Effects Of Hypnagogic Imagery On The Event-Related
Transcription
Effects Of Hypnagogic Imagery On The Event-Related
Effects of Hypnagogic Imagery on the Event-Related Potential to External Tone Stimuli Nanae Michida, MA; Mitsuo Hayashi; PhD Tadao Hori, PhD Department of Behavioral Sciences, Faculty of Integrated Arts and Sciences, Hiroshima University, Higashi-Hiroshima, Japan reaction times than 5000 milliseconds were analyzed. Electroencephalograms were recorded from Fz, Cz, Pz, Oz, T5 and T6. There were no differences in reaction times and electroencephalogram spectra between the conditions of with and without hypnagogic imagery. These results indicated that the arousal levels were not different between the 2 conditions. On the other hand, the N550 amplitude of the event-related potentials in the imagery condition was lower than in the no-imagery condition. Conclusions: The decrease in the N550 amplitude in the imagery condition showed that experiences of hypnagogic imagery exert some influence on the information processes of external tone stimuli. It is possible that the processing of hypnagogic imagery interferes with the processing of external stimuli, lowering the sensitivity to external stimuli. Keywords: Event-related potential, Hypnagogic imagery, N550 Citation: Michida N; Hayashi M; Hori T. Effects of hypnagogic imagery on the event-related potential to external tone stimuli. SLEEP 2005;28(7): 813-818. Study Objectives: The purpose of this study was to examine the influence of hypnagogic imagery on the information processes of external tone stimuli during the sleep onset period with the use of event-related potentials. Design: Event-related potentials to tone stimuli were compared between conditions with and without the experience of hypnagogic imagery. To control the arousal level when the tone was presented, a certain criterion named the electroencephalogram stage was used. Stimuli were presented at electroencephalogram stage 4, which was characterized by the appearance of a vertex sharp wave. Setting: Data were collected in the sleep laboratory at Hiroshima University. Participants: Eleven healthy university and graduate school students participated in the study. Interventions: N/A. Measurements and Results: Experiments were performed at night. Reaction times to tone stimuli were measured, and only trials with shorter is perceived. Components of event-related potentials (ERPs) are useful to examine the information processing of external tone stimuli because these reflect intracerebral information processes. Concerning previous studies about ERPs during the sleep-onset period, changes of ERPs influenced by declines in the arousal level, variation of stimulus frequency, or differences of the task load have been reported.6-14 However, there are no reports on the relationship between hypnagogic imagery and ERPs. Comparison of ERPs to external tone stimuli between the conditions with and without hypnagogic imagery makes it possible to estimate the influence of hypnagogic imagery on the information processing of tone stimuli. It must be noted that the amplitude of the ERP components changes with the fluctuation of the arousal level. According to a review of ERPs during the sleep-onset period,14 amplitudes of the negative wave peaking at 100 milliseconds (N100) and the positive component peaking around 300 milliseconds (P300) gradually decrease as the arousal level becomes lower. Apparent diminution of these 2 components is observed when the subject no longer signals detection of the external stimulus. On the other hand, P200 may increase during the sleep-onset period. The decrease in N100 and the increase in P200 have been explained by the removal of a long-lasting processing negativity associated with attention and consciousness in the waking state. During late stage 1 sleep of the standard sleep criteria (provided by Rechtschaffen & Kales),15 N300 begins to emerge. And finally, in standard stage 2 sleep, which is regarded as definitive sleep, the large N550-P900 components of the K-complex become clearly visible. Therefore, it is necessary to control the arousal level when tone stimuli are presented to investigate differences in the processing of tone stimuli between the presence and absence of imagery. To objectively judge the arousal level during the sleep- INTRODUCTION IT IS KNOWN THAT SIMILAR PHENOMENA TO DREAMS ARISE DURING THE PERIOD OF TRANSITION FROM WAKEFULNESS TO NON-RAPID EYE MOVEMENT (NREM) SLEEP. This dream-like phenomenon during the sleep-onset period is called hypnagogic imagery. The usual way experimental studies regarding hypnagogic imagery are performed is to awaken a dozing subject and discuss his or her mental experiences that occurred before awakening. However, this method relies on the introspection of the subjects. Therefore, a psychophysiologic method is needed to more objectively study hypnagogic imagery. Although there are several reports on the functional activity of the brain immediately before waking with imagery during the sleeponset period using spectral analysis of electroencephalogram (EEG) records,1-5 these studies do not show a common view corresponding to the presence of imagery. Therefore, it seems worthwhile for intracerebral and intercerebral information processing of hypnagogic imagery to be investigated from another point of view. It is thought that the processing of hypnagogic imagery has an influence on other information processes when imagery Disclosure Statement This was not an industry supported study. Drs. Michida, Hayashi, and Hori have indicated no financial conflicts of interest. Submitted for publication December 2003 Accepted for publication February 2005 Address correspondence to: Tadao Hori PhD, Department of Behavioral Sciences, Faculty of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima, 739-8521, Japan. Tel: +81-82-424-6580; Fax: +81-82-424-0759. E-mail: tdhori@hiroshima-u.ac.jp SLEEP, Vol. 28, No. 7, 2005 813 Effects of Hypnagogic Imagery on the ERP—Michida et al onset period, a certain criterion, named the EEG stage, has been proposed.3,16,17,18 This criterion divides the sleep-onset period into 9 stages