Dissociation is conceptualised both as a cognitive trait in the general population and as a psychological state which is linked to certain psychopathologies.Reference Holmes, Brown, Mansell, Fearon, Hunter and Frasquilho1 Non-pathological dissociation has been described as a cognitive trait involving suggestibility, fantasy proneness and daydreaming,Reference Giesbrecht, Lynn, Lilienfeld and Merckelbach2 rather than as a psychological symptom.Reference de Ruiter, Elzinga and Phaf3 Trait dissociation has been linked to increased emotionally elaborated memories,Reference Oathes and Ray4 as well as poor memory for associative material and diminished executive control.Reference Amrhein, Hengmith, Maragkos and Hennig-Fast5 Theorists vary on their conceptualisations of dissociative experiences, some believing that these fall on a continuum from mild to pathologicalReference Hilgard6,Reference Bernstein and Putnam7 and others arguing for a taxonomic distinction between trait and pathological dissociationReference Waller, Putnam and Carlson8 which may be differentially related to past trauma;Reference Irwin9 however, all dissociations share some cognitive disruptions in level of awareness.Reference Butler10 Therefore, identifying neurostructural correlates of non-pathological dissociation may inform aspects of cognitive neuroscience in general and suggest key brain regions potentially involved in the understanding, identification and treatment of pathological dissociation. We are not aware of any brain imaging research directly assessing trait dissociation in healthy adults or children, so this exploratory study of normative dissociation in healthy children is truly novel.
Neuroimaging in pathological dissociation
This is the first neuroimaging study of trait dissociation in a healthy population and brain regions involved in normative dissociation are unknown; however, previous studies have identified brain regions involved in people with pathological dissociation. For a comprehensive review of neurobiological findings in pathological dissociation, we direct readers to a 2021 review by Roydeva & Reinders.Reference Roydeva and Reinders11 This review identified 44 structural neuroimaging studies and reported that decreased volumes in limbic structures – specifically the hippocampus, basal ganglia and thalamus – are common in pathological dissociation. Very few volumetric studies have examined pathological dissociation in children or adolescents. Such studies found that dissociation correlated negatively with total corpus callosum volume in youth with post-traumatic stress disorder (PTSD);Reference De Bellis, Baum, Birmaher, Keshavan, Eccard and Boring12,Reference De Bellis, Keshavan, Frustaci, Shifflett, Iyengar and Beers13 dissociation was not associated with superior temporal gyrus volumes in youth with PTSD;Reference De Bellis, Keshavan, Frustaci, Shifflett, Iyengar and Beers13 and dissociative symptoms were negatively correlated with right amygdala and positively correlated with left prefrontal volumes in adolescents with PTSD.Reference Mutluer, Şar, Kose-Demiray, Arslan, Tamer and Inal14 The one functional study of pathological dissociation in traumatised children found that dissociation was negatively correlated with bilateral putamen activation in children with reactive attachment disorder.Reference Mizuno, Takiguchi, Yamazaki, Asano, Kato and Kuriyama15 These limited findings in children again point to decreased volume or function in limbic structures and add a potential increase in prefrontal volumes in the presence of dissociation.
