Table 2. Figure 2. Pathways of the best and worst social role functioning in patients with schizophrenia, showing that social cognition mediates between neurocognition and functional outcomes. Reproduced from Bae et al. An assessment of the associations between mental state attribution i. This effect was not mediated by neurocognition i.
Mental state attribution was the only significant cognitive predictor of social skills, although levels of disorganized and negative symptoms were found to predict large proportions of variance in social functioning [ 71 ]. An investigation that used voxel-based morphometry and a battery of behavioral assessments of ToM processing indicated that ToM deficits in patients with schizophrenia may be related to a reduction in ventromedial prefrontal cortex gray matter volume [ 72 ].
However, it is currently not known whether loss of ventromedial prefrontal cortex gray matter could cause poor ToM skills, or whether the social isolation experienced by those with schizophrenia, and the consequent loss of opportunities to employ ToM skills, could cause loss of ventromedial prefrontal cortex gray matter over time [ 72 ].
This potentially has important therapeutic implications, since interventions aimed at improving ToM skills might, in theory, mitigate gray matter loss, and restore ventromedial prefrontal cortex function [ 72 ]. Individuals at ultra-high risk of schizophrenia have also been shown to have significant impairments in ToM abilities, compared with healthy controls [ 73 ].
Furthermore, ToM ability—but not emotion recognition, social perception, or attributional style—has been shown to be significantly correlated with current role and global functioning assessed using the Global Functioning Social and Role scales, and the Social and Occupational Functioning Assessment Scale in individuals at ultra-high risk of psychosis [ 74 ].
Evidence has also indicated that ToM deficits confined to comprehension of higher-order false belief emerge in subjects with at-risk mental state [ 75 ]. ToM was assessed using the Reading the Mind in the Eyes Test-Revised Version which measures the decoding component of ToM , and the authors speculate whether tools that assess the reasoning rather than the decoding aspect of ToM might better elucidate the role of ToM as a marker of vulnerability for later developing schizophrenia [ 77 ].
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Although results from such studies are somewhat mixed, taken together they may indicate a role for specific preventative strategies targeting ToM at the prodromal stage. ToM deficits also appear to affect patients' parenting ability. In a study investigating the association between functional ability in the parental role i.
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The results demonstrated that deficits in first- and second-order ToM were significantly associated with parental role dysfunction, as were cognitive flexibility, speed of processing, and motivation [ 78 ]. Second-order ToM was found to be a specific predictor of parental role on logistic regression analysis [ 78 ]. In a study investigating the relationships between insight and ToM, an association was found between awareness of illness and ToM specifically, the ability to understand the intentions of others on the Hinting Task , which was independent of other illness-related variables neurocognition and clinical symptoms [ 80 ].
Moreover, ToM was shown to be a mediator linking neurocognition with awareness of illness. In contrast, no association was observed between ToM and cognitive insight [ 80 ]. These findings indicate that social cognition interventions that target ToM skills, such as perspective-taking, could potentially improve awareness of illness and functional outcome in schizophrenia [ 80 ].
IPSAQ measures a causal locus external-personal vs. Some studies have specifically investigated the role of attributional bias in persecutory delusions in schizophrenia. A comparison of attributional bias assessed using the IPSAQ in patients with early psychosis and gender- and age-matched controls found that although a high proportion of the patients had persecutory delusions, they did not differ from the controls in terms of personalizing or externalizing bias [ 81 ].
In a cross-sectional study in which attributional bias was assessed using a revised version of the IPSAQ IPAQ-R in patients with persistent positive symptoms of schizophrenia and healthy controls, there were no differences between the healthy controls and either the overall group of patients with schizophrenia or the subgroup of patients with persecutory delusions, in terms of personalizing or externalizing biases [ 82 ]. Patients with schizophrenia and the subgroup with persecutory delusions both displayed a self-blaming attributional style, tending to attribute negative events to themselves [ 82 ].
In a study comparing attributional style assessed using the AIHQ , FAR assessed using the FEIT, Facial Emotion Discrimination Test, and ER and ToM assessed using the Hinting Task in outpatients with schizophrenia, outpatients with bipolar disorder, and a group of healthy controls, the clinical groups demonstrated hostile social cognitive biases, in comparison with the control group [ 64 ]. Patients with schizophrenia also showed poorer ToM ability than the patients with bipolar disorder and healthy controls [ 64 ]. Moreover, in patients with schizophrenia, a tendency to aggressiveness and PANSS score were the factors most strongly associated with global functioning [ 64 ].
Similarly, in a study into the factor structure of social cognition in schizophrenia, and the correlation between these factors and symptoms, neurocognition, and functional outcome, hostile attributional style was found to be significantly associated with PANSS positive and emotional discomfort factors, as well as PANSS total score [ 83 ]. Hostile attributional style also approached significance in predicting quality of life assessed using the Quality of Life Scale [ 83 ].
