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. Author manuscript; available in PMC: 2016 Feb 10.
Published in final edited form as: Neuropsychology. 2015 Apr 20;29(4):543–549. doi: 10.1037/neu0000198

Alterations in autobiographical memory for a blast event in OEF/OIF veterans with mild TBI

DJ Palombo 1,3, HS Kapson 1,4, G Lafleche 1,3, JJ Vasterling 2,3, BP Marx 2,3, M Franz 1, M Verfaellie 1,3
PMCID: PMC4748832  NIHMSID: NIHMS749126  PMID: 25893970

Abstract

Objective

Although loss of consciousness associated with moderate or severe traumatic brain injury (TBI) is thought to interfere with encoding of the TBI event, little is known about the effects of mild TBI (mTBI), which typically involves only transient disruption in consciousness.

Method

Blast-exposed Afghanistan and Iraq War veterans were asked to recall the blast event. Participants were stratified based on whether the blast was associated with probable mTBI (n=50) or not (n =25). Narratives were scored for organizational structure (i.e., coherence) using the Narrative Coherence Coding Scheme (Reese et al., 2011) and episodic recollection using the Autobiographical Interview coding procedures (Levine et al., 2002).

Results

The mTBI group produced narratives that were less coherent but contained more episodic details than those of the no-TBI group.

Conclusions

These results suggest that mTBI interferes with the organizational quality of memory in a manner that is independent of episodic detail generation.

Keywords: mild traumatic brain injury, autobiographical memory, coherence

Introduction

Increased use of improvised explosive devices in contemporary warfare has significantly enhanced the risk of traumatic brain injury (TBI) among military personnel, especially mild TBI (mTBI). MTBI is associated with at least transient disruption of brain functioning at the time of the event, manifested by alteration or loss of consciousness (LOC) up to 30 minutes and loss of memory for events immediately before or after the injury, with posttraumatic amnesia (PTA; i.e., a persistent difficulty in remembering events occurring immediately after the injury) no longer than 24 hours (Ruff, 2005). During the acute phase of injury, cognitive impairment is commonly observed in mTBI (Eskridge et al., 2013; McCrea, 2001; McCrea, Kelly, Randolph, Cisler, & Berger, 2002), which includes reduced memory for the injury event itself (Eskridge et al., 2013). Although most cognitive deficits do not endure in the majority of people who have suffered an mTBI, (e.g., McCrea, 2001; McCrea et al., 2002; but see e.g., Pertab, James, & Bigler, 2009; Pontifex, O'Connor, Broglio, & Hillman, 2009), it is unknown whether difficulties in memory for the injury event persist. A persistent deficit in memory might be expected, however, to the extent that this impairment reflects impoverished encoding of the injury event.

By definition, encoding of the event would not take place during LOC, which is typically observed in moderate to severe TBI (Malec et al., 2007). Yet, because mTBI is commonly associated with only transient and incomplete disruptions in consciousness, complete amnesia for the event would be less likely as compared with more severe TBI. Instead, it is possible that mTBI-related alterations in consciousness, including confusion and disorientation, during the event, even if transient, may degrade encoding of the injury event, resulting in partial or fragmented subsequent recall of the event. For example, Creamer, O’Donnell, and Pattison (2005) found that the majority (82%) of mTBI patients presenting to a Level I trauma center reported incomplete memory for the event eight days post-injury. However, this study relied on subjective patient estimations of the amount of information they would be able to recall. Such metamemorial judgments are subject to decision biases and do not necessarily reflect the availability of the memory per se (e.g., Dougal & Rotello, 2007).

Both the overall TBI and mTBI literatures currently lack studies examining objective indices of memory for the injury event. Such an approach requires quantitative analysis of specific autobiographical features of the memory, such as level of episodic detail or degree of coherence (Levine, Svoboda, Hay, Winocur, & Moscovitch, 2002; Reese et al., 2011). The integrity of a patient’s recall of the mTBI event may hold relevance to accurate TBI diagnosis and prognosis, particularly for unwitnessed events, as injury characteristics (e.g., PTA) often serve as markers of TBI severity and persistent neural abnormalities (Collins et al., 2003; Jorge et al., 2012). The integrity of memory for the event may also be relevant to development of psychiatric co-morbidities, particularly posttraumatic stress disorder (PTSD), which has known associations with autobiographical memory abnormalities (see Verfaellie & Vasterling, 2009).