Roydeva & Reinders’ reviewReference Roydeva and Reinders11 also included 71 functional neuroimaging studies of pathological dissociation. Most of the reviewed studies were conducted in patient groups with PTSD or dissociative identity disorder (DID) and measured brain activity in response to emotional stimuli. Pathological dissociation is a transdiagnostic symptom which is the defining feature of DID, dissociative amnesia and depersonalisation disorder, and is associated with PTSD and borderline personality disorder.Reference Lyssenko, Schmahl, Bockhacker, Vonderlin, Bohus and Kleindienst16 Underlying the generally well-accepted aetiological role of trauma in pathological dissociation,Reference Bremner17 pathological dissociation may function as a coping strategy allowing psychological escape from traumatic events.Reference de Ruiter, Elzinga and Phaf3,Reference Dalenberg, Brand, Gleaves, Dorahy, Loewenstein and Cardeña18 Frontolimbic alterations are the most common neuroimaging findings in trauma-related disordersReference Pitman, Rasmusson, Koenen, Shin, Orr and Gilbertson19 and are consistent with theories of PTSD and DID in which midline frontal regions attempt to downregulate emotional arousal by overmodulating limbic structures.Reference Lanius, Vermetten, Loewenstein, Brand, Schmahl and Bremner20,Reference Reinders, Willemsen, den Boer, Vos, Veltman and Loewenstein21 Roydeva & Reinders’ reviewReference Roydeva and Reinders11 supported the involvement of frontal and limbic regions in pathological dissociation – specifically the dorsomedial and dorsolateral prefrontal cortex, superior frontal regions, anterior cingulate and basal ganglia – as functional biomarkers of pathological dissociation. Notably, they also highlighted the role of posterior association areas – specifically the precuneus – in pathological dissociation.
Studying clinical populations has been the standard approach to parsing out brain regions responsible for dissociation; however, this approach is inherently and inextricably confounded by the presence of other psychopathological symptoms and trauma exposure. As a result, researchers and clinicians should consider the possibility that brain regions identified in previous neuroimaging studies of pathological dissociation in traumatised samples have likely overrepresented the importance of frontal and limbic regions, at least in non-trauma-related, non-pathological dissociation. The trauma confound in previous imaging studies is particularly concerning, as some theorists suggest that trauma exposure is of limited importance even in pathological dissociation and call for a paradigm shift away from trauma-centric views in developing a full understanding of dissociation.Reference Giesbrecht, Lynn, Lilienfeld and Merckelbach2,Reference Giesbrecht, Lynn, Lilienfeld and Merckelbach22 Because trauma exposure is not aetiologically requiredReference Butler10 – nor even suspected in trait dissociation – we did not want to base the regions of interest in our current study on regions identified by previous trauma-related dissociation work. Consequently, we looked for neuroimaging research on non-pathological cognitive functions that overlap well with trait dissociation.
Daydreaming, mind-wandering and the default mode network
To that aim, Giesbrecht and colleaguesReference Giesbrecht, Lynn, Lilienfeld and Merckelbach2 reviewed cognitive processes in dissociation and found that fantasy proneness (including daydreaming), suggestibility and subtle cognitive failures such as a lapsed attention account for a significant proportion of the variance in dissociation. Butler described normative dissociation as a ‘forum for mental processing’,Reference Butler23 that is a passive, spontaneous absorptive experience, typically termed daydreaming, that occurs in the absence of environmentally cued cognitive demands. In her foundational article on normative dissociation, ButlerReference Butler10 noted that much of our stream of consciousness is filled with dissociative experiences such as daydreaming and fantasy involving a temporary separation from other mental processes. Therefore, considering constructs that have been operationally defined in previous neuroimaging research, we determined that trait dissociation shares notable commonalities with daydreaming, mind-wandering and undirected thought, all of which have been associated with default mode network (DMN) activation.Reference Christoff24,Reference Smallwood and Schooler25 The DMN is a network of brain regions with highly correlated mental activity when a person is awake but not engaged in task-focused work.Reference Fox, Snyder, Vincent, Corbetta, Van Essen and Raichle26,Reference Raichle and Snyder27 Past research reports enhanced dynamic DMN functional connectivity and activity during daydreaming and mind-wandering,Reference Fox, Spreng, Ellamil, Andrews-Hanna and Christoff28 and DMN connectivity was recently implicated as a potential predictor of trauma-related dissociation after controlling for psychological symptoms and trauma,Reference Lebois, Li, Baker, Wolff, Wang and Lambros29 which reinforced our selection of the DMN.
Study aims
To date, brain regions structurally related to the specific concept of trait dissociation in healthy people are unknown – and very little is known about brain regions involved in any type of dissociation in child and adolescent samples. Our study goal was to identify potential neurostructural correlates of non-pathological trait dissociation in healthy children. To this aim, we designed an exploratory volumetric study of all regions in the DMN, including the hippocampus. We controlled for age, gender, scanner site and, most importantly, trauma exposure. Trauma exposure was evaluated as a covariate of interest to examine its potential interaction with dissociation in this sample.
