Review articleNeuropsychological functioning of childhood trauma and post-traumatic stress disorder: A meta-analysis
Introduction
Research suggests that trauma exposure during childhood has implications for neurodevelopmental outcomes. The physiological stress response is triggered through exposure to a traumatic event, and can have detrimental effects on the brain if prolonged. Activation of the physiological stress response results in the release of glucocorticoids, among other neurochemicals, in various brain regions (Gunnar and Quevedo, 2007), with suppressed or elevated levels being associated with impaired brain development and functioning (Lupien et al., 2009). Supporting this notion, prolonged trauma exposure in the context of childhood maltreatment or deprivation is consistently associated with dysregulated glucocorticoid and catecholamine activity in the developing brain (Weber and Reynolds, 2004, Wilson et al., 2011).
Exposure to extreme stress or deprivation (i.e., trauma) has the potential to disrupt experience-dependent neuroactivity during critical periods of development, which may adversely affect neural structure and function, and disrupt the overall course of neurodevelopment (Gunnar and Quevedo, 2007, Perry et al., 1995). The brain develops in a hierarchical manner starting with primitive structures and functions (i.e., the brainstem and breathing) and ending with complex cortical structures and functions (i.e., frontal lobes and executive functioning; Gogtay and Thompson, 2010). At the neuronal level, this process involves dendritic arborisation, myelination, and synaptogenesis (Anderson et al., 2014, Perry et al., 1995). Given different brain regions develop, organise and become fully functional at different critical developmental periods, age at trauma exposure probably plays a significant role in neurodevelopmental outcomes (Perry et al., 1995, Teicher et al., 2003, van der Kolk, 2003). Supporting this notion, findings from neuroimaging and psychophysiological studies suggest that early life stress occurring during critical developmental periods may affect those brain regions undergoing specific growth spurts at that time, and may also disrupt the development of higher-order association cortices that have prolonged developmental trajectories (e.g., the prefrontal cortex; for review see Pechtel and Pizzagalli, 2011).
In addition to the impact of the trauma exposure itself, the development of post-traumatic stress disorder (PTSD) probably places a child at increased risk of adverse neurodevelopmental outcomes. Post-traumatic stress disorder is a psychiatric disorder that may result from a single-traumatic event, although a dose-response relationship or ‘building-block effect’ is noted in the literature, with cumulative trauma exposure rendering an individual at increased risk of developing the disorder (Breslau et al., 1999, Brewin et al., 2000, Copeland et al., 2007, Wilker et al., 2015). It is characterized by the onset of trauma-related symptoms including intrusive memories, flashbacks, or nightmares of the trauma; avoidance of trauma-related stimuli; marked alterations in arousal and reactivity post-trauma; and negative alterations in cognitions and mood post-trauma (American Psychiatric Association, 2013).
A widely accepted neurobiological model of PTSD hypothesizes core symptoms of the disorder are associated with a maladaptive stress response that remains disrupted in the absence of the traumatic event (Rauch et al., 1998, Yehuda et al., 2015). There is an abundance of studies investigating the neuroendocrinology, psychopathophysiology, neurostructural and neurofunctional correlates of PTSD in view of this notion. This literature is beyond the scope of this paper, but has been comprehensively reviewed elsewhere (see Pitman et al., 2012, Yehuda et al., 2015). In brief, PTSD symptoms are thought to be associated with structural and functional abnormalities across interacting frontolimbic brain regions that are implicated in the physiological stress response, emotion processing and fear extinction. Core brain regions of interest include the amygdala, hippocampus and prefrontal cortex (Pitman et al., 2012, Yehuda et al., 2015).
