Association between EEG alpha power and visuospatial function in obsessive–compulsive disorder
Assoc. Professor Jun Soo Kwon, Department of Psychiatry, Seoul National University College of Medicine, 28 Yongon-dong, Chongno-gu, Seoul 110-744, Korea. Email: firstname.lastname@example.org
Abstract The purpose of the present paper was to determine if frontal activity, measured as electroencephalogram alpha power, correlates with visuospatial functions in obsessive–compulsive disorder (OCD). Electroencephalography and the Rey–Osterrieth Complex Figure Test (RCFT) were performed on 23 patients meeting the Diagnostic and Statistical Manual of Mental Disorders (4th edn; DSM-IV) OCD criteria. After quantitatively analyzing EEG recordings taken over the frontal, temporal, parietal and occipital regions (F1, F2, T3, T4, P3, P4, O1 and O2), the log transformed absolute power values of the alpha frequencies of the regions were regressed with each RCFT index (copy, immediate recall and delayed recall score). On the frontal region (F1, F2), the RCFT copy score was found to be correlated with the alpha power with regression coefficients that had different directions according to hemisphere (F1, 5.62; F2, −5.26). The result that visuo-constructional ability represented by the RCFT copy score correlated with frontal activation as measured by decreased alpha power, supports the opinion that visuospatial dysfunction in OCD is not in the visuospatial memory per se but rather that it is mediated by executive function deficit. The opposite correlation directions indicate that greater left frontal activation correlates with a poorer RCFT copy score and that greater right frontal activation correlates with a better copy score. These relationships provide indirect evidence of the possibility that the main pathology of OCD is located in the left hyperfrontality and that the right hyperfrontality of OCD occurs by a compensatory mechanism.
One of the most consistent findings in neuroimaging research of obsessive–compulsive disorder (OCD) is ‘hyperfrontality’,1–4 and visuospatial dysfunction is considered similarly in neurocognitive research of OCD.5,6 Despite the fact that these two findings have been reported steadily in OCD, few hypotheses have been suggested to link these findings. Recently Savage et al. provided a clue to this relationship, by showing that visuospatial dysfunction in OCD can originate from executive function problems.7 They found that the low visuospatial memory function of OCD, as measured by the Rey–Osterrieth Complex Figure Test (RCFT) was mediated by impaired organizational strategies during the initial copying of the RCFT figure. Therefore the primary deficit was not in visuospatial memory per se but in executive function, which corresponds to the current theory of a fronto-striatal system problem in OCD. However, there remains a problem concerning the relation between ‘hyperfrontality’ of the brain and cognition ‘hypofunctionality’. Hyperfrontality here guarantees only a high frontal lobe perfusion rather than real activity of the frontal lobe.8,9 There is also a possibility that high perfusion could be caused by a compensatory mechanism to low neuronal cell activity.
Electroencephalography (EEG) measurements may offer a route to the solution of this problem because they directly reflect the activity of neuronal cells.10,11 Although there is a little debate on the physiological meaning of alpha attenuation,12 if one considers the fact that EEG alpha activity is suppressed by arousal13 or activated during tasks,14 it can be reasonably presumed that lower alpha power reflects higher brain activity.15–17
Generally, visuospatial function is considered to be controlled in the parietal lobe in normal people.18,19 In EEG studies relating brain regions with visuospatial memory, the involvement of the parietal lobe has been reported in normal people.20–22 Such studies have found that better visuospatial performance is correlated with decreased right parietal alpha power at rest. However, if visuospatial dysfunction in OCD, as measured by RCFT, is more an organizational problem than a problem of the visuospatial function per se, then it is likely that neuronal activity measured by alpha power is correlated with the RCFT score in the frontal lobe rather than in the parietal lobe. Extending the argument, we posed the question ‘is hyperfrontality really associated with cognitive hypofunction?’. Thus, we undertook to investigate whether frontal activity, as measured by alpha power, is correlated with a poorer cognitive function. Because if so, then it is possible to state that hyperfrontality per se has a pathologic effect on cognition in OCD patients. In contrast, if hyperfrontality is not a cause but an epiphenomenon of OCD due to some compensatory mechanism, then it would be expected that the frontal lobe functions properly and, consequently, that the frontal activities of OCD patients, as measured by alpha power, should correlate with a better cognitive function.