Method
Participants
Typically developing children aged 9 to 15 years were enrolled in our Developmental Chronnecto-Genomics (DevCoG)Reference Stephen, Solis, Janowich, Stern, Frenzel and Eastman30 study of healthy brain development after obtaining parental permission and consent and participant assent. Children completed psychological assessments and underwent structural magnetic resonance imaging (MRI) (n = 183). Three children were excluded because of unusable data, giving a final sample of n = 180. The sample was evenly distributed by gender, with 94 males and 86 females, by study site, with 89 at the University of Nebraska Medical Center (UNMC) and 91 at the Mind Research Network (MRN), and by age, with an average age of 11.97 years (s.d. = 1.73). Children were excluded from the study if parents reported that their child ever had a diagnosis of any psychiatric or behavioural disorder, a history of traumatic brain injury or other neurological condition, or the presence of metallic implants (e.g. orthodontia). The study was approved by both study sites’ institutional review boards (IRBs) and all research was conducted according to ethical principles including obtaining fully informed written parental consent and child assent. The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. All procedures involving human participants/patients were approved by the IRBs at the University of Nebraska Medical Center in Omaha, Nebraska, USA (UNMC IRB #503-15-EP) and at the Mind Research Network in Albuquerque, New Mexico, USA.
Psychological measures
The Trauma Symptom Checklist for Children (TSCC)Reference Briere31 is a self-report measure for children aged 8–16, with scores for five clinical scales, of which we used the TSCC dissociation scale. This 10-item self-report scale includes statements such as ‘Trying not to have any feelings’, ‘Pretending I'm somewhere else’, ‘My mind going empty or blank’ rated on a Likert scale from 0 (never) to 3 (almost all of the time). The Cronbach's alpha for the dissociation scale in this sample was very good, at 0.80. Providing evidence of convergent validity, the TSCC dissociation scale correlates highly in adolescent samples with the Adolescent Dissociative Experiences Scale (e.g. r = 0.79).Reference Sadowski and Friedrich32
We used a modified version of the UCLA Trauma History ProfileReference Steinberg, Brymer, Decker and Pynoos33 to assess the number of traumatic life events encountered by children in the study. Children answered ‘yes’ or ‘no’ to whether they had experienced each of 12 potentially traumatic events. We shortened the original 15 event measures to exclude items about sexual abuse or physical abuse that occurred specifically in the home, so that participation would be considered low risk by the IRBs. Both personally experiencing violence and witnessing violence to family members were still assessed. The items used in the current study were: having someone close to them die; being hit, punched or kicked very hard; seeing a family member hit, punched or kicked very hard; seeing or hearing about violence to a loved one; being a victim of community violence; being in a war; being in a disaster; being in a bad accident; having a painful or scary medical procedure; seeing a dead body not at a funeral; and having anything else very scary or upsetting happen.