Taken together, these findings indicate that hostile attributional style is an important driver of functional outcomes in schizophrenia and therefore a potential candidate for targeted intervention. It includes the ability to integrate contextual information and social knowledge into judgment about other people's behaviors e. Measures of social perception include Relationships Across Domains [ 42 ] Table 1. Social perception has been shown to be related to social behavior, social problem solving, and community functioning, and to mediate the relationship between neurocognition and functional outcome [ 9 , 17 , 84 ].
Poor social perception has also been associated with an inability to form trustingschizophrenia outpatients compared MSCT relationships and improve quality of life [ 16 , 85 ]. Social perception may therefore be a rational target for interventions aiming to enhance functional improvements [ 17 ]. In individuals with schizophrenia, social perception, and emotion responsivity were found to be positively correlated with functional outcome [ 86 ]. Emotion responsivity for positive and negative stimuli were shown to be slightly reduced in patients with schizophrenia, compared with controls, but the relationship between emotional responsivity, and functional outcome did not appear to be mediated by social perception [ 86 ].
These findings indicate that it may be important to take account of how a patient responds emotionally to supposed positive or rewarding events, in addition to their social cognitive abilities, when considering interventions aiming to improve functional outcomes [ 86 ]. Social cognition training programs aim to correct the specific social cognitive impairments associated with schizophrenia that are related to social functioning and readily transferable to real-world situations [ 16 ]. Such programs have additionally been found to indirectly result in improvements in clinical positive and negative symptoms, vocational prospects, and quality of life [ 16 ].
Broad-based interventions designed to improve functioning such as Integrated Psychological Therapy [ 87 ], Integrated Neurocognitive Therapy [ 88 ], and Cognitive Enhancement Therapy [ 89 ] have shown limited success in schizophrenia, but have helped inform the development of more targeted interventions [ 16 ], as outlined in the next section. In general, cognitive remediation programs are most effective in enhancing functional outcomes when integrated with psychosocial rehabilitation programs, by allowing individuals to practice cognitive skills in real-world settings [ 90 ].
SCIT is a week, manualized, group intervention targeting emotion perception, ToM, and attributional bias [ 91 ]. It comprises three phases: emotion training, figuring out situations, and integration [ 91 ]. Pilot studies conducted in the inpatient setting reported improvements in ToM, attributions for ambiguous situations, and emotional and social perception following SCIT, as well as improvements in aggressive behaviors and self-reported social relationships [ 92 , 93 ].
Effects on social functioning were sustained over 6 months in a follow-up study [ 94 ]. A modified version of SCIT comprising twice-weekly sessions for 8 weeks was compared with treatment as usual in an inpatient forensic ward in a randomized, single-blind, feasibility study [ 95 ]. In the outpatient setting, preliminary data from a quasi-experimental study comparing SCIT plus treatment as usual vs. A subsequent randomized controlled trial did not show significant improvement in emotional perception, but improvements in hostile attributional bias and social functioning were reported [ 97 ].
In the community setting, an initial study demonstrated the transportability, acceptability, and feasibility of SCIT, and there were indications of improvements in ToM and emotion perception but not attributional bias following SCIT [ 98 ]. Feasibility studies conducted in China and Finland have demonstrated that translated versions of SCIT are acceptable and effective in improving social cognition and social functioning [ 99 , ].
A week pilot study investigated the impact of once-weekly family-assisted SCIT, compared with social stimulation once every 3 weeks, on quality of life, social functioning, and social cognition in clinically stable schizophrenia outpatients [ ]. When pre-randomization assessments were compared with assessments after 16 weeks, patients who had received family-assisted SCIT demonstrated significant improvements in quality of life, social cognition, and social functioning; by contrast, results for nearly all outcome parameters declined in those who received social stimulation [ ].
A preliminary efficacy study conducted in clinically stable schizophrenia outpatients compared MSCT administered as 18 sessions over 10 weeks with treatment as usual [ ]. MSCT resulted in significant improvements in ToM, social perception, emotion recognition, and social functioning [ ].
In addition, MSCT significantly reduced the tendency to jump to conclusions [ ]. PECS was shown to improve some areas of ToM measured using the Hinting Task , as well as the emotion recognition of sadness, anger, fear, and disgust, in outpatients with schizophrenia [ , ].
