1. Introduction
Childhood adversity is highly prevalent worldwide, affecting about one third of the general population [Reference Briere and Elliott1, Reference Kessler, McLaughlin, Green, Gruber, Sampson and Zaslavsky2], and contributing to a number of negative outcomes in later life, including higher rates of criminal behaviour [Reference Wolff and Shi3], alcohol and drug use [Reference Kendler, Bulik, Silberg, Hettema, Myers and Prescott4], and lower academic achievement [Reference Lieberman and Knorr5]. Adverse childhood experiences have been identified as major risk factors for the development of many psychiatric disorders, such as schizophrenia, bipolar disorder, borderline personality disorder, major depressive disorder and posttraumatic stress disorder [Reference Read, Perry, Moskowitz and Connolly6–Reference Maercker, Michael, Fehm, Becker and Margraf9]. Specifically, childhood trauma – often defined in terms of physical and emotional neglect, and physical, emotional, and sexual abuse - has been a particular focus of research because of their deleterious and long-lasting effects [Reference Bebbington10]. The types and frequencies of these traumatic experiences can have a negative impact on mental health in adulthood [Reference Read, Fosse, Moskowitz and Perry11]. In fact, traumatic experiences in childhood are frequently reported to show increased prevalence in patients with psychiatric disorders, with rates as high as 85% in schizophrenia spectrum disorders [Reference Larsson, Andreassen, Aas, Rossberg, Mork and Steen12], 82% in personality disorders [Reference Battle, Shea, Johnson, Yen, Zlotnick and Zanarini13], 77% in affective disorders including major depressive disorder and bipolar disorder [Reference Larsson, Andreassen, Aas, Rossberg, Mork and Steen12], and 70% in patients with posttraumatic stress disorder [Reference Kessler, Aguilar-Gaxiola, Alonso, Benjet, Bromet and Cardoso14]. Emotional abuse and neglect appear to represent the most common forms of childhood maltreatment [Reference Taillieu, Brownridge, Sareen and Afifi15, Reference Young and Widom16].
In addition to childhood maltreatment, a number of other types of adverse early life experiences, such as early loss of caregivers and insecure attachment styles (i.e. dismissive-avoidant, fearful-avoidant and anxious-pre-occupied [Reference Bartholomew17]) have also been related to psychopathology in adulthood [Reference Morgan, Kirkbride, Leff, Craig, Hutchinson and McKenzie18–Reference Schreier, Wolke, Thomas, Horwood, Hollis and Gunnell20]. The link between childhood trauma and insecure attachment has been supported by a number of studies showing that a history of childhood trauma is significantly positively associated with attachment insecurities in later life [Reference Stalker and Davies21–Reference Erozkan24], indicating significant overlap between these experiences. This suggests that adverse childhood experiences may provoke the development of insecure types of attachment. According to Fonagy [Reference Fonagy and Target25], childhood trauma is the most destructive factor in the development of the attachment system.
The importance of attachment was emphasised by Bowlby [Reference Bowlby26], who argued that the relationships and bonds between parents and their offspring are critical for children’s cognitive, emotional and social development. Specifically, he claimed that insensitive, maltreating and neglectful parenting negatively influences individuals’ interpretations and expectations, and results in construction of an unworthy and inadequate internal working model of relationships [Reference Bowlby27]. This attachment structure not only integrates past experiences, but also provides the basis on which to form expectations for later relationships. Exposure to inconsistent and unreliable attachment figures, as well as the experience of childhood trauma, can negatively affect a child’s sense of safety and security, essential to the development of secure attachment and positive mental representations of self and others [Reference Cyr, Euser, Bakermans-Kranenburg and Van Ijzendoorn28]. Specifically, the first 3 years of life are a very sensitive period for the development of the attachment relationships and exposure to traumatic events during this time has irreversible effects on subsequent cognitive, social and emotional development [Reference Bowlby26, Reference Bowlby27, Reference Lieberman, Chu, Van Horn and Harris29]. Once an attachment pattern is formed in childhood, it tends to persist beyond youth [Reference Ainsworth, Rosenblatt, Hinde, Beer and Busnel30].
Of relevance to social cognitive development, Bowlby’s [Reference Bowlby31] ‘defensive exclusion’ hypothesis posits that insecurely attached individuals will filter out all information related to his/her attachment figure, as this is associated with emotional pain. Even positive attachment-related information will be prohibited from entering conscious awareness as it protects individuals from experiencing psychological pain associated with the notion that they have no or very little positive experiences with their attachment figure [Reference Vandevivere, Braet, Bosmans, Mueller and De Raedt32]. As a result of this selective or ‘biased’ information processing an individual also lacks integrated memories of negative states, which in turn may impact their Theory of Mind (ToM) development [Reference Vanwoerden, Kalpakci and Sharp33]. Without the proper use and reflection of positive and negative mental states within one’s own mind, making correct inferences about another person’s beliefs or intentions can also be impaired.
