Impaired upper alpha synchronisation during working memory retention in depression and depression following traumatic brain injury
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).
Section snippets
Participants
Thirty-four healthy controls, 20 MDD, 20 TBI-only, and 15 TBI-MDD participants were recruited. Data from six participants was excluded; three controls (one showed mild depression and two due to equipment faults), and three MDD participants (one did not meet depression severity criteria, and two due to equipment faults). This left 31 control, 17 MDD, 20 TBI-only, and 15 TBI-MDD participants. Participants were recruited through the Monash Alfred Psychiatry Research Centre database, the Alfred
Demographics, depression, and TBI severity
Table 2 displays the means and standard deviations for demographic data and clinical measures. Groups did not significantly differ in age, handedness or estimated pre-morbid IQ (all F's < 2.05, all p's > 0.10). Significant differences were found for years of education (F(3,78) = 2.96, p < 0.05). Post hoc Tukey showed the TBI-MDD group had fewer years than the control group (p < 0.05). The TBI-only and TBI-MDD groups did not significantly differ in brain injury severity as measured by length of PTA, GCS,
Discussion
The aim of this study was to determine the relative impact of TBI and MDD on inhibitory (upper alpha) processes during WM retention. We found that individuals with MDD and TBI-MDD show delayed WM reaction times compared to controls, and individuals with MDD alone showed accuracy impairments. We also found that individuals with MDD and TBI-MDD showed less elevated posterior upper alpha activity while information is being retained in WM. No WM impairments or reductions in upper alpha activity
Disclosure statement
PBF has received equipment for research from Medtronic ltd, Magventure A/S and Brainsway Ltd. and funding for research from Cervel Neurotech. NWB, RAS, KEH, JJM have no conflicts to declare.
Acknowledgments
Funding for this study was provided by Monash University and the Victorian Neurotrauma Initiative. Equipment funding was provided in part by the Neurosciences Victoria Clinical Neurobiology of Psychiatry Platform. PBF is supported by a Practitioner Fellowship grant from the National Health and Medical Research Council (NHMRC). RAS and KEH are supported by Post Doctoral Training Fellowships from NHMRC. JJM is supported by an NHMRC CDF Fellowship.
References (36)
- et al.
Peak alpha frequency: An electroencephalographic measure of cognitive preparedness
Clinical Neurophysiology
(2004) - et al.
The long-term effects of mild head injury on short-term memory for visual form, spatial location, and their conjunction in well-functioning university students
Brain and Cognition
(2004) - et al.
EOG correction of blinks with saccade coefficients: A test and revision of the aligned-artefact average solution
Clinical Neurophysiology
(2000) - et al.
Behavioural and physiological impairments of sustained attention after traumatic brain injury
Cognitive Brain Research
(2004) - et al.
Cognitive inhibition and working memory in unipolar depression
Journal of Affective Disorders
(2009) - et al.
Depression following traumatic brain injury: A 1 year longitudinal study
Journal of Affective Disorders
(1993) - et al.
EEG alpha oscillations: The inhibition-timing hypothesis
Brain Research Reviews
(2007) - et al.
Routine and quantitative EEG in mild traumatic brain injury
Clinical Neurophysiology
(2005) The assessment and analysis of handedness: The Edinburgh Inventory
Neuropsychologia
(1971)- et al.
Functional limitations and depression after traumatic brain injury: Examination of the temporal relationship
Archives of Physical & Medical Rehabilitation
(2008)
Neuropsychiatric sequalae of traumatic brain injury
Psychosomatics
The impact of major depression on outcome following mild-to-moderate traumatic brain injury in older adults
Journal of Affective Disorders
Upper alpha activity during working memory processing reflects abnormal inhibition in major depression
Journal of Affective Disorders
Quantification of event-related coherence (ERCoh)
Internal consistencies of the original and revised Beck Depression Inventory
Journal of Clinical Psychology
A review of mild head trauma. Part I: Meta-analytic review of neuropsychological studies
Journal of Clinical and Experimental Neuropsychology
Depression and memory impairment: A meta-analysis of the association, its pattern, and specificity
Psychological Bulletin
Gender differences in the EEG during cognitive activity
International Journal of Neuroscience
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