How does noninvasive brain stimulation during nocturnal slow wave sleep affect EEG- activity and performance in a visual memory task in healthy older adults? Sven Paßmann1, Nadine Külzow1, Sascha Tamm2, Agnes Flöel1 1Department
of Neurology, NeuroCure Cluster of Excellence, Neurocure Clinical Research Center, Charite-Universitätsmedizin, Berlin 2Departement of Experimental and Neurocognitive Psychology, Center for Applied Neuroscience, Freie Universität Berlin contact:
[email protected]
Introduction Previous studies demonstrated an improvement in both overnight retention of word-pairs and associated neurophysiological events (frontal
slow oscillatory activity (SWA; 0.5-1Hz), spindel activity) by exogenous transcranial slow oscillating stimulation (tSOS) during NREM sleep in young healthy subjects (1). Given the coincidence of age-related decline in memory and SWA, these results are encouraging in terms of boosting SWA and in parallel memory consolidation in the elderly. However, a recent study using the same word-pair list in a sample of healthy older adults failed to show a beneficial effect (2).
Aim This study examines whether the application of tSOS (resembling the same protocol as Marshall et al.) during nocturnal sleep impact sleep
associated neurophysiological events (SWA, slow/fast spindle band) and modulate visual-spatial memory consolidation in healthy older adults .
Material / Subjects: 21 healthy older adults (64.9 ± 1.3, 11 male) Methods
Design: • 2 nights, cross-over with counterbalanced tSOS / SHAM stimulation, separated by at least 2-3 weeks
Stimulation: • location: bifrontal • duration: 5 x 5min-blocks of oscillatory stimulation, 1min artifact- and stimulation-free intervals in between • frequency: 0.75Hz, offset: 260μA, max. current density: 0,522mA/cm2 • inter-stimulus intervals monitored online for sleep stage 2 at least
Visual Recognition Task Encoding: • 38 neutral pictures (3) of different categories e.g., objects, plants, scenes; presented in one of four quadrants (Fig. 2) Recall (immediate and delayed): • OLD/NEW recognition task: 38 old intermixed with 38 new neutral pictures centered on the screen - if a picture deemed as “OLD” – a “WHERE“ response was required
anodes
Fig 1. Schematic description of procedure
Fig 2. Encoding and recall of visual spatial task
Garten - Beet
500 ms
Wo wurde das Bild gezeigt? cathodes
2000 ms
Garten - Beet
regular nocturnal sleep
Garten - Beet
Proband: SW S-J-011-Exp1N_sp.vhdr
W REM
2000 ms
Garten - Beet
S1
Garten - Beet
1000 -1500 ms
S2 S3
2000 ms
S4
encoding & M immed. recall
adaptation night
neuropsych. assessment
Time
time
9.30-10.30 pm
3000 ms
+ 22:00
23:00
00:00
11.00 pm
01:00
12.00 am
02:00
7.30 am
03:00
delayed recall 04:00
05:00
06:00
07:00
+
1000 ms
1000 ms
7.50–8.15 am
encoding trial
tSOS/SHAM
immediate-/ delayed recall
4 minutes after start NREM2
Results Visual-Recognition Task (OLD-NEW-Decision):
• Decrease in accuracy (percent correct) after stimulation
(Condition x
Time: F(1,20) = 5.08, P = .036, Fig.3)
Location (WHERE) Task: no significant effect (P > .05) Control Tasks: • no significant differences in finger-tapping, VAS-tired, affective state (PANAS) and tiredness symptoms (all P > .086) • Tension (VAS): before, but not after sleep subjects were less relaxed under SHAM compared to STIM (Condition X Time: F(1,20) = 5.08,
Sleep Stages (entire night): • no significant stimulation effects in WASO and in sleep stages, except sleep stage 4 (SP4STIM < SP4SHAM, P = .046) • no significant impact on sleep quality or sleep efficiency EEG: • inter-stimulus intervals I1-I5: significant effects only in higher frequency bins (see Fig. 4 and Table 1; non-linear Mixed Model Analyses) • SWA (0.5-1Hz) n.s. (P > .05)
P = .036)
difference from learning
4
Memory Performance
frequency band slow spindles (8-12Hz)
stim sham
*
2
0
fast spindles (12-15Hz) -2
-4
PRcorrect stim
PRcorrect sham
Fig 3. Performance measured in % correct. Results shows difference scores (morning– evening). Positive values indicate improvement.
Fig 4. stim-sham difference of mean value of power (µV), averaged over inter-stimulus interval 1-5 for slow (8-12Hz) and fast (12-15Hz) spindle band
electrode site prefrontal
b .132*
SE b .061
95% CI .01, .25
frontal
.112†
.060
-.01, .23
central
.153**
.057
.04, .27
centroparietal
.139*
.062
.02, .26
parietal
.085
.061
-.04, .21
prefrontal
.176**
.059
.06, .29
frontal
.123*
.058
.01, .24
central
.132*
.057
-.03, .29
centroparietal
.097
.062
-.03, .22
parietal
.011
.055
-.10, .12
Table 1. prefrontal (FP1, AFZ, FP2); frontal (FC1, FZ, FC2); central (C3, CZ, C4); centro-parietal (CP1,CZ,CP2); parietal (P3,PZ,P4); b = regression coefficient; SE = standard error; 95% CI = confidence interval ; † p < .10, * p < .05, ** p < .01;
Discussion • Although tDCS lead to enhanced power in spindle bands, SWA remained unaffected and in parallel visual memory performance was
impaired • discrepancy may result from differences in stimulation protocol (suggest an adapted protocol for elderly e.g., later start of stimulation) or specificity of the age group (e.g., higher intervariability on stimulation-response, age-related changes in the sleep-consolidation relationship (4))
References
1Marshall
et al. (2006). The Journal of Neuroscience 24(44): 9985–92; 2Eggert et al. (2013). Brain Stimul. 2013 Nov;6(6):938-45, 3The Multimodal Stimulus Set (MULTIMOST) was developed by Schneider TR, Debener S & Engel AK at the Dept. of Neurophysiology and Pathophysiology, University Medical Center Hamburg- Eppendorf, Germany; 4Scullin and Bliwise (2015). Perspectives on Psychological Science Vol10(1) 97–137.