EEG Patterns Prior to Motor Activations of Parasomnias: A Systematic Review

Figures & data

Figure 1 Flow diagram.

Table 1 Quality Assessment of Documents (Newcastle–Ottawa Quality Assessment Scale Case–Control Studies)

Ref	Selection (Maximum 4 Stars)	Comparability (Maximum 2 Stars)	Exposure (Maximum 3 Stars)
Schenck et al^Citation40	⋆⋆		⋆⋆
Zadra et al^Citation41	⋆⋆	⋆	⋆⋆⋆
Espa et al^Citation20	⋆⋆⋆⋆	⋆	⋆⋆
Guilleminault et al^Citation34	⋆⋆	⋆	⋆⋆
Pilon et al^Citation35	⋆⋆	⋆	⋆⋆
Jaar et al^Citation42	⋆⋆		⋆⋆
Perrault et al^Citation43	⋆⋆		⋆⋆
Januszko et al^Citation44	⋆⋆		⋆⋆
Desjardins et al^Citation45	⋆⋆

Table 2 Sample Characteristics and Night Recordings Description

	Sample Characteristics					Night Recordings
Ref	Parasomnia Group				Control Group	Experimental Night	Activations Characteristics
	N	Gender	Mean Age (Years) (sd)	Parasomnia Diagnosis
							Behavioral Episodes of NREM Parasomnias (BEp)			Non-Behavioral Arousals (NBEp)
							N	Episode Onset		N	Episode Onset
Schenck et al^Citation40	38*	F=17	28.9 (9.6)	SW= 3 SW and ST=35	-	1 or 2** Undisturbed night	87	SWS		163	SWS
Zadra et al^Citation41	1	F	32	ST=1	N° 10 (F=5) Age: matched	P: 3 undisturbed nights C: 2 undisturbed nights	3	SWS		-	-
Espa et al^Citation20	11	F=6	31.2 (2.24)	SW=3 ST=6 SW and ST=2	N° 11 (matched) Mean age: 32.1 (2.48)	P: 1 undisturbed night C: 1 undisturbed night	15	SWS		P=15 C=40	P=SWS C=SWS
Guilleminault et al^Citation34	12	F=7	23.8 (3)	SW=12	-	1 Undisturbed night	21	SWS		-	-
Pilon et al^Citation35	10	F=7	25.1 (4.1)	SW=10	-	Sleep-deprivation protocol (h38): 1 Baseline night 1 Recovery	35	SWS		-	-
Jaar et al^Citation42	22	F=11	28.6 (7.4)	SW and/or ST=22	-	Sleep-deprivation protocol (h25): 1 Baseline 1 Recovery	22	SWS		-	-
Perrault et al^Citation43	12	F=9	27.4 (8.4)	SW=12	-	1 Undisturbed night	12	SWS		12	SWS
Januszko et al^Citation44	20	F=4	Age range: 18–38	SW=7 SW and ST=13	-	1 Undisturbed night	26	SWS		-	-
Desjardins et al^Citation45	27	F=14	29 (7.6)	SW and/or ST=27	-	1 Undisturbed night	27	SWS		-	-

Notes: The “Sample Characteristics” column reports the description of parasomniac and control group. The “Night Recordings” column details the numbers of experimental night and the description of night protocol. The “Activation Characteristics” column describes the behavioral episodes of NREM parasomnia (BEp) and Non-behavioral arousals (NBEp) features, specifically the number of BEp and the BEp’s onset by sleep stage. *Schenck et al⁴⁰ recruited the 38 subjects’ PSG from a storage room. **Schenck et al⁴⁰ reported that some participants performed 2 consecutive nights while others only 1 night.

Abbreviations: F, female; sd, standard deviation; SW, sleepwalking; ST, sleep terrors; P, parasomniac group; C, control group; SWS, slow wave sleep.