The neurocircuitry model of PTSD posits the amygdala response remains exaggerated or hyperactive in the absence of the traumatic event, while the prefrontal cortex remains hyporesponsive, failing to regulate the amygdala response and inhibit associated emotions and irrelevant cognitions (Pitman et al., 2012, Yehuda and LeDoux, 2007, Yehuda et al., 2015). Together these dysfunctions result in deficits in emotion regulation, attentional biases toward perceived threats, increased fear responses, and impaired extinction of trauma-related memories (Pitman et al., 2012). The hyperactive amygdala is also believed to inhibit hippocampal function, leading to impairments in the consolidation of hippocampal-dependent features (i.e., autobiographical memories) of the traumatic event (Goodman et al., 2012). The hyperactive amygdala encodes and consolidates its own version of the traumatic event, with sensory-based representations of the trauma in the amygdala, insula and dorsal visual stream thought to be involved in vivid flashbacks (Brewin et al., 2010, Goodman et al., 2012). Inhibition of the hippocampus is likely associated with the individual’s inability to voluntarily recall important aspects of the traumatic event and fragmented or disorganised recall of the traumatic memory (Goodman et al., 2012). Disruption in the hippocampus is also probably associated with deficits in contextual processing post-trauma, whereby the individual fails to distinguish safe from dangerous contexts, resulting in an exaggerated response to trauma-related stimuli (Yehuda and LeDoux, 2007).
Findings from adult structural and functional neuroimaging research show abnormalities in these key frontolimbic regions in individuals with PTSD, providing support for the neurocircuitry model of PTSD (Garfinkel and Liberzon, 2009, Hayes et al., 2012, Patel et al., 2012, Rauch et al., 1998). With regard to the paediatric literature, however, neuroimaging studies on PTSD are relatively scarce. It is therefore difficult to determine whether this neurobiological model is an accurate depiction of childhood PTSD. Current findings are variable and are not entirely consistent with the documented neuropathological process involved in the adult traumatic stress response and PTSD. A detailed review is beyond the scope of this article but has been comprehensively covered in previous literature (see Rinne-Albers et al., 2013).
In brief, results have shown abnormal hippocampal function (Carrión et al., 2010a, Carrión et al., 2010b, Garrett et al., 2012, McLaughlin et al., 2014, Yang et al., 2004), but not structure (Karl et al., 2006, Rinne-Albers et al., 2013, Woon and Hedges, 2008). Abnormalities are also noted in frontal function (Crozier et al., 2014, Garrett et al., 2012, Yang et al., 2004) and structure (Carrión et al., 2001, Carrión et al., 2009, Carrión et al., 2010a, Carrión et al., 2010b, De Bellis et al., 2002, Richert et al., 2006). Whilst findings on amygdala structure are reportedly normal (Woon and Hedges, 2008), emerging research shows a significant positive association between age and right amygdala volumes in children with PTSS/PTSD, thus age at investigation probably plays a critical role in research findings (Weems et al., 2015, Weems et al., 2013).
Abnormalities in the hippocampus, frontal regions and amygdala, have implications for neuropsychological functioning and behavioural outcomes. For example, the hippocampus is critical in the formation of memories, while the frontal regions are responsible for various higher-order cognitive functions including attentional control, working memory, inhibition, impulse control, and problem-solving (Schoenberg and Scott, 2011). The amygdala is responsible for emotional processing and can influence the functioning of these regions (Schoenberg and Scott, 2011). Disruption to these regions has the potential to not only impact upon cognitive function, but also upon behavioural and academic outcomes (Perfect et al., 2016).
The neuropsychological effects of trauma exposure and PTSD have received some attention in the literature, although findings are variable and difficult to interpret. Research on the effects of trauma exposure and PTSD employ different research designs that can be characterized as follows: 1) comparisons of children exposed to trauma with unknown PTSD status to healthy controls or normative data; 2) comparisons between children with PTSD and healthy controls; 3) comparisons between trauma-exposed children with and without PTSD; or 4) comparisons between children with PTSD, trauma-exposed children without PTSD and healthy controls.
