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The Journal of Nervous and Mental Disease • Volume 195, Number 9, September 2007 785
Propper et al. The Journal of Nervous and Mental Disease • Volume 195, Number 9, September 2007
episodic memory processing (e.g., Babiloni et al., 2004; and Fp2, referenced to linked mastoids, and grounded to
Kaiser and Lutzenberger, 2005; Klimesch et al., 1994). Be- forehead. EEG was amplified using the Biopac MP30
cause alpha has been associated with semantic memory pro- (Biopac Systems, Inc., Santa Barbara, CA) and digitally
cesses (e.g., Klimesch et al., 1994; Mima et al., 2001), we recorded at 200 samples/s on a 12 in (30.5 cm) iBook
also examined the alpha frequency to rule out a general, Macintosh Laptop using the AcqKnowledge 3.6.6 software.
nonepisodic memory-related effect of stimuli condition on Impedance was kept below 10 KÙ. EEG was inspected for
interhemispheric interaction. artifact; EEG greater than "200 !V was excluded.
The power spectrum for the first artifact-free 1-second
METHODS epoch per prestimuli and poststimuli blocks (EO pre, EC pre,
EO post, EC post) was Fast Fourier transformed using a
Participants Hamming Window for each participant in each frequency.
Twenty-two right-handed undergraduates participated This epoch definition was chosen to illustrate the immediate
(M age ! 20.11, SD ! 1.49) for extra credit in a psychology impact on the EEG after the saccade that is closer in line with
course. All read and signed an informed consent form, and the event-related brain potential literature epochs of 1 second
the experimental protocol received Institutional Review (Intriligator and Polich, 1995; Spencer and Polich, 1999).
Board approval from the University of Toledo Institutional Epochs occurred at least 3 seconds after the beginning or 3
Review Board committee. A 1-second, artifact-free epoch seconds before the end of a block. No artifact occurred less
from at least one of the pre- or poststimuli blocks was unable
than 0.5 seconds before or after an epoch. EEG was band-
to be recovered for 4 participants; data from these individuals
pass filtered such that the gamma band was 35 to 54 Hz (this
were not included in analyses (total N ! 18). Ten participants
gamma band is higher than the typical beta bands that are
(7 females, 3 males) served in the moving stimuli (MS)
often measured up to 35 Hz; we chose 54 Hz as the upper
condition, and 8 (4 females, 4 males) served in the colored
cutoff to avoid any 60 Hz notch filtering induced by AC
stimuli condition.
current that could artificially modulate gamma activity), theta
Materials and Procedure band was 4 to 8 Hz, and alpha band was 8 to 13 Hz.
Coherence (IhCo) values were calculated using a point by
Stimuli
point squaring of a serial cross-correlation of the power
Stimuli and instructions were presented on a Macintosh
spectrum resulting in a coherence value #left (Fp1) $
G3 computer with a 16-in (40.64 cm) monitor using Superlab
right (Fp2)%/(left (Fp1) & right (Fp2)% for each power band
Pro 1.75 (Cedrus Corporation, 1997). Participants sat approx-
imately 60 cm from the monitor. Replicating (Christman et (gamma, alpha, and theta). EEG coherence refers to the
al., 2004, 2006), the MS condition induced saccadic EMs by squared cross-correlation between EEG power from 2 scalp
having participants move their eyes to follow a black dot locations within a frequency band and indexes the functional
(approximately 4° of visual angle in diameter) that appeared covariation of activity between 2 different cortical areas
sequentially on the left and right portions of the white screen (Nunez et al., 1997). IhCo was calculated between Fp1 and
of the computer monitor. The dot changed positions every Fp2 for each epoch in each EO and EC block. IhCo change
500 milliseconds, resulting in 2 saccadic EMs per second, for was calculated as IhCo poststimuli $ IhCo prestimuli for EO
30 seconds. The dots were located approximately 27° of and EC blocks separately; positive numbers represent in-
visual angle apart. The color stimuli (CS) condition was creasing interhemispheric coherence from pre to post; nega-
identical to that used in Christman et al. (2006). Participants tive numbers indicate decreasing interhemispheric coherence
viewed a centrally presented dot (approximately 4° of visual from pre to post.