Table 3 Data Analysis

Ref	Channel Analyzed	EEG Variables	Time Window Before Activations		Other Conditions
			Before BEp	Before NBEp
Schenck et al^Citation40	C3	Visual scoring: →Delta wave build-up →Delta wave cluster	0–10 sec 11–30 sec	0–10 sec 11–30 sec	-
Zadra et al^Citation41	Fp1, Fp2, F3, F4, F7, F8, C3, C4, P3, P4, 01, 02, T3, T4, T5, T6, Fz, Cz, Pz	Spectral analysis: FFT →EEG power: - Total (0.75–31.00 Hz) - Delta (0.75–3.75 Hz) - Theta (4.00–7.75 Hz) - Alpha (8.00–12.75 Hz) - Beta (13.00–20.25 Hz - Beta2 (20.50–31.00 Hz)	P -0–60 sec	-	C -60 sec of continuous sleep: sleep stage and cycle matched
Espa et al^Citation20	C3, C4	Spectral analysis: FFT →EEG power: - SWA (0.75–4.50 Hz)	P -whole continuous period of NREM stage 3 –10 min (the mean of SWA value averaged over 2 min) -0–2 min Time course: 10 min (10 epochs of 60 sec)	P -whole continuous period of NREM stage 3 –10 min (the mean of SWA value averaged over 2 min) -0–2 min C -whole continuous 3NREM sleep periods - 10 min (the mean of SWA value averaged over 2 min) -0–2 min	-
Guilleminault et al^Citation34	C4	Spectral analysis: FFT →EEG power: delta: - Low (0.75–2.00 Hz) - High (2.25–4.00 Hz)	Time course: 4–32 sec (7 epochs of 4 sec)	-	-
Pilon et al^Citation35	F3, C3, P3, T3, O1	Visual scoring: →HSD →Delta-wave build-up →Delta-wave cluster.	Time course: 5 min (5 epochs of 60 sec) 0–10 sec 11–30 sec	-	-
Jaar et al^Citation42	Fz, Cz, Pz	Spectral analysis: FFT →EEG power - SWA (0.50–4.00 Hz) - Delta (1.00–4.00 Hz) - Slow delta (0.50–1.00 Hz) Automatical detection -SO:(1) negative peak <−80 μV; (2) peak-to-peak amplitude >180 μV; (3) duration of negative deflection >125 ms and <1500 ms; and (4) duration of positive deflection <1000 ms	0–200 sec 0–32 sec 0–180 sec 0–20 sec	-	-
Perrault et al^Citation43	C3	Spectral analysis: FFT →EEG power: - SWA (0.50–4.00 Hz) - Delta (1.00–4.00 Hz) - Slow delta (0.50–1.00 Hz)	0–32 sec 32 sec–1min 1 min−2 min 2 min–3 min Time course: 1 min (15 epochs of 4 sec)	0–32 sec 32 sec–1min 1 min−2 min 2 min–3 min	-
Januszko et al^Citation44	N=23 localization NS	Spectral analysis: FFT →eLORETA; EEG: -SWA (0.50–4.00 Hz) - Delta (0.50–3.50 Hz) - Theta (3.50–7.50 Hz) - Alpha (7.50–12.50 Hz) - Beta1 (12.50–18.00 Hz) - Beta2 (18.00–24.00 Hz) - Beta3 (24.00–30.00 Hz)	0–4 sec 4–8 sec	-	-
Desjardins et al^Citation45	Functional connectivity: Fp1, Fp2, F3, F4, F7, F8, Fz, C3, C4, Cz, T3, T4, T5, T6, P3, P4, Pz, O1, O2	Spectral analysis: FFT →EEG power: - Delta (0.50–4.00 Hz) - Theta (4.00–8.00 Hz) - Alpha (8.00–12.00 Hz) - Sigma (12.00–14.00 Hz) - Beta1 (14.00–22.00 Hz) - Beta2 (22.00–32.00 Hz) →EEG functional connectivity: - MSC - Icoh	0–20 sec 120–140 sec	-	-

Notes: The first column shows the derivations analyzed. The second column details the analyses performed, the sleep EEG parameters considered and the frequency range. The remained columns report the selected epochs’ duration. The “Other Conditions” column indicates the EEG segment not preceded by BEp or NBEp.