Also relevant to social cognitive development, children with the experience of abuse may also be more likely to develop an enhanced sensitivity to social cues that are reminiscent of the adults who abused them [Reference Bower and Sivers34]. Consequently, maltreated individuals may become more vigilant and distracted by threatening stimuli (‘threat-related attention bias’) [Reference Pine, Mogg, Bradley, Montgomery, Monk and McClure35], thus failing to adequately process peripheral cognitive and social information. There is also substantial evidence that maltreating parents provide less affective interactions as compared to non-abusive parents and tend to isolate themselves and their children from social interactions, providing no stable models for forming close relationships in later life [Reference Bugental, Blue and Lewis36–Reference Young and Widom39]. Specifically, those children who develop an avoidant attachment pattern would be expected to show fearfulness and avoidance in social situations, so that they are less likely to develop adequate representations of the social environment and expressions needed to accurately recognise others’ emotions.
Supporting these hypotheses, a number of studies in children have shown that exposure to adverse environments interferes with the development of social cognition [Reference Pollak, Vardi, Putzer Bechner and Curtin40–Reference Curtis and Cicchetti42], which refers to the set of mental operations underlying social interactions, and in psychiatric studies generally comprises the following domains: (1) emotion recognition and regulation, (2) ToM, (3) attributional style, and (4) social perception. Deficits in social cognitive function are a hallmark feature of major psychiatric disorders resulting in impaired social and occupational functioning [Reference Green43, Reference Henry, von Hippel, Molenberghs, Lee and Sachdev44].
Despite the relevance of early life experience to understanding development of social cognition in those who go on to experience psychiatric disorders, the association between early life experiences and social cognition in psychiatric disorders remains poorly understood. To synthesise what is currently known, we undertook a systematic review of the existing literature on the relationships between childhood experiences of adversity, attachment (both secure and insecure) and social cognition in adults with major psychiatric disorders, including schizophrenia (SZ), bipolar disorder (BD), borderline personality disorder (BPD), major depressive disorder (MDD) and posttraumatic stress disorder (PTSD).
2. Methods
2.1. Search strategy
An electronic search was conducted using PubMed and PsycINFO to identify original articles addressing the relationship between adverse early life experiences, attachment and social cognitive measures in adults with major psychiatric disorders, published up to May 2018. The following terms were used as search terms ((emotion recognition OR self-regulation OR theory of mind OR attribution OR facial expression OR face perception OR social cognition OR social perception OR face discrimination OR emotion regulation OR emotion perception OR social inference) AND (parent death OR institutional care OR foster care OR physical abuse OR verbal abuse OR sexual abuse OR emotional abuse OR domestic violence OR parent divorce OR parental mental illness OR neglect OR parental alcoholism OR parental maltreatment OR adversities OR childhood trauma OR attachment OR early life stress OR parental bonding OR adverse childhood experience OR childhood adversity) AND (schizophrenia OR schizoaffective disorder OR psychosis OR bipolar disorder OR borderline personality disorder OR major depressive disorder OR posttraumatic stress disorder)). We included only studies that assessed the direct relationship between adverse early life experiences (e.g. childhood trauma) and/or attachment and social cognition (e.g. theory of mind, emotion recognition) in adult patients with schizophrenia spectrum disorders, bipolar disorder, borderline personality disorder, major depressive disorder and/or posttraumatic stress disorder. Searches were limited to original articles written in English and published in peer-reviewed journals up to May 2018. Neuroimaging studies were excluded.
2.2. Quality assessment
The quality assessment was based on the revised version of the quality evaluation scale employed in previous systematic reviews [Reference Bauer, Pascoe, Wollenhaupt-Aguiar, Kapczinski and Soares45, Reference Misiak, Stanczykiewicz, Kotowicz, Rybakowski, Samochowiec and Frydecka46], and comprised the following items: (1) The clinical sample was representative of the target population (eligible cases were recruited in hospitals and/or mental health services settings with a diagnosis based on well-established clinical diagnostic manuals), (2) The clinical sample was appropriately matched to the control group (patients and controls matched for at least two confounding variables: age and/or sex and/or education level and/or body mass index), (3) The authors performed sample size calculations and/or power analysis, (4) The study used well-established measures of early life stress and attachment styles, (5) The study used well-established measures of social cognition, (6) The authors reported effect sizes and/or confidence intervals of their main findings. Each item scored one point if the criterion was met (i.e. present) and the overall quality score was calculated by adding up all the items.
2.3. Study characteristics
The literature search identified 2619 relevant publications of which 20 were found to meet criteria for inclusion after examining the titles and abstracts. Based on a review of the reference list of these papers a further five published studies met the inclusion criteria. In total 25 publications were included. These included nine studies conducted in patients with schizophrenia spectrum disorders, two studies included patients with bipolar disorder, six studies of patients with borderline personality disorder, three studies of patients with posttraumatic stress disorder, one study which included borderline personality disorder and bipolar disorder patients, one was performed on borderline personality disorder and major depressive disorder patients, two on patients with major depressive disorder and one was carried out in patients with borderline personality disorder plus additional personality disorders. Studies focused only on healthy participants were not included in this review; however, in patient studies in which a healthy comparison group was included, the data from these groups are reported. The PRISMA flow diagram is presented in Fig. 1 [Reference Moher, Liberati, Tetzlaff and Altman47] and the relevant studies are presented in Table 1.
