are differentially associated with regional cerebellar and cortical volumes
Human Brain Mapping
Gesture subtype-dependent left lateralization of praxis planning: an event-related fMRI study
Cerebral Cortex
Action knowledge, visuomotor activation, and embodiment in the two action systems
Annals of the New York Academy of Sciences
Critical brain regions for tool-related and imitative actions: a componential analysis
Brain
A word in the hand: action, gesture and mental representation in humans and non-human primates
Philosophical Transactions of the Royal Society of London Series B Biological Sciences
Unified Parkinson's disease rating scale
Cited by (35)
Using dynamic point light display stimuli to assess gesture deficits in schizophrenia
2022, Schizophrenia Research: CognitionMotor cognition in schizophrenia: Control of automatic imitation and mapping of action context are reduced
2022, Schizophrenia ResearchCitation Excerpt :Functional imaging studies in healthy individuals located this control in the medial prefrontal cortex (mPFC) and right temporoparietal junction (rTPJ) and not in the MNS itself (Brass et al., 2005; Liepelt et al., 2016; Santiesteban et al., 2012). A possible explanation that some studies have found reduced imitation in schizophrenia could be that the majority of previous studies investigated voluntary imitation, i.e., participants were asked to replicate observed actions (Braun et al., 1991; Gaebel, 1992; Matthews et al., 2013; Park et al., 2008; Putnam and Kring, 2007; Schaefer et al., 2013; Schwartz, 2006; Stegmayer et al., 2016; Trémeau et al., 2005; Walther et al., 2013; Walther, 2015) or to imitate emotional stimuli like facial expressions (Gilbert and Burgess, 2008; Haker and Rösler, 2009; Schaefer et al., 2013; Thakkar et al., 2014). These experimental arrangements might not have sufficiently considered motor, cognitive, and emotional deficits associated with schizophrenia itself, which might have confounded experimental results obtained in voluntary imitation studies.
Hand gesture performance is impaired in major depressive disorder: A matter of working memory performance?
2021, Journal of Affective DisordersGesture deficits and apraxia in schizophrenia
2020, CortexCitation Excerpt :Structural brain abnormalities in subjects with gesture impairments are localized within the praxis network (see Fig. 2). Grey matter volume is reduced in patients with gesture deficits compared to healthy subjects predominantly in the left inferior frontal gyrus (IFG), left superior parietal lobe, left middle temporal cortex, but also in the right insula, right temporal and parietal cortex (Stegmayer, Bohlhalter, et al., 2016). Interestingly, patients with gesture deficits had lower grey matter volumes than patients without gesture deficits in the right insula, right inferior parietal lobe (IPL), and the right superior temporal gyrus.