Functional MRI of Verbal Self-monitoring in Schizophrenia: Performance and Illness-Specific Effects
TL;DR: It is concluded that hypoactivation of a neural network comprised of the thalamus and frontotemporal regions underlies impaired speech monitoring in schizophrenia.
Abstract: Previous small-sample studies have shown altered frontotemporal activity in schizophrenia patients with auditory hallucinations and impaired monitoring of self-generated speech. We examined a large cohort of patients with schizophrenia (n = 63) and a representative group of healthy controls (n = 20) to disentangle performance, illness, and symptom-related effects in functional magnetic resonance imaging-detected brain abnormalities during monitoring of self- and externally generated speech in schizophrenia. Our results revealed activation of the thalamus (medial geniculate nucleus, MGN) and frontotemporal regions with accurate monitoring across all participants. Less activation of the thalamus (MGN, pulvinar) and superior-middle temporal and inferior frontal gyri occurred in poorly performing patients (1 standard deviation below controls' mean; n = 36), relative to the combined group of controls and well-performing patients. In patients, (1) greater deactivation of the ventral striatum and hypothalamus to own voice, combined with nonsignificant activation of the same regions to others' voice, associated positively with negative symptoms (blunted affect, emotional withdrawal, poor rapport, passive social avoidance) regardless of performance and (2) exaggerated activation of the right superior-middle temporal gyrus during undistorted, relative to distorted, feedback associated with both positive symptoms (hallucinations, persecution) and poor performance. A further thalamic abnormality characterized schizophrenia patients regardless of performance and symptoms. We conclude that hypoactivation of a neural network comprised of the thalamus and frontotemporal regions underlies impaired speech monitoring in schizophrenia. Positive symptoms and poor monitoring share a common activation abnormality in the right superior temporal gyrus during processing of degraded speech. Altered striatal and hypothalamic modulation to own and others' voice characterizes emotionally withdrawn and socially avoidant patients.
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TL;DR: It is found that mentally healthy people should use certain brain regions, especially the superior and medial temporal gyri, and the way people with schizophrenia use their brains should differ from mentally healthy brain activation patterns shown in functional neuroimaging.
Abstract: Previous research has explained the production and perception of speech and anomalies found in the brains and cognitive abilities of people with schizophrenia when compared with mentally healthy controls. One aspect of research that has been lacking is an explanation of auditory verbal hallucinations and referential delusions of communication that combines social cognition theory with neuroimaging evidence, with particular emphasis on detecting an intention to communicate. Developing this knowledge could reduce the difficulties faced in early detection of schizophrenia. This study aimed to find clear evidence that mentally healthy people describe sounds in certain qualitative ways and whether a diagnosis of schizophrenia influences this. Second, it aimed to identify brain regions in mentally healthy adults that are involved in the detection of auditory intention to communicate and to hypothesize regarding what could differ in schizophrenia. We conducted a selective review of literature pertaining to the development of theory of mind and its relationship to schizophrenia, with a focus on the “intention to communicate.” We found that mentally healthy people should use certain brain regions, especially the superior and medial temporal gyri, and the way people with schizophrenia use their brains should differ from mentally healthy brain activation patterns shown in functional neuroimaging. Now these links and differences can be examined in more detail, using novel, schizophrenia-relevant tests.
1 citations
Cites background from "Functional MRI of Verbal Self-monit..."
...Further, participants with schizophrenia showed reduced right superior temporal gyrus (STG) activity and also reduced activation in the striatum and hypothalamus when discriminating between degraded voices that were either one’s own or another’s (Kumari et al., 2010)....
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...…this suggests that fronto-temporal regions of the brain are normally responsible for distinguishing another’s voice from one’s own, that the right STG is important in processing ambiguous vocal stimuli (Fu et al., 2006; Kumari et al., 2010), and that such regions may be disrupted in schizophrenia....
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...Taken together, this suggests that fronto-temporal regions of the brain are normally responsible for distinguishing another’s voice from one’s own, that the right STG is important in processing ambiguous vocal stimuli (Fu et al., 2006; Kumari et al., 2010), and that such regions may be disrupted in schizophrenia....
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TL;DR: This article found that verbal hallucination proneness was associated with higher rates of false recognition of high-frequency words and with activation of language and decisional brain areas during false recognitions of low-, but not high-, frequency words.