3. Results
3.1. Quality evaluation
The quality of the 25 studies included in this systematic review was assessed by two independent reviewers and is presented in Supplementary Table 1. The scores ranged from 3 to 6 points (out of 6) in the quality assessment instrument. All of the studies recruited clinical populations in hospitals and mental health services, and their diagnosis was confirmed using well-established clinical diagnostic manuals (e.g. Structured Clinical Interview for DSM-IV (SCID) [Reference Association AP73])). Only three studies reported performing sample size calculations and/or power analysis [Reference Koelkebeck, Liedtke, Kohl, Alferink and Kret50, Reference Preißler, Dziobek, Ritter, Heekeren and Roepke71, Reference Powers, Etkin, Gyurak, Bradley and Jovanovic74] and six studies used a sample size of less than 30 patients [Reference Palmier-Claus, Berry, Darrell-Berry, Emsley, Parker and Drake52, Reference Petersen, Brakoulias and Langdon56, Reference Nazarov, Frewen, Oremus, Schellenberg, McKinnon and Lanius60, Reference Fletcher, Parker, Bayes, Paterson and McClure63–Reference Nicol, Pope and Hall65], thus limiting the generalisability of findings. Other methodological flaws included either poorly matched control groups [Reference Palmier-Claus, Berry, Darrell-Berry, Emsley, Parker and Drake52, Reference Garcia, Montalvo, Creus, Cabezas, Sole and Algora54, Reference Pos, Bartels-Velthuis, Simons, Korver-Nieberg, Meijer and de Haan61] or no control groups at all [Reference Jimenez, Sole, Arias, Mitjans, Varo and Reinares51, Reference Olbert, Penn, Reise, Horan, Kern and Lee53, Reference Beeney, Stepp, Hallquist, Scott, Wright and Ellison57, Reference Gunther, Dannlowski, Kersting and Suslow58, Reference Fletcher, Parker, Bayes, Paterson and McClure63, Reference Scott, Kim, Nolf, Hallquist, Wright and Stepp67, Reference MaBeth, Gumley, Schwannauer and Fisher69, Reference Lysaker, Gumley, Brune, Vanheule, Buck and Dimaggio70, Reference Powers, Etkin, Gyurak, Bradley and Jovanovic74, Reference Russo, Mahon, Shanahan, Solon, Ramjas and Turpin75]. The majority of the studies employed well-established measures of early life stress and attachment (e.g. Childhood Trauma Questionnaire (CTQ) [Reference Bernstein, Ahluvalia, Pogge and Handelsman76], Relationship Questionnaire [Reference Bartholomew and Horowitz77])) and social cognition (e.g. Reading the Mind in the Eyes Task [Reference Baron-Cohen, Wheelwright, Hill, Raste and Plumb78], Emotion Recognition Task [Reference Robbins, James, Owen, Sahakian, McInnes and Rabbitt79]) providing a valid description of the childhood experiences and social cognitive functioning. Less than half of the studies [Reference Schalinski, Teicher, Carolus and Rockstroh48, Reference Kilian, Asmal, Chiliza, Olivier, Phahladira and Scheffler49, Reference Jimenez, Sole, Arias, Mitjans, Varo and Reinares51–Reference Olbert, Penn, Reise, Horan, Kern and Lee53, Reference Beeney, Stepp, Hallquist, Scott, Wright and Ellison57, Reference Nazarov, Frewen, Oremus, Schellenberg, McKinnon and Lanius60, Reference Pos, Bartels-Velthuis, Simons, Korver-Nieberg, Meijer and de Haan61, Reference Fletcher, Parker, Bayes, Paterson and McClure63, Reference Nazarov, Frewen, Parlar, Oremus, MacQueen and McKinnon64, Reference Preißler, Dziobek, Ritter, Heekeren and Roepke71, Reference Powers, Etkin, Gyurak, Bradley and Jovanovic74] reported the effect sizes and/or the confidence intervals of the main statistical analyses affecting the interpretation of the findings.
Prisma flow diagram of studies selected for systematic review.
3.2. Early social environment and social cognition in major psychiatric disorders
3.2.1. Schizophrenia spectrum disorders
We identified a total of nine studies that investigated the impact of early life environment on social cognition in patients with schizophrenia spectrum disorders.
