Enhanced mismatch negativity in adolescents with posttraumatic stress disorder (PTSD)

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Abstract

The mismatch negativity (MMN) is observed following rare or unique sensory events, and reflects pre-attentional sensory processing of unexpected stimuli. The MMN is altered in several mental illnesses, including post-traumatic stress disorder (PTSD), but did not yield consistent results. We measured MMN in 27 survivors of the Wenchuan earthquake, including 13 who were diagnosed with PTSD, to determine if pre-attentive processing in the auditory cortex was altered by this disease. The amplitude of MMN was significantly greater in the PTSD group compared to the control group. In contrast, no significant group difference was found in the N1 potential, an event-related potential that reflects cortical transmission of sensory information. These results demonstrated an increased sensitivity to deviant stimuli in PTSD that may reflect a chronic state of hyperarousal and hypervigilance in trauma victims.

Research Highlights

► The amplitude of MMN was significantly greater in the PTSD group. ► These results implied an increased sensitivity to deviant stimuli in PTSD victims. ► A chronic state of hyperarousal and hypervigilance sensitizes trauma victims to changes.

Introduction

Mismatch negativity (MMN), a component of the event-related potential (ERP) evoked by rare changes or “deviants” aimed repetitive sensory stimuli, was first described over 30 years ago (Näätänen et al., 1978). The MMN is studied extensively in cognitive and clinical neuroscience because it is believed to reflect a pre-attentive cortical processing that is largely independent of conscious awareness or rehearsal. It can even be recorded in the absence of focus attention or specific task instruction, which makes it particularly suitable for clinical populations (Näätänen, 2003). For example, MMN has been used to study the information processing in patients with dyslexia (Schulte-Körne et al., 2001), schizophrenia (Baldeweg et al., 2004, Michie, 2001, Shelley et al., 1991) and depression (Kähkönen et al., 2005, Ogura et al., 1993).

MMN has been also used to explore the pre-attentive processing in patients with posttraumatic stress disorder (PTSD). Most individuals with PTSD are characterized by persistent reexperiencing of the traumatic event, persistent avoidance of stimuli associated with the trauma, and chronic hyperarousal (DSM-IV, American Psychiatric Association, 1994). Previous studies provided evidence for alterations in information processing in individuals with PTSD, but some results and conclusions have been contradictory. Morgan and Grillon (1999) found that the amplitude of the MMN, evoked in an auditory frequency discrimination task, was significantly greater in a PTSD group of sexual assault survivors than in a control group. It was concluded that there were abnormalities in the preconscious auditory sensory memory in PTSD subjects that manifested as increased sensitivity to stimulus changes. In contrast, a reduced MMN was demonstrated in PTSD patients when the discrimination involved sound duration or sound gaps, but not when the deviant stimuli differed in frequency (Menning et al., 2008). A reduction in pre-attentive auditory sensory memory in PTSD was proposed, possibly due to hyperarousal and impaired concentration.

The main difference between these two studies was the paradigm employed. Morgan and Grillon (1999) used the traditional paradigm (Näätänen et al., 1982) that employs just one kind of deviant stimulus imbedded in one kind of repeating standard stimulus. Menning et al. (2008) used an optimal paradigm, in which five kinds of deviants, varying in frequency, intensity, direction, gab and duration, could be manipulated within the same experiment (Näätänen et al., 2004). Both paradigms have limitations. The more complex optimal paradigm may engage additional or entirely different processing mechanisms. The utility of the traditional MMN paradigm has also been challenged because that refractoriness of organized cortical neurons was not excluded in this paradigm (Jacobsen and Schröger, 2001). Moreover, the effect of deviance on ERP characteristics in the traditional paradigm was mainly due to an effect on the N1 amplitude (Horvath et al., 2008). These conflicting data suggest two alternative explanations for MMN. The sensorial view states that MMN is caused by refractoriness of frequency-specific afferent cortical neurons, while the cognitive view implicates a mismatch between the sensory input of the deviant tone and a sensory memory trace for the frequently presented standard tone (Maess et al., 2007).

In order to exclude the effect of refractoriness and to measure the genuine memory comparison-based MMN, a controlled MMN paradigm was developed (Schröger and Wolff, 1996). In this paradigm, in addition to the oddball block, a control block with 10 tones, including standards and deviants, was presented additionally. There was a deviant-related negativity in the deviant-control comparison, which eliminated the influence of different probability. It was proposed that these results were best explained by the memory-comparison hypothesis. In later studies, the controlled MMN paradigm was used to explore this pre-attentive change-detection system widely (Jacobsen and Schröger, 2003, Maess et al., 2007, Horvath et al., 2008).

The goal of the current study was to explore how PTSD symptoms influence change detection processing in the auditory cortex as measured by MMN. The controlled MMN paradigm was used to investigate the pre-attentive processing of earthquake survivors. With this version of the task, we could compare the difference in the sensorial, non-comparator mechanism and the cognitive comparator mechanism between two groups. We predicted that brain potentials indicative of pre-attentive auditory processing differ in PTSD subjects.

Section snippets

Participants

Volunteers were recruited from the Beichuan Vocational High School in Sichuan Province. They all experienced the tremendous earthquake in Wenchuan County of Sichuan Province, China on May 12, 2008, that measured 8.0 on the Richter scale and left about 69,000 people dead. These subjects were not injured and did not receive any psychiatric treatment or medication before this study. They completed the PTSD Checklist-Civilian Version (PCL-C) for PTSD screening (Andrykowski et al., 1998, Blanchard

Psychometric data

The Spielberger anxiety, PCL-C, and HSCL-25 scale scores were shown in Table 1. All scores were significantly higher in the PTSD group than in the control group, but there was no significant correlation between psychometric data and ERP data in the PTSD or control groups.

ERP data

ERPs and difference waves were presented in Fig. 1. The ANOVA (group × location × condition) was tested for N1 amplitude. No group effect was detected on N1 amplitude. The main effect of location on N1 mean amplitude was

Discussion

Patients with PTSD exhibited significantly increased MMN amplitudes, compared to control group, in both traditional MMN (DS) and controlled MMN (DC). In contrast, there were no significant group differences in the amplitude of N1, which was thought to reflect the transmission of sensory information to the cortex.

The present paradigm, which we believe to be more rigorous because it employs an additional control block (Jacobsen and Schröger, 2001, Horvath et al., 2008), was designed to

Acknowledgements

This work was supported by NSF China (90924017) and the Project for Young Scientist Fund, IP, CAS (O9CX062006). We express great appreciation to the teachers and students in Beichuan Vocational High School for their courage after experiencing the earthquake and their supports in this study.

References (43)

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