The aim of the present investigation was to determine whether frontal activity, as measured by alpha power, correlates with visuospatial function in OCD as measured by RCFT or not, and to probe whether ‘hyperfrontality’ is an essential feature or simply an epiphenomenon of pathology in terms of cognitive function in OCD.
Twenty-three patients with OCD (14 men and nine women) with a mean age of 27.1 years (SD = 8.7) were recruited from the Seoul National University Hospital Obsessive–Compulsive Disorder Clinic, Seoul, South Korea. Twenty of the OCD subjects had been medication-free for at least 2 weeks at the time of evaluation. Twenty-one of the OCD subjects were right-handed. Diagnoses of OCD were made according to Diagnostic and Statistical Manual of Mental Disorders (4th edn; DSM-IV) OCD criteria23 by consensus between two board-certified psychiatrists. Exclusion criteria were comorbid axis I disorders, current or past neurological illness, mental retardation, and substance abuse, as evaluated by history, physical examinations, and laboratory testing (complete blood count, urinalysis, liver function tests, and serology). The Yale–Brown Obsessive–Compulsive Scale (YBOCS)24,25 was used to assess symptom severity; their mean YBOCS score was 24.05 (SD = 10.05). Depressive symptom level was measured using the Beck Depression Inventory (BDI),26 and anxiety symptom severity was measured by the Beck Anxiety Inventory (BAI);27 their mean BDI score was 22.82 (SD = 13.72) and their mean BAI score was 23.70 (SD = 13.97). After we had given a complete description of the study to the subjects, written informed consent was obtained.
All patients were instructed to copy an RCFT figure and subsequently draw what they remembered immediately and after a 30 min delay. Accuracy of copy and recall was quantified using a scoring system developed by Meyers and Meyers;28 their mean RCFT copy score was 33.26 (SD = 3.17), mean immediate recall score was 15.00 (SD = 6.55) and their mean delayed recall score was 15.56 (SD = 6.16).
The patients were seated comfortably in a sound- and light-attenuated room and 10–15 min of resting EEG data was recorded from 21 electrode sites, according to the International 10/20 protocol for a computer-based system (Cadwell Spectrum 32, software 4.21; Cadwell Laboratories, Kennewick, WA, USA). Whenever any decreased alertness was detected on the EEG, the patient was instructed to open his or her eyes. Data from 24 epochs (2.5 s/epoch, total of 1 min) of artifact-free data were selected, and these samples were digitized at 205 samples/s to obtain power spectra by fast Fourier transformation (FFT). Artifacts were eliminated by visual inspection. Impedance was kept below 5 kOhm for each electrode. A time constant of 0.3 s and a high cut-off frequency of 70 Hz were used. Electro-oculogram was used to exclude eye movement. The EEG absolute amplitude values of the alpha (7.5–12.5 Hz) frequency band (after FFT) were evaluated for the frontal, temporal, parietal and occipital regions (F1, F2, T3, T4, P3, P4, O1 and O2).
In order to fit the EEG data into a normal distribution, a log transformation of the power values of alpha frequency at each electrode location was calculated prior to statistical analysis as previously recommended.29,30 A linear regression model was used to evaluate systematic linear trends between the eight channel alpha powers and each RCFT score (copy, immediate recall and delayed recall score). Age and sex were considered in the regression model. A Bonferroni correction was performed because the regression procedure was performed in triplicate for the copy, immediate recall and the delayed recall scores (α = 0.05, Bonferroni corrected α′ = 0.017).
Significant linear trends were found between the log transformed alpha power and the RCFT copy score in the region of the left frontal (F1) and right frontal (F2) lobe. Table 1 summarizes the result of the linear regression analysis. As can be seen from the table, the regression coefficient (β) of the frontal area was found to have a different direction in the different hemispheres (i.e. positive on the left frontal region (F1: 5.62) and negative on the right (F2: 5.26)). No significant linear trends were found for the immediate and delayed recall scores. Age and sex did not affect the results.