In a study of 34 patients with first-episode psychosis (FEP) MaBeth et al. [Reference MaBeth, Gumley, Schwannauer and Fisher69] showed that patients classified as having an insecure/dismissing (avoidant) attachment style had significantly lower scores on a measure of emotional ToM than patients with either a secure or an insecure/preoccupied (anxious) attachment style. However, the generalisability of these results was limited by the small sample size, particularly of patients with an insecure-preoccupied attachment style, and the absence of a healthy participant group. In terms of established illness, Donohoe et al. [Reference Donohoe, Spoletini, McGlade, Behan, Hayden and O’Donoghue72] examined the association between relationship style, an adult indicator of early childhood attachment, and attributional style in 73 patients with schizophrenia or schizoaffective disorder and 78 healthy controls. The authors found that lower ‘personalising bias’ (attributing negative events to others rather than to situational factors) was predicted by higher secure relationship style ratings in the patient group but not in healthy controls. Several studies since then have examined the link between (childhood) attachment/parental bonding styles and social cognitive outcomes in patients with an established psychotic disorder. Pos et al. [Reference Pos, Bartels-Velthuis, Simons, Korver-Nieberg, Meijer and de Haan61] reported that avoidant attachment (measured with the Psychosis Attachment Measure; PAM [Reference Berry, Wearden and Barrowclough80]) was significantly associated with cognitive (second order) and affective (first and second order) ToM in patients with a diagnosis of schizophrenia spectrum disorder (n = 111). Additionally, anxious attachment was linked to poorer performance in cognitive ToM (second order). Neither anxious nor avoidant attachment styles were associated with ToM measures in non-affected siblings (n = 106) or healthy controls (n = 63). By contrast, Olbert et al. [Reference Olbert, Penn, Reise, Horan, Kern and Lee53], who again used the PAM to assess the relationship between adult attachment style and social cognition in 138 patients with schizophrenia, found no correlations between these measures. The authors suggest that these findings may reflect construct validity issues with the PAM, the psychometric properties and construct validity in terms of measuring ToM.
Characteristics of the studies included in the review.
SZ: schizophrenia; SZD: schizoaffective disorder; BD: bipolar disorder; BPD: borderline personality disorder; MDD: major depressive disorder; PTSD: posttraumatic stress disorder; FEP: first-episode psychosis; LP: low performance; AP: average performance; HP: high performance; PAM: Psychosis Attachment Measure; CT: childhood trauma; MACE: Maltreatment and Abuse Chronology of Exposure Scale; MCCB: MATRICS Consensus Cognitive Battery; CTQ: Childhood Trauma Questionnaire; CTQ-SF: Childhood Trauma Questionnaire – Short Form; FEE: Fragebogen zum erinnerten elterlichen Erziehungsverhalten (German: questionnaire on recalled parental rearing behaviour); CBE: Conflicting Beliefs and Emotions; MAS: Metacognition Assessment Scale; MASC: Movie for the Assessment of Social Cognition); BLERT: Bell-Lysaker Emotion Recognition Task; ECR-R: Experience in Close Relationships Scale – Revised; CAT: Child Abuse and Trauma Scale; TAA: Trauma Assessment for Adults; AAS: Adult Attachment Scale; EAT: Expression Attribution Test; IPSAQ: Internal, Personal and Situational Attributions Questionnaire; SCAF: Social Cognition and Functioning; AIHQ: Ambiguous Intentions Hostility Questionnaire; MSCEIT-ME: Mayer–Salovey–Caruso Emotional Intelligence Test – Managing Emotions; IPT-15: Interpersonal Perception Task-15; PAI-BOR: Personality Assessment Inventory-Borderline Personality Disorder Identity Scale; IIP: Inventory of Interpersonal Problems; AAI: Adult Attachment Interview; RF: Reflective Function; TEI: Traumatic Events Inventory; RMET: Reading the Mind in the Eyes Task; ERT: Emotion Recognition Task; MOPS: Measure of Parental Style; CERQ: Cognitive Emotion Regulation Questionnaire; DERS: Difficulties in Emotion Regulation Scale; PBI: Parental Bonding Instrument; JACFEE: Matsumoto and Ekman Japanese and Caucasian Facial Expressions of Emotion; RQ: Relationship Questionnaire; AAPR: Adult Attachment Prototype Ratings; EERI: Emotion Experiencing and Regulation Interview; ERQ: Emotion Regulation Questionnaire; ToM; Theory of Mind; NR: not reported.
* gender and mean age was reported for three different cluster groups.
** non-affected siblings of patients.
*** 67 participants with PTSD symptoms (30% of the sample met diagnostic criteria for PTSD).
**** paranoid (n = 13), schizoid (n = 26), schizotypal (n = 14), antisocial (n = 8), borderline (n = 7), histrionic (n = 18), narcissistic (n = 3), avoidant (n = 14), dependent (n = 8), or obsessive-compulsive (n = 12) personality disorders.