Structural T1-weighted MRI
Structural T1-weighted MRI images were acquired using a Siemens 3-Tesla Skyra (at UNMC) or a Siemens 3-Tesla TRIO (at MRN), both with 32-channel head coils and closely calibrated sequences. A three-dimensional magnetisation-prepared rapid gradient-echo (3D MP-RAGE) sequence was used with the following parameters: repetition time TR = 2400 ms; echo time TE = 1.94 ms; flip angle 8°; field of view FOV = 256 mm; slice thickness 1 mm; base resolution 256; 192 slices; voxel size 1.0 × 1.0 × 1.0 mm. The T1-weighted structural brain images of all participants were processed using the Freesurfer software version 5.3 on a Linux Ubuntu platform (http://surfer.nmr.mgh.harvard.edu). Regional volumes were computed for the automatic cortical parcellation (aparc)Reference Desikan, Ségonne, Fischl, Quinn, Dickerson and Blacker34 and automatic subcortical segmentation (aseg)Reference Fischl, Salat, Busa, Albert, Dieterich and Haselgrove35 atlases in Freesurfer. We followed the ENIGMA protocol for quality assurance, which included performing visual checks of all cortical segmentations (http://enigma.usc.edu/protocols/imaging-protocols) and checking for motion, among other artifacts. Participants whose MRI images had large motion artifacts were excluded (n = 3). In addition, histograms of all regional values were computed for visual inspection. All volumes were normalised by dividing each regional volume by the total intracranial volume (TIV) per participant, to avoid the bias of head size in the volumetric measurements.Reference Whitwell, Crum, Watt and Fox36
Statistical analysis
The DMN regions of interest were: the caudal middle frontal, hippocampal, inferior parietal, isthmus cingulate, medial orbital frontal, parahippocampal, posterior cingulate, precuneus, and rostral anterior cingulate regions. For each of the nine DMN regions of interest, we conducted a univariate ANCOVA generalised linear model (GLM). Each of the models utilised the TIV-corrected volume averaged across the brain hemispheres for each structure of the DMN, which was entered as a dependent variable per model. TSCC dissociation score was the independent variable, and scanner site (UNMC or MRN), age, gender (male or female) and number of traumatic events experienced were entered as covariates. Full models were corrected using the Benjamini–Hochberg false discovery rate multiple comparison correction (denoted as BH in corrected p-values) as implemented in the p.adjust function in R version 1.2.5019 on a Windows 10 platform.
Results
TSCC dissociation scale scores in the full sample (n = 180) ranged from 0 to 19 and averaged 5.33 (s.d. = 4.02). Both the median and modal dissociation scores were 4.00, and the sample dissociation scores had acceptable skewness and kurtosis. The pathological cut-off scores for the TSCC dissociation scale varied slightly by age and gender but centred around a score of 15.Reference Briere31 Importantly, less than 4% of our sample scored above the pathological cut-off score, supporting the non-pathological nature of dissociation in our sample. The most strongly endorsed dissociation items were daydreaming, forgetfulness, my mind going empty or blank, and going away in my mind/trying not to think. Trauma exposure scores ranged from 0 to 7 (mean 2.17, s.d. = 1.81), with the most commonly endorsed traumas including the death of a loved one, the violent or serious injury of a loved one, and being a victim of physical violence. As expected, dissociation and trauma exposure scores were significantly correlated (r = 0.36, p < 0.001).
We conducted univariate ANCOVAs for each cortical structure of the DMN using the aparc atlasReference Desikan, Ségonne, Fischl, Quinn, Dickerson and Blacker34 (Fig. 1) and added the subcortical hippocampus defined by the aseg atlasReference Fischl, Salat, Busa, Albert, Dieterich and Haselgrove35 for completeness. Levene's test of equality showed no significant differences in error variance in any model (p = 0.200–0.798). Significant effects were found in the precuneus (F 5,174 = 4.83, p BH = 0.003, R2 = 0.12) and inferior parietal lobes (F 5,174 = 3.98, p BH = 0.008, R2 = 0.10), and these results survived multiple comparison correction.
Fig. 1 Cortical default mode network regions included in this study and labelled by the (aparc) atlas. Note that we also included the hippocampus, not shown in this figure.
In the precuneus, dissociation significantly predicted TIV-corrected volumes (F 1,174 = 3.05, p BH = 0.002) above and beyond the covariates in the model, such that greater volumes were found in those with higher dissociation values (Table 1). Age was a significant predictor in this model, such that older age was associated with smaller TIV-corrected volumes, but no other covariate significantly predicted precuneus volumes. In the inferior parietal region, trauma but not dissociation significantly predicted TIV-corrected volumes (F 1,174 = 5.96, p BH = 0.008), such that greater numbers of traumatic events were associated with decreased volumes (Table 1). Age was also a significant predictor in this model, such that as age increased, volume decreased. The models examining the effects in caudal middle frontal (F 5,174 = 1.07, p BH = 0.380), hippocampus (F 5,174 = 2.81, p BH = 0.055), isthmus cingulate (F 5,174 = 1.09, p BH = 0.380), medial orbital frontal (F 5,174 = 1.89, p BH = 0.177), parahippocampal gyrus (F 5,174 = 2.18, p BH = 0.131), posterior cingulate (F 5,174 = 1.41, p BH = 0.335) and rostral anterior cingulate regions (F 5,174 = 1.25, p BH = 0.373) were not significant even before multiple comparison correction.
