Impaired upper alpha synchronisation during working memory retention in depression and depression following traumatic brain injury

Highlights

• We tested working memory in depression post-traumatic brain injury.

• We examined alpha inhibitory processes during the retention period using EEG.

• We found reduced parietal-occipital alpha in traumatic brain injury depression.

• We also found reduced parietal-occipital alpha for depression alone.

• However, there were no changes in traumatic brain injury alone.

Abstract

Rates of major depressive disorder (MDD) following traumatic brain injury (TBI) are higher than in the general population. Individuals with depression following traumatic brain injury (TBI-MDD) exhibit working memory (WM) impairments. Electrophysiological evidence has suggested that parieto-occipital upper alpha synchronisation may enhance WM retention by inhibiting irrelevant processes. The current research assessed whether retention period WM parieto-occipital upper alpha activity is disrupted in groups with TBI-only (N = 20), MDD (N = 17), and TBI-MDD (N = 15) compared to healthy controls (N = 31). Behavioural data indicated poorer performance in MDD and TBI-MDD. Parietal-occipital upper alpha was reduced in the MDD and TBI-MDD groups, but was unaffected in TBI-only. These results suggest inhibitory deficits may account for WM impairments in MDD and TBI-MDD, and that for individuals with TBI-MDD it may be the depression rather than the TBI that impairs WM.

Introduction

Following traumatic brain injury (TBI), rates of major depressive disorder (MDD) are higher than in the general population. Estimates suggest rates of 20–45% measured at time points between 3-months and 30-years post-injury, compared with an annual prevalence of between 5% and 10% for the general population (Jorge et al., 1993, Kreutzer et al., 2001, Pagulayan et al., 2008, World Health Organisation, 2001). MDD has been shown to have a negative impact on outcomes following TBI, including cognitive outcomes (Rapoport et al., 2006, Satz et al., 1998).

One aspect of cognition frequently impaired in TBI, MDD, and their co-occurrence is working memory (WM) (Burt et al., 1995, Chuah et al., 2004, Jorge et al., 2004). Electroencephalography (EEG) can be used to measure brain activity related to effective WM performance. In particular, an increase in synchronous upper alpha activity (10–12.5 Hz) in the parieto-occipital region is thought to represent inhibition of non-relevant information (Jensen et al., 2002, Klimesch et al., 2007). Jensen and Mazaheri (2010) propose the mechanism by which the alpha rhythm generates it's inhibitory action is via disruption of ongoing gamma synchronisation, preventing gamma from binding information between areas. This may prevent WM retention from interference by activity in non-WM related regions.

Evidence suggests that alpha activity is disrupted following TBI and in individuals with MDD. Following TBI, research has found reduced alpha desynchronisation during motor inhibition (Dockree et al., 2004), reduced resting alpha peak frequency (Angelakis, Lubar, Stathopoulou, & Kounios, 2004), and reduced inter-regional alpha coherence during WM encoding, retention, and retrieval (Kumar, Rao, Chandramouli, & Pillai, 2009). However, no research has directly examined parieto-occipital upper alpha power during WM retention in this population. It has been suggested that alpha alterations post-TBI are related to anxiety and mood rather than the injury itself (Nuwer, Hovda, Schrader, & Vespa, 2005), so we are currently uncertain as to the effect of mild to moderate TBI-alone on WM retention alpha. Research focusing on MDD, however, has examined upper alpha activity specifically during WM. Segrave et al. (2010) measured WM with the Sternberg task (which is constructed so that information encoding, retention, and recall periods are temporally separate, enabling researchers to isolate each process), and found increased upper alpha activity in MDD over the left parieto-occipital region during the retention period. Currently, no research has examined WM alpha activity in individuals with TBI-MDD.

The aim of current study was to investigate the impact of TBI and MDD and TBI-MDD on inhibitory (upper alpha) processes during WM retention. It was hypothesised that both TBI-only and MDD participants would show reductions in WM upper alpha activity compared to controls, and that the TBI-MDD group would show even larger reductions. It was also hypothesised that these differences would be more apparent with larger WM loads, as alpha activity is modulated by cognitive load (Gevins et al., 1997, Jensen et al., 2002).