Table 1. Summary of linear regression model between eight channel alpha powers and RCFT copy score in the patients with OCD (R2 = 0.567, d.f. = 9,13)
|F1|| 5.62|| 3.44||<0.01|
|T4|| 1.53|| 2.13|| 0.05|
|O2|| 1.93|| 1.83|| 0.09|
As we hypothesized, the frontal region was found to be significantly correlated with the visuospatial function. Our result shows a correlation for the frontal region but not for the parietal region, which is different from previous reports that better visual memory performance was correlated with greater activation of parietal lobe in normal people.20,21,31 It should be kept in mind that our results show only the area that has significant correlation between alpha power and RCFT score, and it is not localizing ‘the source of alpha rhythm’. The source of the alpha generator has not been identified in the frontal lobe as yet, and it is still uncertain as to whether the frontal lobe has an alpha generator or not. Important here is that the correlation was specific to frontal area. This finding supports the notion that primary neuropsychological deficit of OCD, as featured in RCFT, is in the prefrontal executive function.7,32 The most intriguing result, and one which requires further interpretation, is that the regression coefficients had opposite signs in the hemispheres. Greater left frontal activation, measured by lower alpha power, was found to be correlated with a poorer RCFT copy score and greater right frontal activation to be correlated with a better copy score, which indicates that the hemispheres are dissociated in relation to visuospatial skills. Specifically, the left frontal area showed a tendency to have a negative effect on visuospatial skill, whereas the right frontal area functioned normally although its function may be below average. Considering previous reports on ‘hyperfrontality’ together with present results, we can provide a possible explanation for this hemispheric dissociation, namely that the ‘hyperfrontality’ of the right frontal lobe is the result of a compensatory mechanism triggered by the pathology of left frontal hyperacti-vity in OCD. However, we are left with the problem mentioned before, that is, why does hyperactivity of the left frontal lobe reduce organizing function?
Recently, Alan Gevins and Michael E. Smith divided normal subjects into two groups based on their spatial working memory test scores. When the lower ability group was compared with the higher ability group, it was found that the lower ability group used more frontal lobe circuits for organizing information in working memory, whereas the higher ability group used both the frontal and parietal lobes, and specifically, more parietal lobe than frontal lobe.22 They maintained that individuals with low ability use strategies that ‘rely more exclusively on the limited capacity of the frontal lobes circuits’ and that the high-ability group used a strategy that ‘took advantage of distributed cortical processing resources’. Furthermore, they also found hemispheric asymmetries, for example, that verbal cognition tends to make greater use of the left hemisphere whereas non-verbal cognition tends to use the right hemisphere, although this tendency is clearer for the parietal lobe than for the frontal lobe. Other, similar, types of hemispheric asymmetry, which suggests that the left brain dwells on detail while the right brain is good at grasping the whole picture, have also been reported.33 In relation to the hemispheric asymmetry of OCD, recently Tot et al. tried to identify regional differences on the EEG of OCD patients and found a predominant left frontotemporal dysfunction in OCD.34 Therefore, based on all results available to date, we believe that left hyperfrontality is responsible for the dysfunction of visuospatial organizing skill in OCD patients.
The observation that of the RCFT scores only copy score was found to be significantly correlated with the alpha power, prompts us to comment that different information is provided by the copy, immediate and delayed recall scores.35,36 The copy trial reflects perceptual, visuospatial and organizational skills, whereas immediate recall reflects the amount of encoded information, and delayed recall reflects the amount of information that is stored and retrieved from memory. Thus, only the copy score directly reflects an index of visuoconstructional ability. Therefore, the finding that only the copy score is associated with frontal activity also supports the opinion that the primary problem of visuospatial dysfunction in OCD lies in executive function.
One limitation of the study is that we are not sure whether our result is specific to OCD because we did not investigate a normal control group. We can only approximately estimate the specificity of our result from the previous EEG studies of normal people who showed a relationship between better visual memory performance and greater parietal activation, not frontal activation, as was aforementioned.20,21,31 Further study with a normal control group will be helpful to the confirmation of the results.
In conclusion, the present study demonstrates a significant association between visuospatial function and frontal lobe activity in OCD patients, which supports recent opinion that the primary deficit of visuospatial function in OCD is not in the visuospatial memory per se but in the executive function. The opposite directions of the regression coefficients of the right and left frontal area suggest the possibility that the main pathology of OCD is associated with left frontal hyperactivity, and that right frontal hyperactivity in OCD is caused by an attempt to compensate for the left side pathology.
The present study was supported by a grant from Janssen Korea Limited (800–20000313).