In terms of association with early adversity, Lysaker et al. [Reference Lysaker, Gumley, Brune, Vanheule, Buck and Dimaggio70] investigated the relationship with social cognition in 67 patients with schizophrenia and 34 patients with schizoaffective disorder (a healthy participant group was not included in the study). Based on this analysis, the authors found that the group aware of their own emotions but not those of others had a significantly higher report of childhood sexual abuse. Significant associations were also reported in the study by Schalinski et al. [Reference Schalinski, Teicher, Carolus and Rockstroh48] comprised of 168 patients with schizophrenia spectrum disorders and 50 healthy controls. The results highlighted a negative impact of adverse childhood experiences, specifically physical neglect at age 11, on social cognitive function in schizophrenia. Similarly, Garcia et al. [Reference Garcia, Montalvo, Creus, Cabezas, Sole and Algora54] found a negative correlation between higher early life adversity total scores and ToM total scores in FEP patients and Kilian et al. [Reference Kilian, Asmal, Chiliza, Olivier, Phahladira and Scheffler49] provided additional evidence for the association between adverse life events and social cognition as they found that childhood neglect was a significant predictor of social cognitive deficits in the same population of patients. By contrast, in an analysis of the relationship between childhood adversity and social functioning in small clinical groups (20 patients with chronic schizophrenia, 30 FEP patients and 14 ultra-high risk individuals) and a larger healthy control group, Palmier-Claus et al. [Reference Palmier-Claus, Berry, Darrell-Berry, Emsley, Parker and Drake52] found that childhood adversity, as measured by the CTQ [Reference Bernstein, Ahluvalia, Pogge and Handelsman76], did not significantly predict performance on either measure of ToM (Reading the Mind in the Eyes Task, Hinting Task) in any of the statistical models they tested.
3.2.2. Bipolar disorder
Further, in a sample of 75 patients with bipolar disorder, Russo et al. [Reference Russo, Mahon, Shanahan, Solon, Ramjas and Turpin75] found that traumatic childhood experiences, specifically emotional neglect and physical abuse, resulted in impairments in the recognition of angry faces in comparison to those with no such history. A trend level association was also observed for physical neglect. A healthy comparison group was not included in this study. By comparison, a similar study by Jiménez et al. [Reference Jimenez, Sole, Arias, Mitjans, Varo and Reinares51] investigating the association between childhood trauma and cognitive performance in a sample of 113 bipolar patients did not fully replicate findings by Russo and colleagues [Reference Russo, Mahon, Shanahan, Solon, Ramjas and Turpin75] as they only observed a non-significant trend toward an association between physical neglect and social cognition (measured with the Managing Emotions branch of the MSCEIT [Reference Brackett and Salovey81]). However, as suggested by the authors, these findings may be due to the fact that the social cognitive tasks they used did not sufficiently measure this specific domain of social cognition.
3.2.3. Borderline personality disorder
In a sample of age and gender matched patients with bipolar disorder II (n = 24) and borderline personality disorder (n = 24), Fletcher et al. [Reference Green43] investigated the relationship between perceived parental style and emotional self-regulation showing a significant association between dysfunctional parenting experiences and maladaptive emotion regulation strategies. Another study conducted by Zheng et al. [Reference Pos, Bartels-Velthuis, Simons, Korver-Nieberg, Meijer and de Haan61] in 123 patients with various personality disorders and 166 healthy controls, found that parental care significantly predicted emotional accuracy in patients and controls. Specifically, better maternal care was associated with greater accuracy in recognising expressions of sadness, whereas worse quality of paternal care was significantly associated with better recognition of anger. Significant associations were also reported in the study by Scott et al. [Reference Jimenez, Sole, Arias, Mitjans, Varo and Reinares51] comprised of 100 patients with borderline personality disorder (35 males and 65 females), with no comparison control group. The authors showed that preoccupied (anxious) attachment style and difficulties with emotion regulation were significantly positively associated. More recently, Beeney et al. [Reference Beeney, Stepp, Hallquist, Scott, Wright and Ellison57] provided additional evidence for the relationship between attachment insecurities and social cognition as they reported a link between insecure attachments and deficits in mentalization in a sample of 150 patients with borderline personality disorder. Furthermore, Brüne et al. [Reference Pos, Bartels-Velthuis, Simons, Korver-Nieberg, Meijer and de Haan61] found that ToM was associated with parenting style, childhood trauma and attachment style in the patient group based on a study of 30 female borderline personality disorder patients and 30 female healthy controls. Specifically, poorer affective ToM performance was associated with lack of maternal emotional warmth, rejection and punishment, physical neglect and abuse, emotional neglect and preoccupied attachment style. Detrimental effects of childhood trauma, specifically sexual abuse and punishment, on ToM abilities were also reported by Preissler et al. [Reference Preißler, Dziobek, Ritter, Heekeren and Roepke71], and more recently by Petersen et al. [Reference Petersen, Brakoulias and Langdon56] based on 64 and 19 patients with borderline personality disorder, respectively. Likewise, in the study comprised of 20 borderline personality disorder patients and 21 healthy controls, Nicol et al. [Reference Henry, von Hippel, Molenberghs, Lee and Sachdev44] reported a significant association between a childhood history of emotional and physical abuse, and poorer emotional recognition – specifically, identification of disgust. Finally, another study on childhood adversity conducted by Carvalho Fernando [Reference Powers, Etkin, Gyurak, Bradley and Jovanovic62] explored the association between self-reported childhood traumatic experiences and emotional self- regulation in a sample of 49 borderline personality disorder and 48 major depressive disorder patients and 63 healthy controls. They observed that maltreatment experiences, especially emotional neglect and abuse, were significantly associated with poorer emotional self-regulation in both patients and healthy controls, as measured with the Emotion Regulation Questionnaire [Reference Fletcher, Parker, Bayes, Paterson and McClure63] and the Difficulties in Emotion Regulation Scale [Reference Nazarov, Frewen, Parlar, Oremus, MacQueen and McKinnon64].