Table 1 ANCOVA results for precuneus and inferior parietal regions of the DMN
Bold denotes significant results at p < 0.01.
Discussion
To the best of our knowledge, this is the first structural MRI study of brain regions associated with non-pathological dissociation in healthy children. Our most important finding is that the precuneus was larger in children with higher levels of trait dissociation and that volumes in this region were not significantly related to trauma. We also found that the inferior parietal region was smaller in healthy children who had experienced more traumatic events, but this region was not associated with trait dissociation. Research on trait dissociation in healthy people is lacking; however, a meta-analysis of 24 functional neuroimaging studies of the relatively similar concept of mind-wanderingReference Fox, Spreng, Ellamil, Andrews-Hanna and Christoff28 identified the importance of the precuneus/posterior cingulate cortex during this mental state. Similarly, our results are bolstered by two reviews of neuroimaging studies of pathological dissociation. Roydeva & ReindersReference Roydeva and Reinders11 concluded that posterior association areas were functionally relevant in pathological dissociation, and specifically called for more research on the precuneus. In a review of pathological dissociation in borderline personality disorder, Krause-Utz et alReference Krause-Utz, Frost, Winter and Elzinga37 explicitly suggested the importance of the precuneus owing to its role in self-referential processing. Known functions of the precuneusReference Fransson and Marrelec38 are consistent with the phenomenological experience of trait dissociation, including absorption in one's internal world and alterations in one's experience of self or others,Reference Butler23 so finding larger precunei in the current study is intriguing.
Functionally, the precuneus is known to be involved in episodic memory retrieval, mental imagery, self-referential processing tasks, perspective taking and consciousness.Reference Cavanna and Trimble39 Interestingly, a study comparing individuals with DID with actors simulating DID found higher resting-state metabolism in regions of the DMN, including the precuneus, in those with DID, suggesting that they were more involved in self-referential thought than the actors during rest.Reference Schlumpf, Reinders, Nijenhuis, Luechinger, van Osch and Jäncke40 The inferior parietal region is an important association area typically involved in internal sensory processingReference Igelström and Graziano41 and it is also active during rest, especially during self-referential thought, along with the precuneus.Reference Davey, Pujol and Harrison42 Nardo and colleaguesReference Nardo, Högberg, Lanius, Jacobsson, Jonsson and Hällström43 studied dissociation in a traumatised sample and controlled for the effects of psychological symptoms and trauma exposure. Contrary to our results, which found no non-pathological dissociation effect and decreased volumes with trauma exposure in the inferior parietal region, they found that both pathological and trait dissociation were associated with volumetric increases in this region.
Although negative results should be discussed with great caution, we believe it is important to note that the current study did not find any significant volumetric differences in the examined frontal,Reference Nardo, Högberg, Lanius, Jacobsson, Jonsson and Hällström43–Reference Ehling, Nijenhuis and Krikke45 hippocampalReference Chalavi, Vissia, Giesen, Nijenhuis, Draijer and Cole46,Reference Badura-Brack, Mills, Embury, Khanna, Klanecky Earl and Stephen47 or parahippocampalReference Meng, Qiu, Zhu, Lama, Lui and Gong44,Reference Badura-Brack, Mills, Embury, Khanna, Klanecky Earl and Stephen47 regions noted in previous trauma research. Interestingly, a study found that reduced hippocampal volume was related to both severity of dissociative symptoms and trauma exposure in people with PTSD and DID (who also met criteria for PTSD);Reference Chalavi, Vissia, Giesen, Nijenhuis, Draijer and Cole46 however, a rare study of individuals with dissociative disorders who did not meet criteria for PTSD did not find reduced hippocampal volume.Reference Weniger, Lange, Sachsse and Irle48 Perhaps structural findings related to diminished medial temporal and increased frontal volumes become apparent over the course of disorder development, or perhaps these regions are not implicated in non-pathological trait dissociation. These questions are clearly a matter for future research. For now, our absence of frontal and medial temporal findings – an absence noted even before multiple comparison correction – clearly separates our findings on trait dissociation from most work on pathological dissociation related to trauma. Although we are careful in drawing conclusions from negative findings, our results clearly call for future imaging research of dissociation in psychologically healthy individuals to avoid the trauma confound and isolate structural and functional origins of the process of normative dissociation.