Literature investigating the neurocognitive outcomes of trauma-exposed children has mostly focused on maltreated populations and has not typically investigated the role of PTSD. Findings from studies are variable. In some instances, comparisons to healthy controls or norms suggest significantly lower overall IQ (Carrey et al., 1995, Naude et al., 2004, Pears and Fisher, 2005), verbal and non-verbal intellectual skills (Basta and Peterson, 1990, Carrey et al., 1995, Huth-Bocks et al., 2001; Mills et al., 2011; Naude et al., 2004, Nolin and Ethier, 2007), attention and executive functioning (Bücker et al., 2012, Chugani et al., 2001, Hanson et al., 2013, Nolin and Ethier, 2007, Weller and Fisher, 2013), and learning and memory in trauma exposed children (Chugani et al., 2001, Hanson et al., 2013, Scrimin et al., 2009). In contrast, other comparisons do not report significant differences between groups with regard to these skills (Basta and Peterson, 1990, Huth-Bocks et al., 2001, Nolin and Ethier, 2007, Pears and Fisher, 2005, Perna and Kiefner, 2013, Sadeh et al., 1994).
Given the above described studies fail to document the presence of PTSD, it is difficult to determine if impairments in cognitive functioning are due to chronic trauma exposure itself or other confounding variables. Findings from studies that assessed the impact of PTSD compared to healthy controls suggest lower IQ, learning, memory, attention, and executive function in children with PTSS/PTSD (Carrión et al., 2008, DePrince et al., 2009, Moradi et al., 1999, Scrimin et al., 2006, Yasik et al., 2007). However, without comparison to a trauma-exposed group without PTSD, it is unclear whether these deficits are due to PTSD, trauma-exposure or both. Comparisons between trauma exposed children with and without PTSD are equivocal and do not shed light on this dilemma. Specifically, some studies reported no differences between these groups in IQ, attention, working memory, processing speed, memory and inhibition (Samuelson et al., 2010, Yang et al., 2014), whilst others reported poorer learning, memory, and cognitive flexibility in children with PTSD (Samuelson et al., 2010, Schoeman et al., 2009, Yasik et al., 2007).
Findings from studies that compared all three groups of children (i.e., those with PTSD, trauma-exposed without PTSD and healthy controls) suggest poor IQ, visual attention, learning and memory, and inhibition in children exposed to familial trauma, irrespective of PTSD diagnosis, compared to healthy controls (De Bellis et al., 2009, Scrimin et al., 2006). In contrast, Barrera et al. (2013) did not find significant memory differences across children exposed to familial trauma with PTSD, without PTSD and healthy controls. Whereas, Saigh et al. (2006) found children with PTSD following non-familial trauma showed significantly lower IQ and verbal intellectual abilities compared to both trauma-exposed counterparts without PTSD and healthy controls. Children with PTSD also performed significantly worse on a working memory measure, but only in comparison to healthy controls (Saigh et al., 2006).
It is difficult to draw conclusions regarding the impact of PTSD and trauma exposure on cognitive functioning from current literature. Differences in methodologies likely account for some of the variability observed across findings. The role of confounding variables, such as SES, age at trauma exposure, and trauma type, is also unclear. Trauma type probably plays a critical role in findings as well, with the effects of trauma and PTSD likely differing in children exposed to familial compared to non-familial trauma.
Literature suggests distinction between familial versus non-familial trauma may play a critical role in whether children show cognitive deficits and thus it may help explain some of the variability in findings across studies. DePrince et al. (2009) investigated the effects of familial (i.e., childhood maltreatment that is perpetrated by a parent, caregiver or relative) and non-familial trauma (e.g., exposure to a natural disaster) on cognitive function. Results showed that children exposed to familial trauma performed more poorly on working memory, inhibition, auditory attention and information processing measures. These effects were maintained even when the contributions of dissociation, anxiety symptoms including those of PTSD, SES and potential traumatic brain injury (TBI) were controlled for in the analyses. These results also bring into question the role of the PTSD symptoms in the detriment to cognitive function, although it should be noted that the mean symptom severity score for each of the groups fell well below the reported cut-off for detecting a diagnosis of PTSD (DePrince et al., 2009, Steinberg et al., 2004), suggesting that these groups of children probably suffered mild symptoms. Further exploratory analyses also suggested the number of familial but not non-familial traumas explained unique variance in cognitive function scores. These findings indicate that trauma-related factors other than chronicity may impact upon a children’s cognitive functioning.