3.2.4. Major depressive disorder
Evidence for the association between childhood adversity and social cognitive functioning was also provided by Günther et al. [Reference Gunther, Dannlowski, Kersting and Suslow58] in a sample of 45 patients with major depressive disorder; no healthy participants were included in the study. The authors reported that more severe maltreatment during childhood resulted in mood-congruent biases in emotion processing (i.e. sustained attention toward sad facial expressions). In terms of the association with attachment, Koelkebeck et al. [Reference Koelkebeck, Liedtke, Kohl, Alferink and Kret50] showed that dependent and anxious attachment styles were related to lower scores on the ToM task in 38 patients with major depressive disorder patients suggesting that trustful and less dependent attachment in relationships may result in better social cognitive abilities.
3.2.5. Posttraumatic stress disorder
Three further studies have examined the association between adverse early social environment and social cognition in patients with posttraumatic stress disorder. The first study by Powers et al. [Reference Powers, Etkin, Gyurak, Bradley and Jovanovic74] conducted in 67 individuals with PTSD symptoms (19 of which met diagnostic criteria for PTSD) and comparing individuals with low and high childhood trauma reported that moderate-to-severe childhood abuse was significantly related to worse emotional regulation scores. This finding was independent of current PTSD symptoms, depressive symptoms, and adult trauma exposure. Furthermore, Nazarov et al. [Reference Nazarov, Frewen, Parlar, Oremus, MacQueen and McKinnon64] demonstrated, in a sample of female patients with PTSD (n = 31) and matched healthy controls (n = 20), that traumatic childhood experiences in individuals with PTSD were associated with difficulties interpreting scenes depicting kinship interactions, as measured with the Interpersonal Perception Task-15 [Reference Costanzo and Archer82]. Finally, in the subsequent and similarly sized study by Nazarov et al. [Reference Nazarov, Frewen, Oremus, Schellenberg, McKinnon and Lanius60] examining the ability to discriminate affective prosody in women with PTSD and healthy controls, the authors observed that childhood maltreatment (specifically emotional abuse, emotional and physical neglect) was related to less accurate discrimination and slower identification of emotions.
4. Discussion
The main aim of this review was to synthesise the literature exploring the association between early life environment (i.e. attachment, childhood trauma) and social cognition in individuals with a diagnosis of either schizophrenia, bipolar disorder, borderline personality disorder, major depressive disorder and/or posttraumatic stress disorder. Thus, we conducted a systematic search of the literature, which identified 25 relevant studies. Of these studies, nine were conducted in patients with schizophrenia spectrum disorders, seven in patients with personality disorders, four in patients with affective disorders, three in patients with anxiety disorders and two in mixed groups of patients with either affective or personality disorders. This literature is relatively recent, with the first study being published ten years ago [Reference Donohoe, Spoletini, McGlade, Behan, Hayden and O’Donoghue72], with an apparent growth in the numbers of articles published, which indicates an increased interest in the topic.
The majority of the studies reviewed showed a significant association between early childhood experience, including both sub-optimal parenting and childhood adversity relating to neglect or abuse, and poorer social cognition. Together, these data suggest that these negative early social experiences deleteriously impact on later social cognitive function in patients, and to some extent in healthy participants also. Specifically, emotional and physical abuse, neglect, and avoidant attachment styles were found to be the strongest predictors of ToM, emotion recognition deficits, and emotional dysregulation. The only studies (n = 3) that did not report this relationship were either based on small sample sizes (n<30) [Reference Palmier-Claus, Berry, Darrell-Berry, Emsley, Parker and Drake52] which were likely to have been underpowered, employed a measure of attachment with unclear construct validity [Reference Olbert, Penn, Reise, Horan, Kern and Lee53] or used a task that was not sufficient to measure a specific domain of social cognition [Reference Jimenez, Sole, Arias, Mitjans, Varo and Reinares51].
Some limitations should be acknowledged regarding the generalisability of the data reviewed in this study. Firstly, a number of studies were based on small sample sizes, which may not have been sufficiently powered for detecting small effects regarding the relationship between adverse early life environment and social cognition. Secondly, the majority of the studies included either poorly matched control groups or no control groups at all, thus limiting the generalisability and reliability of findings. In particular, this made it difficult to determine whether there were differential effects of early social environment on social cognition according to status as patient or healthy controls, or between patient groups. Thirdly, these studies were conducted in patients of different age groups and phases of the illness (e.g. FEP, chronic). While this has the advantage of reflecting the effects of social cognition on a broader population, the effects on different illness phases are unknown. Another limitation of the studies reviewed here is that the early childhood experiences were assessed through subjective retrospective measures affecting potentially the accuracy of these reports. A number of studies have previously provided strong support for the validity and reliability of the retrospective self-reports of childhood maltreatment [Reference Dill, Chu, Grob and Eisen83–Reference Hardt and Rutter85]. However, an important factor that has yet to be addressed is whether and to what extent age of onset and frequency of traumatic experiences moderate their effects [Reference Maercker, Michael, Fehm, Becker and Margraf9, Reference Hagenaars, Fisch and van Minnen86]. Finally, social cognitive measures used in the studies were considerably heterogeneous, thus preventing us from conducting a meta-analysis. Notwithstanding these limitations, and as already noted, the vast majority of the studies provided firm evidence of the significant effects of early childhood environment on social cognitive functioning.