In the present study, we examined the characteristics of autobiographical memory for a blast event in Operation Enduring Freedom and Operation Iraqi Freedom (OEF/OIF) veterans stratified by whether or not they sustained a mTBI as a result of the blast exposure. More specifically, we evaluated recall of blast events for distinct dimensions of autobiographical retrieval quality: organizational structure (i.e., how coherent and integrated the memory is) and episodic recollection (i.e., number of details describing the event). Assuming that mTBI would interfere with the episodic quality and organizational structure of memory, we predicted that narratives of the blast event produced by participants with an associated mTBI would be significantly less coherent and less detailed relative to those of participants without an associated mTBI.

Methods

Participants

Participants included 75 OEF/OIF deployed veterans who self-reported exposure to a blast within 100 m during deployment and who were recruited through the VA Boston Healthcare System Polytrauma Network, flyers and outreach community events. Individuals were stratified based on whether they suffered a mTBI (n=50) or not (n=25) due to a blast exposure (see Methods). Participants were part of a larger research study involving neuropsychological testing, diagnostic interviews, and self-report questionnaires (see Verfaellie, Lafleche, Spiro, Tun, & Bousquet, 2013). Exclusion criteria for the larger study (see Verfaellie et al., 2013) included history of psychosis or neurological diagnosis except mTBI. Participants were also excluded if they demonstrated questionable effort (i.e., below 45 on the retention trial of the Test of Memory Malingering; Tombaugh, 1996). Neuropsychological data for the larger study is reported elsewhere, demonstrating no mTBI-related deficits on a battery of neuropsychological tests (Verfaellie, Lafleche, Spiro, & Bousquet, 2014). Participants provided written informed consent in accordance with the Institutional Review Board at the VA Boston Healthcare System.

Materials and Procedure

TBI Interview

Evaluation of TBI was based on an extensive semi-structured interview performed by a clinical neuropsychologist, which queried the nature of participants’ blast exposure(s) (see Verfaellie et al., 2013). During this interview, participants were first probed about the three most significant deployment-related blast events they had experienced. Next, participants described the most severe blast event in detail, including the events occurring prior to, during, and immediately following the blast. Participants were also asked to describe any neurological symptoms they may have experienced immediately after the event and any medical examination or witness reports that may have occurred. For all parts of the interview, a structured list of probing questions was prescribed, although the order of these prompts varied depending on the context of participants’ responses. As one of the goals of this interview was to establish a complete autobiographical narrative of the blast experience (see below), the experimenter used additional prompts, as needed, to establish the complete “story.”

Although the narratives were obtained for reasons other than examination of autobiographical memory features, our interview procedures were akin to other semi-structured interviews used in the autobiographical memory literature (e.g., Levine et al., 2002). Two investigators evaluated the transcribed interview and stratified participants into mTBI (n=50)1 and no-TBI subgroups (n=25) based on the definition of mTBI provided by the American Congress of Rehabilitation Medicine (1993), which requires at least one of the following: (a) a LOC less than 30 min; (b) a period of PTA not greater than 24 h; or (c) alteration of mental status at the time of the injury. LOC and PTA severity were rated on a scale of 0-4 and 0-5, respectively, with a higher score corresponding to more severe LOC or PTA.

Autobiographical Memory

To assess autobiographical memory for the blast event, narratives were obtained from the portion of the clinical interview during which participants described the most severe blast event in detail. Autobiographical details were analyzed for the full description of the index event, whereas coherence analyses were applied only to the single paragraph that provided the most detail about the index event without being interrupted by the interviewer. The coherence paragraphs typically occurred towards the beginning of the narrative.