Abstract: Abstract Verbal hallucinations in schizophrenia patients might be seen as internal verbal productions mistaken for perceptions as a result of over-salient inner speech and/or defective self-monitoring processes. Similar cognitive mechanisms might underpin verbal hallucination proneness in the general population. We investigated, in a non-clinical sample, the cerebral activity associated with verbal hallucinatory predisposition during false recognition of familiar words —assumed to stem from poor monitoring of inner speech—vs. uncommon words. Thirty-seven healthy participants underwent a verbal recognition task. High- and low-frequency words were presented outside the scanner. In the scanner, the participants were then required to recognize the target words among equivalent distractors. Results showed that verbal hallucination proneness was associated with higher rates of false recognition of high-frequency words. It was further associated with activation of language and decisional brain areas during false recognitions of low-, but not high-, frequency words, and with activation of a recollective brain area during correct recognitions of low-, but not high-, frequency words. The increased tendency to report familiar words as targets, along with a lack of activation of the language, recollective, and decisional brain areas necessary for their judgement, suggests failure in the self-monitoring of inner speech in verbal hallucination-prone individuals.
1 citations
01 Jan 2013
TL;DR: A much simpler auditory ToM task to assess the specific ability to detect whether a sound conveyed an ‘intention to communicate’: Theory-of-Mind-auditory-stimuli (ToMas), to identify brain regions associated with the detection of an intention to communicate in people with schizophrenia and healthy controls when they responded to ToMas.
Abstract: Introduction: Impairments in Theory of Mind (ToM), for example, in schizophrenia, are evidenced in studies which typically use variants of story comprehension tasks (e.g., Hinting, Corcoran et al, 1995). These tasks can be complex and may depend upon IQ and executive functioning (Ducato et al, 2008). So far, it is unknown what parts of the human brain are responsible for detecting an intention to communicate from sounds, and distinguishing these from those sounds produced without such intent. We developed a much simpler auditory ToM task to assess the specific ability to detect whether a sound conveyed an ‘intention to communicate’: Theory-of-Mind-auditory-stimuli (ToMas). Our aim was to identify brain regions associated with the detection of an intention to communicate in people with schizophrenia and healthy controls when they responded to ToMas. We hypothesised firstly, that mentally healthy people would perceive and rate auditory stimuli in similar ways and distinguish sounds with an intention to communicate (ITC) from those without. Secondly, we believed that there was insufficient evidence to assume there would be any differences on this task between mentally healthy controls and participants with schizophrenia who were matched on age, gender and IQ. Thirdly, we expected that mentally healthy controls would use language-specific brain regions for ITC stimuli which were not used for non-ITC stimuli, when recorded using functional brain imaging. Lastly, we expected the differential activation seen in the healthy controls would be markedly absent in the people with schizophrenia, even though they would be matched on similar variables and their behavioural responses would be the same. Method: Participants: The behavioural study involved testing 50 mentally healthy participants (18 male) from Research Registers and the community (mean age 38.5, SD=15.1); a subset was matched on age and gender to 14 people with schizophrenia (10 male; mean age 40.0, SD=11.6). Then nine participants (6 male) from each group, matched on age and gender, were scanned whilst performing ToMas (mean age 37, SD=9.9). Procedure: Initially, healthy adults and those with schizophrenia were asked to listen to sounds played and answer qualitative questions about them. Twenty fMRIpilot participants of ToMas rated sounds on familiarity, source, emotional salience, meaningfulness, and intention to communicate (ITC), leading to a subset of 30 stimuli, where the ITC was either clearly evident, clearly absent, or ambiguous. The aim of Detecting an intention to communicate; Using ToMas to test Theory of Mind in people with schizophrenia and healthy controls Author: Mary-Claire Hanlon Date: 5 September 2013 Page 7 of 267 ToMas was to distinguish sounds with an ITC from those without. In the neuroimaging paradigm, participants were presented with a sound, then asked “Message?”, to which they responded yes/no via button-press. Apparata and stimuli: Haemodynamic responses to stimuli were collected using a Siemens Avanto 1.5Tesla MR scanner in an event-related paradigm. Group-level random effect analyses were performed separately on each contrast after each individual’s data were analysed (GLM, regressors=stimulus categories, covariates=motion parameters). Data were analysed using SPM8 and Matlab 7.1. Results: Healthy adults aged 18-65 years (N=50) showed qualitative elements such as familiarity, source, emotion, and meaning were used when deciding if a stimulus had an ITC. Our schizophrenia group (N=14) showed no behavioural difference in ToMas from the 14 healthy controls matched on age, gender and IQ: no group differences suggested that our schizophrenia participants were not hampered in identifying stimuli with an ITC from those without. Using a shorter version of ToMas (30 auditory stimuli), in functional neuroimaging (fMRI), we ascertained which parts of the brain were responsible for both perceiving the stimuli, and subtracting out the known brain regions to reveal those which managed the discernment of ITC. Data from mentally healthy participants (N=14) highlighted the impact of the superior temporal and middle temporal gyri (especially right STG and left MTG) in how mentally healthy adults chose between ITC-absent and ITC-present stimuli, and as predicted, the differential activation seen in the healthy group (of right STG & left MTG at p<.001) was remarkably absent in the schizophrenia group
Cites background or result from "Functional MRI of Verbal Self-monit..."