Abbreviations: BEp, behavioral episodes of NREM parasomnias; NBEp, non-behavioral arousals; P, parasomniac group; C, control group; SWA, slow wave activity; SO, slow oscillations; HSD, hypersynchronous delta; FFT, Fast Fourier Transform; NS, not specified; Msc, magnitude-squared coherence; Icoh, imaginary part of the coherence.

Table 4 Main EEG Findings: The Main Results are Divided for EEG Sleep Parameters Investigated

	EEG Investigation	Ref	EEG Finding
Visual scoring	Delta-wave build-up* Delta-wave cluster**	Schenck et al^Citation40	No difference between 0–10 sec and 11–30 sec before BEp and NBEp
		Pilon et al^Citation35	No difference between 0–10 sec and 11–30 sec before the BEp during baseline and recovery nights and as a function of complexity episodes
	Hypersynchronous delta (HSD)***	Pilon et al^Citation35	- Higher HSD prevalence during 5 min before BEp during recovery than baseline night on central leads - No difference in the proportion of BEp preceded by HSD-10 and HSD-30 sec between baseline and recovery nights and as a function of episodes’ complexity on any leads
Quantitative EEG	Slow-wave activity (SWA), delta waves and sub-bands	Espa et al^Citation20	- Higher SWA during 0–2min before BEp than during 10 min and whole NREM sleep stage 3 before BEp -Higher SWA during all time windows before the BEp than the three-time windows before NBEp, in P -No difference between P and C in the mean SWA value before NBEp Time course: significant gradual increase of SWA over the 10 min before BEp
		Guilleminault et al^Citation34	- Higher low delta during 4–8 and 8–12 sec than 28–32 sec before BEp -No difference in higher delta range over the 32 sec before BEp
		Jaar et al^Citation42	- Significant increase in SWA, delta and slow delta over the 32 sec before BEp on the midline - Higher SWA and delta over the 20 sec before BEp than previous 180 sec on Fz and Cz - No difference in slow delta between 20 sec before BEp and previous 180 sec - No significant trend of SWA delta and slow delta over the 200 sec before BEp
		Perrault et al^Citation43	- Higher SWA, delta and slow delta before BEp than NBEp - No difference of SWA, delta and slow delta between the 3 time-windows (0–32 sec; 32 sec–1 min; 1−2 min; 2–3 min) before BEp and NBEp. Time course: - Higher SWA, delta and slow delta during 1 min before BEp than NBEp. - No significant increase of SWA, delta and slow delta over the 1 min before BEp on NBEp.
	Slow Oscillation (SO)	Jaar et al^Citation42	SO density: - Significant linear increase over the 200 sec before BEp on FZ and Cz - Significant linear increase over the 32 sec before BEp on Fz - Higher over the 20 sec before BEp than previous 180 sec, respectively on Fz and Cz SO amplitude: -No significant trend over the 200 sec before BEp - Significant linear increase of SO amplitude over the 32 sec before BEp on FZ - No difference between 20 sec before BEp and previous 180 sec
	Canonical EEG bands	Zadra et al^Citation41	-Higher delta during 60 sec before BEp in P than C, in central and frontal areas - Higher delta in left regions than right frontal areas -Higher delta during most intense ST than less intense
		Desjardins et al^Citation45	-Higher delta during 20 sec before BEp than 20 sec occurring 2 min before BEp on Fz -Higher theta during 20 sec before BEp than 20 sec occurring 2 min before BEp on Fz
	Source Localization (eLoreta)	Januszko et al^Citation44	-Higher beta (24.0–30.0 Hz) during 0–4 sec than 4–8 sec before BEp in 2 voxels (Brodmann area 33 and 24)
	Functional Connectivity	Desjardins et al^Citation45	Msc - No difference between 20 sec before BEp than 20 sec occurring 2 min before BEp ICoh - Lower low delta functional connectivity during 20 sec before BEp than 20 sec occurring 2 min before BEp for parietal and occipital regions -Higher alpha functional during 20 sec before BEp than 20 sec occurring 2 min before BEp connectivity for frontal and parietal regions -Higher beta functional connectivity during 20 sec before BEp than 20 sec occurring 2 min before BEp for fronto-temporal, parietal and occipital regions.