In identifying some – but not unmitigated – overlap between brain areas implicated in pathological and non-pathological dissociation, and given the subtle cognitive errors noted in trait dissociation, our findings align with Loewenstein'sReference Loewenstein49 suggestion that studying dissociation may address puzzling gaps in psychology and neuroscience. These gaps are relevant for understanding not only cognitive function in general, but also pathological disorders because research suggests that mild cognitive impairments may pose a potential risk for PTSD or dissociative disorder in healthy people with high dissociation.Reference Amrhein, Hengmith, Maragkos and Hennig-Fast5 Such risks are consistent with previous research associating alterations in the DMN with psychopathology in general,Reference Andrews-Hanna, Smallwood and Spreng50 and specifically structural variations in the precuneus with subclinical symptoms of clinical disorders.Reference Besteher, Gaser and Nenadić51
Limitations and future research
Despite the novel contribution of the current study, it has limitations. The exploratory research utilised structural MRIs in healthy children. By design, our study did not include a sample of children diagnosed with dissociative disorders. Although such a sample would certainly be smaller, replicating this study in children with dissociative disorders would improve understanding of potential structural alterations related to pathological versus non-pathological dissociation. Future neurofunctional research should include blood oxygen level-dependent (BOLD) or arterial spin labelling (ASL) perfusion or magnetencephalography resting-state studies and functional assessments specifically targeting the precuneus in healthy child and adult samples and pathological samples. Finally, our analyses are cross-sectional, so future work should examine how longitudinal changes in dissociation correspond with changes in brain structure and function. Longitudinal follow-up should also assess whether trait dissociation relates to risk for psychopathology in the current sample. Such future work would allow us to evaluate the extent to which normative dissociation is a risk or protective factor during development.
Implications
We hope our findings on non-pathological trait dissociation in children may inform brain mapping research and also inform research on transdiagnostic symptoms of pathological dissociation, independent of psychiatric diagnoses and trauma exposure. We believe the key implications of this study are the identification of a previously unknown psychological function of the precuneus and the suggestion of this structure as a promising target for future neuropsychological and psychopathological research in healthy and psychopathological groups.
Data availability
The data used in this article are openly available through the COINS framework (https://coins.trendscenter.org/): see data-set COINS:Dev-CoG.
Author contributions
A.S.B.B., J.S., Y.-P.W., V.C. and T.W.W. designed the study. C.M.E., G.P., M.F., J.S. and T.W.W. were involved in data acquisition. A.S.B.B., M.M., C.M.E., G.P. and T.W.W. were involved in data analysis. A.S.B.B., M.M., C.M.E. and A.K.E. were involved in data interpretation. A.S.B.B. and M.M. wrote the main draft of the paper. C.M.E., G.P., M.F., A.K.E., J.S., Y.-P.W., V.C. and T.W.W. revised the paper for important intellectual content. All authors approved the final version and agree to be accountable for the work.
Funding
This work was supported by the National Science Foundation of the USA (#1539067 and 2112455), the National Institutes of Health (R01-MH121101, R01-MH116782, P20-GM144641, R01-EB020407, R01-MH118695 and R56-MH124925) and At Ease, USA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Declaration of interest
None.
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