...Hallucinations and delusions of persecution were particularly associated with poor performance in the speech monitoring task (Kumari et al., 2010)....
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...Participants with schizophrenia have also shown reduced right superior temporal gyrus activity and also reduced activation in striatum and hypothalamus when discriminating between degraded voices which were either one’s own or another’s (Kumari et al., 2010)....
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...Kumari and colleagues (2010) examined monitoring of self-generated and externally generated speech in participants with schizophrenia....
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...Taken together, this line of research suggests that fronto-temporal regions of the brain are normally responsible for distinguishing another’s voice from one’s own and that the right superior temporal gyrus is particularly important in processing ambiguous vocal stimuli (Fu et al., 2006; Kumari et al., 2010), and that such regions may be disrupted in schizophrenia....
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TL;DR: In this article, the authors examined the deficits in internal motor predictive representation in patients with and without passivity experiences (PE), and in healthy controls using a novel paradigm which involved minimal cognitive processes.
Abstract: Numerous studies have identified deficits in the self-monitoring system that are associated with schizophrenia However, the tasks used in the few previous studies generally involved complex cognitive processes and rarely compared between patients with and without passivity experiences (PE) Here, we examined the deficits in internal motor predictive representation in patients with and without PE, and in healthy controls using a novel paradigm which involved minimal cognitive processes All participants completed a modified joint position matching (mJPM) task, in which they were required to replicate a voluntary, a passive verbally-cued, and a passive tactile-cued movement under blinded conditions The absolute difference between the target spot and replicated spot was measured and compared We hypothesised that if there was a failure in the internal motor predictive representation, patients with PEs would replicate less accurately in the voluntary condition, relative to passive conditions while the healthy controls would be more accurate, and, therefore, significant interactions between groups and conditions would be revealed Both healthy controls and patients without PEs replicated more accurately in the voluntary condition compared with the passive conditions The patients with PEs were less accurate in the voluntary condition compared with the passive tactile condition A significant interaction was observed between patients with vs without PEs × voluntary vs passive tactile conditions The findings suggested the relationship between deficits in motor self-monitoring in the prediction process and PEs, thus showing the need to highlight the link between motor performance and PEs
References
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TL;DR: An inventory of 20 items with a set of instructions and response- and computational-conventions is proposed and the results obtained from a young adult population numbering some 1100 individuals are reported.
33,268 citations
TL;DR: Review of five studies involving the PANSS provided evidence of its criterion-related validity with antecedent, genealogical, and concurrent measures, its predictive validity, its drug sensitivity, and its utility for both typological and dimensional assessment.
Abstract: The variable results of positive-negative research with schizophrenics underscore the importance of well-characterized, standardized measurement techniques. We report on the development and initial standardization of the Positive and Negative Syndrome Scale (PANSS) for typological and dimensional assessment. Based on two established psychiatric rating systems, the 30-item PANSS was conceived as an operationalized, drug-sensitive instrument that provides balanced representation of positive and negative symptoms and gauges their relationship to one another and to global psychopathology. It thus constitutes four scales measuring positive and negative syndromes, their differential, and general severity of illness. Study of 101 schizophrenics found the four scales to be normally distributed and supported their reliability and stability. Positive and negative scores were inversely correlated once their common association with general psychopathology was extracted, suggesting that they represent mutually exclusive constructs. Review of five studies involving the PANSS provided evidence of its criterion-related validity with antecedent, genealogical, and concurrent measures, its predictive validity, its drug sensitivity, and its utility for both typological and dimensional assessment.