Notes: The visual scoring criteria of the EEG activities in the first row are in according to Schenck et al⁴⁰ and Pilon et al³⁵. *The delta-wave build-up are defined as the highest-amplitude delta wave had to occur in the 10 seconds immediately preceding a BEp, as compared with the previous 11- to 30-second. **The delta-wave cluster is defined as two or more consecutive highest-amplitude delta waves occurring in the 10 seconds immediately preceding a BEp. ***The Hypersynchronous delta (HSD) is defined as the presence of at least 5 seconds of continuous high-voltage (≥ 150 µV) delta waves (1–3 Hz) immediately preceding a BEp. The minimal interval needed without HSD to score two consecutive HSD events was at least 1 second.

Abbreviations: HSD, hypersynchronous delta; BEp, behavioral episodes of NREM parasomnias; NBEp, non-behavioral arousals; P, parasomniac group; C, control group; magnitude-squared coherence; Icoh, imaginary part of the coherence.

Schenck CH, Pareja JA, Patterson AL, Mahowald MW. Analysis of polysomnographic events surrounding 252 slow-wave sleep arousals in thirty-eight adults with injurious sleepwalking and sleep terrors. J Clin Neurophysiol. 1998;15(2):159–166. doi:10.1097/00004691-199803000-00010

 PubMed Web of Science ®Google Scholar

Zadra AL, Nielsen TA. Topographical EEG mapping in a case of recurrent sleep terrors. Dreaming. 1998;8(2):67–74. doi:10.1023/B:DREM.0000005897.62698.1b

 Web of Science ®Google Scholar

Espa F, Ondze B, Deglise P, Billiard M, Besset A. Sleep architecture, slow wave activity, and sleep spindles in adult patients with sleepwalking and sleep terrors. Clin Neurophysiol. 2000;111(5):929–939. doi:10.1016/S1388-2457(00)00249-2

 Web of Science ®Google Scholar

Guilleminault C, Poyares D, Aftab FA, Palombini L. Sleep and wakefulness in somnambulism: a spectral analysis study. J Psychosom Res. 2001;51(2):411–416. doi:10.1016/S0022-3999(01)00187-8

 PubMed Web of Science ®Google Scholar

Pilon M, Zadra A, Joncas S, Montplaisir J. Hypersynchronous delta waves and somnambulism: brain topography and effect of sleep deprivation. Sleep. 2006;29(1):77–84. doi:10.1093/sleep/29.1.77

 PubMed Web of Science ®Google Scholar

Jaar O, Pilon M, Carrier J, Montplaisir J, Zadra A. Analysis of slow-wave activity and slow-wave oscillations prior to somnambulism. Sleep. 2010;33(11):1511–1516. doi:10.1093/sleep/33.11.1511

 PubMed Web of Science ®Google Scholar

Perrault R, Carrier J, Desautels A, Montplaisir J, Zadra A. Electroencephalographic slow waves prior to sleepwalking episodes. Sleep Med. 2014;15(12):1468–1472. doi:10.1016/j.sleep.2014.07.020

 PubMed Web of Science ®Google Scholar

Januszko P, Niemcewicz S, Gajda T, et al. Sleepwalking episodes are preceded by arousal-related activation in the cingulate motor area: EEG current density imaging. Clin Neurophysiol. 2016;127(1):530–536. doi:10.1016/j.clinph.2015.01.014

 Web of Science ®Google Scholar

Desjardins M, Carrier J, Lina J, et al. EEG Functional Connectivity Prior to Sleepwalking: evidence of Interplay Between Sleep and Wakefulness. Sleep. 2017;40(4). doi:10.1093/sleep/zsx024.

 Web of Science ®Google Scholar