These patients were also shown to pay more attention to areas of the face that display emotion; however, this did not correlate with improvements in FAR performance [ ]. CRT, and these improvements were reflected by a trend toward improvement in global social functioning [ ]. By contrast, CRT only improved targeted neurocognitive areas, such as executive function, working memory, and attention [ ]. RECOS is an individual neurocognitive remediation therapy targeting one to three out of six neurocognitive functions verbal memory, working memory, executive functions, memory, and visuo—spatial attention, selective attention, and processing speed , according to each patient's cognitive and clinical profile [ ].
RECOS also consists of three 1-h sessions per week and was administered for 10 weeks [ ]. ETIT is an imitation treatment that was designed to improve social cognition and social functioning in patients with schizophrenia [ ]. It comprises four phases: observing the gaze of people in photographs, imitating facial expressions, inferring an individual's mental state in a social situation, and attributing intentions by watching people's actions in a series of comic strips [ ]. Preliminary data from a study conducted in outpatients with schizophrenia demonstrated that those who underwent ETIT improved on social cognitive measures, including emotion recognition and ToM, and showed better social functioning than those who underwent Problem Solving Training the control group [ ].
The effects of rehabilitation training on neuro-physiological activation were assessed using the event-related potentials method, and an increase in electroactivity in the medio-frontal areas was only observed following ETIT, supporting the observed benefits on social cognition [ ].
A pilot study evaluated the practicality and effectiveness of a week emotion processing and ToM video-based training program, compared with standard social cognitive rehabilitation treatment, in outpatients with schizophrenia [ ]. Significant improvement in ToM abilities was demonstrated following video-based training, but there were no changes in emotion processing [ ]. MRIGE is an interactive computerized program comprising video clips, audio clips, and brief stories that was originally developed to improve emotion and facial recognition in patients with autism spectrum disorders [ ].
ToMI employs comic strips and faux pas stories to train cognitive and affective ToM [ ]. A study conducted in outpatients with schizophrenia demonstrated improvement in ToM post-ToMI, compared with an active control group [ ]. An integrated multisensory approach, aiming to enhance emotion detection using either video or audio channels, was assessed in outpatients with schizophrenia and compared with an active control group [ ].
Video training comprised short videos depicting human social interactions, selected from TASIT, with the audio and subtitles turned off. Audio training used only the audio component of the same videos. In the active control group, patients were involved in a newspaper discussion group. All three interventions were conducted in a 1-hourly session per week over 8 weeks [ ]. Emotion recognition was assessed using FEIT to evaluate visual recognition of emotion expression and the Montreal Affective Voices test to evaluate emotion expressed via audio [ ].
Significant improvements in both aspects of emotion processing were observed following training, and positive correlations were found between working memory assessed using the Italian version of the Brief Assessment of Cognition in Schizophrenia , social functioning assessed using PSP , and emotion processing [ ]. SoCog-MSRT and SoCog-ERT were assessed in a pilot study conducted in patients with schizophrenia or schizoaffective disorder; both were administered as 12 bi-weekly sessions over 6 weeks [ ].
OXT is a neuropeptide that interacts with a variety of neuromodulators, including serotonin and dopamine, in the nucleus accumbens, and amygdala, respectively [ ]. In healthy controls, OXT has demonstrated beneficial effects on a range of social cognition domains and measures of social functioning [ ]. In a cross-sectional study conducted in patients with schizophrenia and healthy controls, there were significant correlations between OXT plasma levels and social cognitive bias in the control group and in patients with delusions, but these were not observed in patients without delusions [ ].
A significant correlation between social cognitive capacity and OXT plasma levels was only found in patients with delusions [ ]. There is also some evidence to suggest that genetic variants of the OXT receptor may play a role in the social cognitive impairments observed in schizophrenia [ , ]. The therapeutic use of intranasal OXT to improve social cognition and social functioning in schizophrenia has yielded mixed results [ , ].
In a 6-week, placebo-controlled, double-blind pilot study, patients who received intranasal OXT experienced within-group improvements in perspective taking and the ability to recognize fear, and also an improvement in negative symptoms [ ]. A small, randomized, placebo-controlled trial demonstrated that twice-daily intranasal OXT treatment for 14 days improved ToM and social perception in patients with schizophrenia [ ]. In a small, randomized, within-subjects, placebo-controlled study designed to investigate whether a single dose of OXT could improve higher-order and lower-order social cognition, patients with schizophrenia received a single dose of oxytocin nasal spray 24 IU and a placebo, administered 2 weeks apart [ ].
OXT was shown to enhance performance on higher-order social cognition tasks which assess social cognitive processing within the context of social communication , but had no effect on general neurocognition [ ]. Improvement was greatest on tests that measured the appreciation of indirect hints and recognition of social faux pas [ ]. In a week, randomized, controlled trial, outpatients with schizophrenia or schizoaffective disorder received twice-daily intranasal OXT 24 IU or placebo [ ].