PTSD and Combat Exposure

Because mTBI is highly comorbid with PTSD, which has known associations with autobiographical memory abnormalities (see Verfaellie & Vasterling, 2009) we accounted for PTSD symptomatology in all of our analyses. Participants were administered the Clinician Administered PTSD Scale (CAPS) for the Diagnostic and Statistical Manual of the Mental Disorders 4th Edition (DSM-IV-TR; Blake et al., 1995), to obtain information about PTSD symptoms and diagnostic status. Continuous CAPS scores were used as a measure of PTSD severity. Participants were also administered the mood disorders module of the Structured Clinical Interview for the DSM-IV-TR (First, Spitzer, Gibbon, & Williams, 2002) to determine current major depressive disorder (MDD) diagnostic status. Participants also completed the Combat Experiences Scale (CES) of the Deployment Risk and Resilience Inventory (DRRI; two participants did not complete the CES), a self-report scale that assesses exposure to combat-related events, such as being fired on or exposed to an attack (King, King, Vogt, Knight, & Samper, 2006).

Narrative Coding

Organizational structure (coherence)

To assess the coherence of narratives, the Narrative Coherence Coding Scheme (NACCs) was used (Reese et al., 2011). The NACCs has three components: context (the narrator places the event in space and time), temporal ordering (the narrator relates components of the event along a timeline), and theme (the narrator develops and elaborates on the topic and makes interpretations and/or causal linkages to other experiences). These components are each rated on a scale from 0-3, with a higher score corresponding to a more coherent narrative.

Autobiographical details

To assess the number of autobiographical details retrieved, the narratives were segmented into informational bits and classified as “internal” or “external”, as per the Autobiographical Interview (Levine et al., 2002). Internal details pertained to the main event described, were specific to time and place, and conveyed a sense of episodic re-experiencing. Internal details were subdivided into categories: (1) event (happenings), (2) place (locations), (3) time (temporal information), (4) perceptual (sensory details), and (5) thought (emotional states). External details did not pertain to the main event, including (1) semantic information (facts, extended events) and (2) other details unrelated to the main event (repetitions, metacognitions, or editorials). The number of prompts provided by the experimenter for each narrative was also tallied.

Training and reliability of raters

Prior to coding narratives, two raters used an excerpt from Life of Pi by Yann Martel for reliability training. Next, these raters practiced coding narratives from veterans who were not included in the study sample. Once agreement between the two raters was achieved, the raters coded the narratives from the present sample. These raters were not involved in mTBI diagnosis and were blind to group membership. Interrater reliability was established on the basis of approximately 20% of the sampled narratives. Intraclass correlation analysis (Cronbach’s α) indicated high agreement for each autobiographical detail type (range=.90-.99). Relatively lower agreement for coherence subtypes (range=.66-.83) likely reflected the limited range of the coherence scale (0-3).

Statistical Analyses

Group differences in demographic, clinical, and injury characteristics were examined with chi-square tests (χ2) for categorical data and independent samples t-tests for continuous data, with corrections for equality of variance violation performed when necessary.

To examine whether groups differed in aspects of autobiographical memory, a series of repeated measures analysis of covariance (ANCOVA) were conducted. A correction for violation of sphericity was applied when necessary. A log transformation was used to reduce the skewness of the data. Coherence was examined with a mixed-design ANCOVA, with factors of group and coherence dimension (context, temporal ordering, theme), adjusting for CAPS and CES summary scores. Number of autobiographical details was examined with two models, both adjusted for CAPS and CES summary scores, and number of examiner prompts: (1) the first included factors of group and internal detail type (event, place, time, perceptual, thought); (2) the second included factors of group and external detail type (semantic, other). As appropriate, follow-up univariate analyses examined group differences at each level of the dependent variable, adjusted for all other variables in the model. Alpha was set at .05 for all analyses.

To explore associations between autobiographical memory characteristics (coherence scales and internal detail types; dependent variables) and clinical features of mTBI (LOC and PTA; independent variables), we used multiple linear regression. All regression models were adjusted for CAPS and CES summary scores and models involving autobiographical detail types were additionally adjusted for number of examiner prompts.

Results

Demographic, clinical and injury characteristics of the study sample are summarized in Table 1. Groups did not significantly differ in age, education, or injury characteristics (ps ≥ .53), including the number of prior blast exposures, time elapsed since the blast event, or number of pre-deployment mTBIs. The proportion of participants with a diagnosis of MDD did not differ across groups (p=.45). By contrast, there was a trend towards higher prevalence of PTSD diagnosis (χ2=4.76, p=.054) and higher CAPS summary scores (t73=1.77, p=.08, 95% CI [−1.36, 23.40], d = .43) in the mTBI group relative to the no mTBI group. Combat severity (i.e., CES summary scores) was also higher in the mTBI group relative to the no-TBI group (t71=4.75, p<.001, 95% CI [1.80,4.42], d=1.12).