angle in diameter) that alternated between green and red
twice per second, for 30 seconds. The CS condition was a General Procedure
control condition in which participants received 30 seconds Before each block, instructions for each condition ap-
of 2 Hz periodic visual stimulation in the absence of EMs. peared on the computer screen. The experimenter read aloud
Because EMs result in EEG artifact at frontal sites these instructions, ensured participants’ understanding, and
during the MS condition and cannot be analyzed, 4 additional covertly observed the participants’ eyes to make sure instruc-
conditions were used. In the eyes-closed condition (EC), tions were followed.
participants closed their eyes for 30 seconds. In the eyes-open EEG was recorded continuously during the experiment.
condition (EO), participants kept their eyes open and focused All participants viewed 5 blocks: EO prestimuli, EC pre-
on a centrally presented static black dot (approximately 4° of stimuli, stimuli condition (either MS or CS), EO poststimuli,
visual angle in diameter) for 30 seconds. Participants per- and EC poststimuli (order of EO and EC pre- and poststimuli
formed one EC and one EO block as prestimuli baseline was counterbalanced). EO condition: participants kept eyes
conditions and, following either an MS or CS block, per- focused on the black dot in the center of the computer screen;
formed one EC and one EO block as poststimuli recovery EC condition: participants kept eyes closed, and were told
conditions. when to open them; MS condition: participants kept eyes
focused on the black dot as it flashed in different locations on
EEG Materials and Analysis the computer screen; CS condition: participants kept eyes
Biopac EL503 disposable electrodes were applied using focused on the color changing dot in the center of the
the International 10 –20 Electrode Placement System to Fp1 computer screen. Participants were not asked to think about
DISCUSSION
Contrary to our hypothesis of increased interhemi-
spheric coherence after EMs, we found decreased gamma
frequency coherence associated with engaging in 30 seconds
of bilateral EMs with eyes open. Although surprising, these
findings correspond with a recent functional magnetic reso-
nance imaging study. Umeda et al. (2005) reported decreased
functional interaction between the left and right hemispheres
FIGURE 2. IhCo as a function of stimuli condition during the in anterior prefrontal cortex during episodic retrieval. Given
eyes open prestimuli and poststimuli blocks. that the cortical locations of Fp1 and Fp2 coincide with the
location of anterior frontal cortex in which decreased func-
tional interhemispheric interaction was reported (Umeda et
anything in particular but merely to “focus on the dot” or to al., 2005), it seems likely that the results of the present
“keep their eyes closed.” study are related to the findings of Umeda et al. Specifi-
cally, the EM manipulation used in the present study,
RESULTS reported previously to facilitate episodic memory, resulted
Mixed analyses of variance with stimuli condition (MS in decreased interhemispheric EEG coherence in anterior
vs. CS) and block (EO vs. EC) as between- and within- prefrontal cortex.
participants (respectively) variables were performed on IhCo Because the gamma band includes the 40 Hz wave that
change for each frequency. Order of poststimuli block (EO may indicate the active binding of information during the
block or EC block first after stimuli condition) did not interact consolidation of long-term memory storage (e.g., Cahn and
with stimuli condition in any band; analyses collapsed across Polich, 2006), it is particularly notable that the changes in
TABLE 1. IhCo Mean and (SD) as a Function of Stimuli Condition and Block for Each Frequency
Stimuli Condition as a Function of Block
EO Pre EC Pre EO Post EC Post
Frequency Color Stimuli Moving Stimuli Color Stimuli Moving Stimuli Color Stimuli Moving Stimuli Color Stimuli Moving Stimuli
Alpha 0.95 (0.01) 0.94 (0.01) 0.95 (0.01) 0.95 (0.01) 0.95 (0.01) 0.94 (0.01) 0.94 (0.01) 0.95 (0.01)
Theta 0.91 (0.06) 0.90 (0.07) 0.91 (0.06) 0.93 (0.06) 0.86 (0.08) 0.89 (0.05) 0.87 (0.11) 0.93 (0.08)
Gamma 0.68 (0.10) 0.74 (0.06) 0.72 (0.06) 0.75 (0.08) 0.74* (0.04) 0.68* (0.08) 0.70 (0.09) 0.74 (0.05)
*Significance p ' 0.05.
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