4.1. Early social environment and social cognitive deficits in major psychiatric disorders: an attachment perspective
As noted in our introduction, Attachment theory [Reference Bowlby26] provides a framework for understanding the potential cognitive mechanisms behind this relationship between early social environment and social cognition. This theory proposes that typical social, cognitive and emotional development is formed on the basis of an attachment bond with the caregiver, which provides a child with the inputs from which internal representations of others and self are constructed. If the attachment process is disrupted, for instance by a traumatic event, the child may not develop the secure base essential to form and maintain relationships throughout life and acquire social cognitive skills.
The results of our review are complimentary to existing evidence of a strong link between adverse parental experience and childhood trauma and mental health problems in adulthood. In particular, exposure to early life stress has been frequently shown to increase the risk for psychosis [Reference Janssen, Krabbendam, Bak, Hanssen, Vollebergh and de Graaf87, Reference Bebbington, Jonas, Kuipers, King, Cooper and Brugha88], bipolar disorder [Reference Etain, Henry, Bellivier, Mathieu and Leboyer89, Reference Fisher and Hosang90], borderline personality disorder [Reference Battle, Shea, Johnson, Yen, Zlotnick and Zanarini13, Reference Zanarini, Williams, Lewis, Reich, Vera and Marino91], major depressive disorder [Reference Molnar, Buka and Kessler92, Reference Widom, DuMont and Czaja93] and posttraumatic stress disorder [Reference Widom94]. There is also consistent evidence that childhood adversity, specifically emotional abuse, is associated with clinical characteristics of these disorders, including an earlier onset of the illness [Reference Darves-Bornoz, Lempérière, Degiovanni and Gaillard95, Reference Li, Liu, Zhu, Zhang, Tang and Wang96], an increased risk of at least one lifetime suicide attempt [Reference Alvarez, Roura, Oses, Foguet, Sola and Arrufat97, Reference Etain, Aas, Andreassen, Lorentzen, Dieset and Gard98], and higher symptom severity [Reference Hagenaars, Fisch and van Minnen86, Reference Bentall, Wickham, Shevlin and Varese99, Reference Martins, Von Werne Baes, Tofoli and Juruena100]. Because social cognitive abilities are likely to be acquired through interaction with primary caregivers and the broader environment, insecure attachment and traumatic experiences in early developmental stages may disrupt their development. Thus, social cognitive impairments may be a possible pathway through which childhood adversities increase the risk for developing psychiatric disorders and act as a mediator between negative early life experiences and later psychopathology. A direct link between social cognition and symptoms is suggested by the fact that many psychotic symptoms, such as auditory hallucinations or reasoning biases, referred to as ‘jumping to conclusions’, can be a result of attribution of one’s actions, feelings and thoughts to external sources and impaired mentalising abilities, respectively [Reference van Os, Kenis and Rutten101].
4.2. Early social environment and social cognitive development in major psychiatric disorders: biological factors
Since the era of candidate gene studies, the relationship between early life adversity, genetic risk and phenotypic variation has been a subject of great interest to the field of psychiatric genetics. Two genetic variants previously associated with psychiatric risk receiving particular attention have been the Serotonin transporter gene (5-HTT) and the BDNF Val66Met polymorphism. While the potential role for 5-HTT in mediating the effects of early adversity on later outcomes was first highlighted by Caspi et al. [Reference Caspi, Sugden, Moffitt, Taylor, Craig and Harrington102], the role of this variant has remained controversial, and unsupported in a meta-analysis by Risch et al. [Reference Risch, Herrell, Lehner, Liang, Eaves and Hoh103]. To our knowledge, no social cognition studies in humans have been carried out that test the interactive effects of 5-HTT and early adversity, although evidence from animal studies point to cognitive effects [Reference Robbins104]. Similarly, we found only one study of the interaction between early adversity and the Val66Met polymorphism at BDNF in relation to cognition [Reference Aas, Haukvik, Djurovic, Bergmann, Athanasiu and Tesli105], but a measure of social cognition was not included in this study.