Table 1.

Clinical and demographic characteristics of the sample.

mTBI (n=50) No TBI (n=25)
Age, M (SD) 29.3 (7.6) 30 (6.4)
Males, no. (%) 48 (96%) 23 (92%)
Education, M (SD) 13.1 (2.1) 13.4 (2.1)
CAPS total, M (SD) 63.9 (25.3)# 52.9 (25.5)
CES, M (SD) 11.2 (2.4)* 8.1 (3.1)
Months post-blast, M (SD) 47.8 (26.7) 47.2 (32.4)
Pre-deployment mTBI, no. (%) 8 (16%) 6 (24%)
PTSD, no. (%) 40 (80%)# 14 (56%)
Major depressive disorder, no. (%) 19 (38%) 7 (28%)
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Notes: Group differences were assessed with independent samples t test and post-hoc tests.

#

p<.10,

*

p<.05.

Abbreviations: MTBI, mild traumatic brain injury; CAPS, Clinician-Administered PTSD Scale for DSM-4; CES, Combat Experience Scale.

Organizational structure (coherence)

The paragraphs used in the coherence analysis averaged 191 words (SD=214, range=16-1444). The mTBI group produced significantly less coherent narratives than the no-TBI group after accounting for covariates (i.e., CAPS and CES summary scores; F1, 69=4.75 p=.03, η2=.06; Figure 1a). Although the interaction between group and scale type was not significant (p=.15, η2=.03), follow up analyses revealed that the group effect was driven primarily by differences in thematic coherence (F1, 69=10.54, p=.002, η2=.13), with no significant group differences observed for either context (p=.28, η2=.02) or temporal ordering (p=.36, η2=.01). There were no significant associations observed between coherence measures and CAPS or CES summary scores. As groups did not significantly differ in the number of words contained within the paragraph selected for coherence analyses (p=.73, 95% CI [−87.12, 123.04], d=.09), reduced coherence in mTBI relative to no mTBI cannot be accounted for by group differences in number of words generated. There were no significant associations between LOC or PTA and coherence scales.

Figure 1.

Figure 1

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(a) Mean coherence ratings and (b) mean number of episodic details recalled for individuals with and without a mild traumatic brain injury (mTBI), adjusted for covariates (see methods). Error bars indicate standard error of the mean.

Autobiographical details

The narratives used in the analysis of episodic details averaged 1141 words (SD=735, range=223-3611). The number of experimenter-provided prompts was higher in the mTBI group relative to the no-TBI group (t73=4.26, p<.001, 95% CI [7.05, 19.43], d=1.08). Contrary to our hypothesis, the mTBI group produced significantly more internal details than the no-TBI group, even after accounting for all covariates (i.e., CAPS and CES summary scores, experimental cueing; F1, 68=4.02, p=.049, η2=.06), and there was no significant interaction between group and detail type (p=.79, η2=.006, Huynh-Feldt corrected; Figure 1b). In accordance with greater detail generation in mTBI, the mTBI group also produced significantly longer narratives, as indicated by a higher number of words generated, an effect that was significant even when accounting for experimenter cueing (F1, 72=5.33, p=.02, η2=.07).

For external details, there was no significant main effect of group (p=.51, η2=.006) or group by detail type interaction (p=.55, η2=.005).

Linear regression revealed that the duration of LOC (β=− .11, p=.03), but not PTA (p=.22), was inversely related to the number of perceptual details produced. No other significant associations were observed with remaining internal detail types.