18,358 citations
"Functional MRI of Verbal Self-monit..." refers background in this paper
...Remaining 5 patients on both atypical and typical antipsychotics. at (df = 81) = 1.59, P > .10. bt (df = 81) = 2.84, P = .01. ct (df = 80) = 2.99, P = .004 (IQ not assessed in one patient, n reduced to 62). dPANSS = Positive and Negative Syndrome Scale.24 Words ‘‘self,’’ ‘‘other,’’ and ‘‘unsure’’ were displayed on the screen and were outlined in black after each participant’s response....
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...PANSS = Positive and Negative Syndrome Scale.(24) fMRI of Verbal Self-monitoring in Schizophrenia...
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...Note: PANSS = Positive and Negative Syndrome Scale.(24)...
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TL;DR: It is suggested that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain, featuring the presence of anticorrelated networks in the absence of overt task performance.
Abstract: During performance of attention-demanding cognitive tasks, certain regions of the brain routinely increase activity, whereas others routinely decrease activity. In this study, we investigate the extent to which this task-related dichotomy is represented intrinsically in the resting human brain through examination of spontaneous fluctuations in the functional MRI blood oxygen level-dependent signal. We identify two diametrically opposed, widely distributed brain networks on the basis of both spontaneous correlations within each network and anticorrelations between networks. One network consists of regions routinely exhibiting task-related activations and the other of regions routinely exhibiting task-related deactivations. This intrinsic organization, featuring the presence of anticorrelated networks in the absence of overt task performance, provides a critical context in which to understand brain function. We suggest that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain.
7,741 citations
"Functional MRI of Verbal Self-monit..." refers background in this paper
...As noted earlier, these areas were deactivated during active conditions and the observed difference between the poor and good performers in the medial prefrontal and the posterior temporal parietal cortices arose because of a lack of deactivation of these regions in the former group, perhaps reflecting the fact that this group activated task-relevant areas to a markedly reduced degree.(54)...
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07 Feb 2014
6,430 citations
TL;DR: Analysis of regional activations across cognitive domains suggested that several brain regions, including the cerebellum, are engaged by a variety of cognitive challenges.
Abstract: Positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) have been extensively used to explore the functional neuroanatomy of cognitive functions. Here we review 275 PET and fMRI studies of attention (sustained, selective, Stroop, orientation, divided), perception (object, face, space/motion, smell), imagery (object, space/ motion), language (written/spoken word recognition, spoken/ no spoken response), working memory (verbal/numeric, object, spatial, problem solving), semantic memory retrieval (categorization, generation), episodic memory encoding (verbal, object, spatial), episodic memory retrieval (verbal, nonverbal, success, effort, mode, context), priming (perceptual, conceptual), and procedural memory (conditioning, motor, and nonmotor skill learning). To identify consistent activation patterns associated with these cognitive operations, data from 412 contrasts were summarized at the level of cortical Brodmann's areas, insula, thalamus, medial-temporal lobe (including hippocampus), basal ganglia, and cerebellum. For perception and imagery, activation patterns included primary and secondary regions in the dorsal and ventral pathways. For attention and working memory, activations were usually found in prefrontal and parietal regions. For language and semantic memory retrieval, typical regions included left prefrontal and temporal regions. For episodic memory encoding, consistently activated regions included left prefrontal and medial-temporal regions. For episodic memory retrieval, activation patterns included prefrontal, medial-temporal, and posterior midline regions. For priming, deactivations in prefrontal (conceptual) or extrastriate (perceptual) regions were consistently seen. For procedural memory, activations were found in motor as well as in non-motor brain areas. Analysis of regional activations across cognitive domains suggested that several brain regions, including the cerebellum, are engaged by a variety of cognitive challenges. These observations are discussed in relation to functional specialization as well as functional integration.
3,407 citations
"Functional MRI of Verbal Self-monit..." refers background in this paper
...This may be associated with low discrimination between self-generated vs another person’s voices in poorly performing patients given the sensitivity of right TL to auditory distinctiveness.39 Reduced left IFG activity in poor performers may suggest a language-related deficit.38 Reduced IFG activation (in either hemisphere) could also be the cause or effect of reduced verbal WM.40 This in our task would mean loss of information after hearing the feedback, prior to being able to make a response about its origin....
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...Reduced IFG activation (in either hemisphere) could also be the cause or effect of reduced verbal WM.(40) This in our task would mean loss of information after hearing the feedback, prior to being able to make a response about its origin....
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...The left IFG (Broca’s area) activation was also expected given its role in speech and language,(37,38) while the right IFG activation may relate to the earlier noted WM requirement of our task.(40)...
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