Independent of early environment, variation at several genomic loci has been implicated in social cognition, both for specific disorders (e.g. in Schizophrenia with variants within ZNF804A [Reference Hargreaves, Morris, Rose, Fahey, Moore and Cummings106] and MIR137 [Reference Mothersill, Morris, Kelly, Rose, Fahey and O’Brien107]) and across disorders (e.g. Oxytocin; for a recent review see Kendrick et al. [Reference Kendrick, Guastella and Becker108]). To date, however, and to our knowledge, no studies have tested the interaction between social cognition, early adversity, and genome wide associated risk loci for psychiatric disorders. This remains a priority for future research that seeks to model the relationship between early adversity and genetic risk in contribution to social cognitive development.
Patients with major psychiatric disorders reporting a history of early adversity have also been found to show increased hyperactivity of the hypothalamic-pituitary-adrenal (HPA) axis as compared to those with no prior experience of maltreatment [Reference Braehler, Holowka, Brunet, Beaulieu, Baptista and Debruille109, Reference Peng, Long, Li, Guo, Wu and Yang110]. Furthermore, there is some evidence that this relationship may be conditional on genetic variation at the 5-HTT locus [Reference Alexander, Kuepper, Schmitz, Osinsky, Kozyra and Hennig111–Reference Lardinois, Lataster, Mengelers, Van Os and Myin-Germeys113]. This hyperactivity of the HPA axis is thought to affect the neural growth in developmentally sensitive structures and function of brain regions with a high density of glucocorticoid receptors (e.g. hippocampus and prefrontal cortex [Reference Zhu, Liu, Li, Liu, Chen and Han114]) as well as regions sensitive to repeated neuronal excitation (e.g. amygdala [Reference Mothersill and Donohoe115]). These structural and functional changes may result in disruption of cognitive processes, specifically memory, learning, and social information processing [Reference Walder, Walker and Lewine116]. Chronically elevated corticosterone levels resulting from early life adversities have also been found to hinder the integrity of ventral and dorsal medial prefrontal cortex, which comprise the ‘neural circuitry of self’, leading to disruptions in self-referential and self-monitoring processes [Reference Brent, Seidman, Thermenos, Holt and Keshavan117]. Furthermore, in major psychiatric disorders, a history of childhood abuse has been associated with decreased grey matter in brain areas involved in social cognitive processes, i.e. dorsolateral prefrontal cortex, ventromedial prefrontal cortex, and amygdala [Reference Aas, Navari, Gibbs, Mondelli, Fisher and Morgan118–Reference Aguilar-Ortiz, Salgado-Pineda, Marco-Pallarés, Pascual, Vega and Soler122]. Although smaller gray matter volume is found in several brain regions associated with higher cognitive processes in all patients with psychiatric disorders, the experience of childhood trauma appears to be an additional risk factor for gray matter loss [Reference Sheffield, Williams, Woodward and Heckers119]. Numerous studies have also shown that childhood adversities contribute to functional brain alterations that may lead result in social cognitive deficits. For instance, Quidé and colleagues [Reference Quide, Ong, Mohnke, Schnell, Walter and Carr123] reported a positive association between early life trauma and activation of the dorsomedial prefrontal cortex in schizophrenia and an increased amygdala activation was reported by Hentze et al. [Reference Hentze, Walter, Schramm, Drost, Schoepf and Fangmeier124] in trauma-exposed patients with chronic depression during an affective ToM task. Additionally, in a recent study involving patients with schizophrenia, Cancel et al. [Reference Cancel, Comte, Boutet, Schneider, Rousseau and Boukezzi125] has found that during an emotional valence task, childhood trauma was negatively associated with decreased connectivity between the amygdala and the precuneus, the posterior cingulate cortex and the calcarine sulcus, all of which are involved in theory of mind.
5. Conclusion
Deficits in social cognition are suggested to represent a core aspect of disability in psychiatric disorders such as Schizophrenia, and may be more predictive of psychosocial functioning than general cognitive ability [Reference McGlade, Behan, Hayden, O’Donoghue, Peel and Haq126]. The fact that these deficits are not generally improved by antipsychotic medication [Reference Daros, Ruocco, Reilly, Harris and Sweeney127, Reference Kucharska-Pietura and Mortimer128] makes social cognition an important treatment target, and makes the development of a causal working model of social cognitive deficits of crucial importance.
This systematic review provides a comprehensive picture of current research on the relationship between early life environment and social cognition in patients with major psychiatric disorders. The studies reviewed suggest a crucial role of early childhood experiences in the development of social cognitive abilities, which may represent a mediator between early life adversities and later symptom severity. Studies to understand the mechanisms by which this occurs at neurocognitive and biological levels remain an important goal for the field. Alongside these research needs, the findings of this review underline the importance of addressing the various types of early childhood social experiences and adversity in clinical assessment and interventions, given the abundant evidence of the later effects of these experiences. Finally, the studies reviewed are relevant from a public health perspective, highlighting the importance of early childhood interventions (e.g. parenting programs) that seek to minimise the occurrence and long term effects of adversity in early life.
Funding
This work was funded by grants to GD from the European Research Council (ERC-2015-STG-677467) and Science Foundation Ireland (SFI-16/ERCS/3787).
Conflict of interest
None to declare.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.eurpsy.2018.06.006.
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