Discussion

We investigated the integrity of autobiographical memory for the event leading to a mild brain injury in blast-exposed OEF/OIF veterans. There were two main findings. First, as expected, blast event narratives produced by individuals with mTBI were less organized than those produced by individuals who did not experience TBI as a result of the blast. Group differences in coherence were driven primarily by differences in how coherently thematic elements of the narrative were constructed, suggesting that the narratives of mTBI participants contained fewer elaborations, evaluations, interpretations, and/or causal linkages that would aid in maintaining topicality of the narrative. This finding remained significant after accounting for PTSD severity, suggesting that mTBI was independently associated with the quality of autobiographical memory. Second, contrary to expectation, participants who experienced a blast-related mTBI produced more, not fewer, internal (episodic) details than those whose blast exposures did not lead to TBI, even after accounting for PTSD. As such, reduced coherence in mTBI cannot be accounted for by a dearth of episodic details.

The relatively reduced coherence in blast narratives is consistent with the hypothesis that transient symptoms of mTBI experienced at the time of blast exposure (i.e., transient LOC, confusion, or disorientation) disrupt the encoding or integration of memories (Bryant et al., 2009; Vasterling, Verfaellie, & Sullivan, 2009). Elevated recall of episodic details for the blast event in participants with associated mTBI may seem hard to reconcile with this interpretation. However, we speculate that this elevation could be attributable to the blast event carrying greater personal significance for those with associated mTBI because of the emotional relevance of incurring greater clinical symptomology in association with the blast event and subsequent diagnosis of mTBI. Although we did not query the importance of the blast event to participants, previous research has shown that negative events that are more personally relevant are better remembered (Sharot, Martorella, Delgado, & Phelps, 2007). As such, degree of personal relevance is an important consideration in future research investigating autobiographical recall of TBI events.

Within the mTBI group, however, exploratory post-hoc analyses indicated that the duration of LOC (but not PTA) was inversely related to the number of internal details, a finding that supports the interpretation that some features of mTBI may disrupt encoding of the blast event. Notably, this effect was specific to perceptual details; other categories (i.e., place, time, event, thought) showed no such relationship with LOC. It can be speculated that, whereas non-perceptual detail categories can more readily be bolstered by details constructed after the event has occurred, perceptual details (e.g., sounds, objects, pain) are more difficult to reconstruct. As such, they may be more closely tied to the original encoding experience, thus demonstrating greater sensitivity to injury characteristics such as LOC.

Although mTBI was associated with lower coherence, a significant relationship was not observed between coherence and either duration of LOC or PTA. The limited range of the coherence scale (0-3) may have obscured such an association. Alternatively, it may be that the generation of event details and the organization of those details into a coherent memory rely on distinct cognitive processes (Race, Keane, & Verfaellie, 2014). Whereas the generation of event details in mTBI may be constrained by the quality of encoding, the organization of the memory may be related to post-encoding processes that are affected by mTBI in the acute or even post-acute stage. In the aftermath of LOC and PTA, residual cognitive deficits, such as weakened top-down cognitive control (i.e. executive processes involved in mnemonic consolidation or integration), may interfere with the organizational structure of this event (Conway & Pleydell-Pearce, 2000). Still, it is also possible that the coherence deficit observed in the mTBI group reflects a persistent deficit in retrieval output. Some evidence suggests that mTBI is associated with enduring anatomical abnormalities, including those involving white matter tracts coursing through frontal and medial temporal lobe structures (e.g., Morey et al., 2013; Yallampalli et al., 2013) that may be involved in narrative coherence (Mar, 2004; Race et al., 2014). Arguing against persistent cognitive impairment as an explanation for our coherence findings, a related study using an overlapping but larger sample failed to detect enduring cognitive differences between participants with and without a mTBI on clinical neuropsychological tests thought to be sensitive to prefrontal and medial temporal damage (Verfaellie et al., 2014).

To help tease apart the cognitive mechanisms (i.e., encoding, consolidation, retrieval) underlying reduced coherence in mTBI, future research is necessary to determine whether mTBI also degrades the coherence of other autobiographical memories involving non-injurious events, particularly for events occurring in close temporal proximity to the injury event. If, for example, individuals with mTBI also showed reduced coherence for events occurring shortly after the index event, it would confirm that the observed reduction is not attributable to cognitive inefficiencies in encoding that take place at the time of injury (e.g., due to LOC). Moreover, examining the integrity of autobiographical memory more broadly may illuminate how mTBI affects the generation of autobiographical details for experiences that are less salient than the one sampled here. Some studies have demonstrated more pervasive autobiographical memory deficits in moderate to severe TBI (Piolino et al., 2007; Rasmussen & Berntsen, 2014), but little is known about autobiographical memory in mTBI.