The greater effects of familial trauma may be due to both the chronicity and relational nature of the trauma experienced. Infancy, childhood and adolescence are periods in which individuals are particularly vulnerable to maladaptive stress responses. These developmental periods are associated with high biological dependency on the caregiver and physiological and psychological immaturity (Gunnar and Quevedo, 2007, Stratakis and Chrousos, 1995). Therefore, given the young child depends on his/her caregiver for survival, it is not surprising that childhood deprivation and abuse that is perpetrated by a parent is associated with neurobiological and psychological abnormalities, including a maladaptive stress response and disrupted attachment (Gunnar and Quevedo, 2007, Kira, 2001). Supporting this notion, pre-clinical studies in rodents and non-human primates consistently suggest early maternal separation has long-term neurotoxic effects, including altered HPA-axis activity, neural abnormalities and behavioural dysfunction (Lupien et al., 2009). Consequently, distinction between familial and non-familial trauma appears important.
Findings on the neuropsychological functioning in trauma-exposed children with and without PTSD are variable and difficult to interpret. While they do suggest cognitive deficits in trauma-exposed children, it remains unclear whether these are due to the effects of PTSD or the trauma exposure itself. Results from studies on adults also appear controversial (Qureshi et al., 2011), although meta-analytic syntheses of the literature suggest adult PTSD is associated with deficits in learning and memory, especially in the verbal domain, processing speed, attention/working memory, and executive function (Brewin et al., 2007, Johnsen and Asbjørnsen, 2008, Polak et al., 2012, Scott et al., 2015). Generalizability of these findings to children with PTSD is unknown, and may be limited considering documented neuroimaging differences between adults and children (e.g., decreased hippocampal volumes associated with adult but not childhood PTSD; Karl et al., 2006, Woon and Hedges, 2008).
While literature reviews on the cognitive functioning of childhood trauma exposure and PTSD are available (Irigaray et al., 2013, Turley and Obrzut, 2012), none have implemented statistical techniques to evaluate the magnitude of such deficits. Furthermore, these reviews did not attempt to disentangle the effects of trauma exposure versus PTSD. Therefore, the primary aim of this study was to use meta-analytic techniques to evaluate the existing evidence for cognitive impairments in children exposed to non-familial trauma and familial maltreatment-related trauma, with or without current or resolved acute or chronic post-traumatic stress reactions. Secondary aims were to disentangle the cognitive effects of PTSD versus trauma exposure and to assess the cognitive impact of familial versus non-familial trauma and age at assessment.
Section snippets
Methods
The following procedures were conducted as per the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (Liberati et al., 2009). Consistent with these guidelines, this meta-analysis was prospectively registered on the National Institute for Health Research PROSPERO International Prospective Register of Systematic Reviews website (registration number: CRD42014006873).
Study demographics
Together the 27 studies comprised 1526 participants, including 412 TE children, PTSD unknown; 300 PTSD+ children, 323 PTSD-, and 491 trauma-naive HCs. Table 2 shows trauma characteristics and cognitive domains investigated in each of the studies. Very few studies reported on important variables that have the potential to confound findings, such as time since trauma and PTSS severity. Trauma duration and age at onset or occurrence were also rarely reported. This is possibly due to assumed
Discussion
The primary aim of this study was to use meta-analytic techniques to evaluate the existing evidence for cognitive impairments in children exposed to non-familial and familial maltreatment-related trauma, with or without current or resolved acute or chronic post-traumatic stress reactions. Secondary aims were to disentangle the effects of PTSD and trauma exposure, and to assess the role of familial versus non-familial trauma and age at assessment.
Conclusions
Findings from this meta-analytic study suggest children exposed to trauma with and without PTSD display cognitive deficits. Greatest impairments in a broad range of functions are associated with a diagnosis of PTSD. The cognitive functioning of children exposed to trauma without PTSD appears to lie intermediate to children with PTSD and HCs. However, it remains difficult to disentangle the effects of PTSS and trauma exposure itself. Chronic trauma exposure likely results in ongoing activation
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