No evidence of beneficial effects on social cognition was observed for OXT compared with placebo [ ]. OXT was slightly more beneficial than placebo on a component of social functioning, but there was also evidence that placebo was more beneficial than OXT on the role-play task [ ]. In the schizophrenia subgroup, OXT resulted in a significant within-group reduction in PANSS negative symptoms and a significant between-group improvement in negative symptoms [ ].
A randomized, double-blind, placebo-controlled trial investigated the efficacy of an extended treatment of OXT nasal spray combined with social cognition training to improve social cognition, clinical symptoms, and social functioning in young people with early psychosis [ ]. No benefit of OXT nasal spray treatment vs. In another randomized, double-blind, placebo-controlled trial, intranasal OXT did not modify jumping to conclusions in stable, medicated patients with schizophrenia [ ].
The mixed findings observed in studies investigating the therapeutic potential of OXT in schizophrenia may be due to the impact of factors including task-specific effects, patient effects e. Several studies have specifically explored the effects of antipsychotic treatment on social cognition and social functioning. An 8-week, randomized, multicenter, open-label study examined the effects of aripiprazole, and risperidone on social cognition and neurocognition in patients with schizophrenia [ ].
Both treatments resulted in improvements in social cognitive and neurocognitive test scores, and reaction time [ ]. The agents differed little on social cognitive test scores [ ]. However, aripiprazole was significantly superior compared with risperidone on symbol substitution and reaction times for emotional working memory and working memory, and these improvements were shown to correlate with social functioning [ ].
A 6-month, open-label, randomized, controlled pilot study compared the effects of risperidone long-acting injection and paliperidone palmitate on non-acute-phase social functioning in patients with schizophrenia [ ]. Paliperidone palmitate was significantly more effective than risperidone long-acting injection on change from baseline in SFS total score, and the SFS competence and performance subscales scores [ ].
Patients participating in a 6-month, randomized, double-blind clinical trial comparing olanzapine, and quetiapine were assessed for improvements in social cognition and social functioning [ ]. Social cognition was assessed using signal detection analysis of performance on the Social Cue Recognition Test [ ]. In both treatment groups, there were modest, but significant, improvements on three out of four social cognition subscales [ ]. Evidence regarding the relative impacts of antipsychotic treatments on social cognition in schizophrenia is currently inconclusive, due to inconsistencies in study designs, methodologies, and medication dosages [ ].
Despite the lack of definitive evidence, it is rational to consider the wider impact of antipsychotics on cognition when selecting treatment [ , ]. Raloxifene is a first-generation selective estrogen receptor modulator that acts as an estrogen receptor agonist in the brain and bone , and as an antagonist in other tissues [ ]. Adjunctive raloxifene was found to significantly increase activation in the right hippocampus and left inferior frontal gyrus, compared with placebo, indicating that it may reverse abnormal neural activity during FAR, and suggesting a potential modifying role for estrogen in schizophrenia [ ].
Research in social cognition is gaining significant importance in schizophrenia. However, the complexity of the subject remains challenging. The past few decades have seen concerted multidisciplinary efforts from different fields, including neuroscience, psychiatry, psychology, computer sciences, anthropology, and philosophy, which have markedly changed the ways in which we conceptualize how knowledge is acquired, processed, and used. This area is also highly relevant to clinical practice, since impairments in social cognition are consistently found in patients with schizophrenia.
There is increasing evidence that social cognition is a direct predictor of functional outcomes, particularly community functioning. Similarly, the concepts of neurocognition and social cognition are interlinked, with social cognition mediating the relationship between basic neurocognition and functional outcome, thereby making it central to daily life functioning. Several psychosocial interventions have shown promise in overcoming and correcting impairments in social cognition associated with schizophrenia.
Indeed, current evidence indicates that most of the targeted social cognitive training programs that have been developed to date may produce improvements in the domains of social cognition for which they are designed. Further research is required to advance our understanding of the role of social cognition in schizophrenia, and to further establish the utility of targeted interventions in this setting. AJ and AC made substantial contributions to the conception of this article, and the analysis and interpretation of data it contains; were involved in drafting the article or revising it critically for important intellectual content; provided final approval of the version to be published; and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work were appropriately investigated and resolved.
Editorial support for the preparation of this publication was funded by an educational grant from Sunovion Pharmaceuticals. AJ has received speaker fees from, and undertaken consultancy work and the organization of scientific meetings for, Sunovion and Lundbeck, over the past 3 years. AC declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Editorial support for the preparation of this manuscript was provided by John Scopes of m X m Medical Communications. Leucht S, Lasser R. The concepts of remission and recovery in schizophrenia. Pharmacopsychiatry 39 — Psychosocial treatments to promote functional recovery in schizophrenia.
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