Future efforts would also benefit from inclusion of techniques to quantify additional autobiographical memory features. Our analysis of coherence was based on qualitative rating scales that are applied to multiple clauses or an entire body of text, thus providing a global measure of coherence (Reese et al., 2011). These categories are conceptually broad, thereby making it difficult to ascertain whether the deficits in thematic coherence observed in the mTBI group are due to difficulty in topic development, elaboration, or making causal linkages to personal identity –all of which are subsumed under the theme category. Additional techniques for assessing other aspects of coherence at a microanalytic level (Foa, Molnar, & Cashman, 1995) may be useful for clarifying this issue.

Despite outstanding questions regarding the exact nature of the alterations in autobiographical memory in mTBI, our findings have clinical relevance. First, given the widespread reliance on self-reported description of the injury event in making deployment-related mTBI diagnoses, the finding that mTBI disrupts only the coherence but not the content of the injury memory, suggests that diagnosis of mTBI is not hampered by a paucity of informational detail. Second, the observation that mTBI disrupts the coherence of the injury event may be relevant to understanding the interplay between mTBI and PTSD. Several studies have reported that the prevalence of PTSD is higher among injury survivors with mTBI relative to those without mTBI (e.g., Bryant et al., 2009; Creamer et al., 2005; Hoge et al., 2008), a trend observed in the present study. Some conceptualizations of PTSD (Brewin, 2001; Ehlers & Clark, 2000) hold that intrusive, involuntary memories of the traumatic event arise in PTSD from deficient encoding and integration of the event into a verbally accessible narrative. If degraded encoding of psychologically-traumatic events does increase risk of PTSD, the prevalence of PTSD among warzone veterans with mTBI may in part reflect acutely disrupted cognitive processes, which interfere with the organizational structure (i.e., coherence) of brain injury events that are also psychologically traumatic (Vasterling et al., 2009). Indeed, there is some empirical support that traumatic memories in PTSD are fragmented and less coherent relative to those experienced by individuals without PTSD (e.g., Foa et al., 1995; Jelinek, Randjbar, Seifert, Kellner, & Moritz, 2009). However, other studies have failed to demonstrate reduced coherence in PTSD (e.g., Berntsen & Rubin, 2014; Rubin, 2011). Moreover, given that the narrative in the present study was not the Criterion A trauma event for the majority of participants, our findings cannot directly inform this issue.

Our study has several limitations. First, in contrast to controlled laboratory-studies, it was not possible to verify the accuracy of the reported memories. Autobiographical memories are susceptible to distortions over time (Schmolck, Buffalo, & Squire, 2000), especially with repeated retrieval (Nadel, Campbell, & Ryan, 2007), which may have occurred to a greater extent in the mTBI group. Although it would have been informative to probe the frequency of rehearsal of the injury event, solicitation of this information would involve self-report, which is also susceptible to distortion. Similarly, mTBI determination was based on self-report (using a guided interview) due to limited documentation at the time of injury. Although retrospective self-report of injury is currently standard in mTBI (Corrigan & Bogner, 2007) and is especially common in report of combat injuries for which real-time documentation can be challenging, the absence of medical reports or eye witness accounts does not permit us to validate the accuracy of the memory.

In spite of these limitations, this study is the first detailed assessment of autobiographical memory features for an event leading to mTBI. Our findings suggest that mTBI interferes with some aspects of autobiographical memory, in part, due to cognitive processes taking place during encoding, and possibly due to alterations in post-encoding processes. As such, this type of research may lay the groundwork for helping to elucidate the cognitive mechanisms associated with mTBI.

Acknowledgements

This research was supported by VA RR&D grant #IO1RX000216 awarded to M.V. D.J.P is supported by the Canadian Institutes of Health Research. The authors thank Meredith Charney, Keely Burke, Elizabeth Race and Matthew Grilli.

Footnotes

1

The mTBI group was initially further subdivided into participants based on LOC status (mTBI + no LOC, n=25; mTBI + LOC, n=25), however, because these sub-groups performed very similarly, they were collapsed.

The authors declare no conflicts of interest.

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