based on the typical appearance of EEG as declining with the arousal level. Hori et al3 used a 5-stage simplified version of this criterion (Figure 1) to analyze the occurrence rate of hypnagogic imagery for each EEG stage. According to their study, the average recall rates of hypnagogic imagery for each EEG stage showed an inverse U-shaped distribution. The recall rate at EEG stage 3 was the highest, followed by stage 2 after stage 4. In this study, EEG stage 4 of the Hori et al criteria3 was used because there seemed to be a good possibility of obtaining both “with-imagery” and “without-imagery” samples. The purpose of this study was to examine the influence of hypnagogic imagery on the information processing of external tone stimuli with the use of ERPs. It has been hypothesized that ERPs to external tone stimulus show some differences between the 2 cases of the presence and absence of hypnagogic imagery. It must be noted that the fluctuation of the arousal level affects the ERP amplitudes. Thus, EEG signals just before each tone stimulus were subjected to spectral analysis to make sure that the arousal levels during the stimulus-presentation period were not different between the conditions of with and without hypnagogic imagery. pended on the progress of sleep onset of the subjects, though the minimum time between the stimuli was more than 30 seconds. Procedure Subjects were tested in a bed in a dark, electrically shielded, 2950×2800×2200 room. They were instructed to sleep if they became drowsy but to press the microswitch button taped to their right hand as soon as possible whenever they heard tones. They were also instructed to explain in detail what they experienced immediately before pressing the button upon having a cue tone signal in every trial. They were requested to use one of the following words to explain their experiences: “saw,” “heard,” “felt,” “thought,” “forgot,” and “nothing.” These words were used to categorize their mentations. To control the arousal level when the pip-tone stimuli were presented, the 5 EEG-stage scoring system for the sleep-onset period3 was used. The EEG from Cz for 5 seconds just before the tone stimuli was used for the determination of the EEG stage. Tone stimuli were presented at EEG stage 4, which was characterized by the appearance of a well-defined vertex sharp wave. Subjects were awakened at each trial because they were required to report their mentations. Thus, the process of falling asleep was repeated again and again during the experiment. After the experiments, the EEG stages of tone-presented trials were scored again, and the trials that were confirmed as EEG stage 4 were used for further analysis. If a K-complex was evoked by a tone stimulus, the trial was not regarded as EEG stage 4 because the stage is defined as a part of sleep stage 1 of the standard criteria (provided by Rechtschaffen & Kales).15 According to the standard sleep criteria, the K-complex is one of the characteristics of sleep stage 2. Experiments performed were excluded when the number of tones sounded reached 200 or when the tone-presenting period lasted longer than 2 hours. When the number of adoptable trials for each condition did not reach 20 times, which was the minimum number of trials to determine ERPs, additional trials were made on another night. Reaction times to tone stimuli were measured with a microswitch button. Only those trials with a shorter reaction time than 5000 milliseconds were analyzed. Two seconds after the press of the button, a tone stimulus (1,500 Hz, 60 dB SPL, 1 second) was given to subjects as a cue to report their hypnagogic mentations. Based on the report, each trial was divided into 2 categories for analysis: imagery and no imagery. All trials of every experiment were categorized by 1 experimenter. There were some trials that were excluded from the analysis. It has been reported that visual imagery is included in the majority of experiences in hypnagogic imagery.3,19-21 Therefore, only trials with visual imagery were categorized as the imagery condition to control the homogeneity of imagery experiences. Trials with auditory or kinesthetic imagery without visual imagery were excluded from the analysis. When subjects did not recall details of their mental experiences, the trial was also excluded from analysis. Meanwhile, trials with no mental experience and logical or illogical thought without clear imagery were categorized as the no-imagery condition. METHODS Subjects Eleven university and graduate school students (3 men and 8 women) between the ages of 18 and 25 years (mean=21.3 years) participated in this study. They were screened for health and sleep problems. All of them were right handed and had some experience with sleep experiments. Informed consent was obtained. Stimuli Pip-tone stimuli (1,000 Hz, 60 dB SPL, 50 milliseconds) were presented from a speaker set up 1.4 meters above a pillow. The stimuli were manually presented by the experimenter under the condition as follows. Each tone stimulus was produced within 5 seconds of the appearance of a well-defined vertex sharp wave in EEG from Cz that appeared more than 30 seconds after the preceding stimulus. Therefore, the length of the stimulus interval de- EEG Recording Figure 1—Representative electroencephalogram (EEG) patterns for 5 electroencephalographic stages and correspondence to standard sleep stages. SLEEP, Vol. 28, No. 7, 2005 EEGs were recorded from Fz, Cz, Pz, Oz, T5, and T6 with AgAgCl surface electrodes referred to linked earlobes with the forehead as the ground. Electrooculogram recordings were obtained 814 Effects of Hypnagogic Imagery on the ERP—Michida et al from electrodes affixed at the corner of both eyes referred to the ipsilateral earlobes for horizontal eye movements and attached to the supraorbital and infraorbital positions of the left eye, referred to each other for vertical eye movement. A time constant of 3.2 seconds was used for both EEG and electrooculogram recordings. An electromyogram was recorded from surface electrodes placed on the chin (mentalis), referred to each other. The time constant for EMG was 0.03 seconds. In all recordings, 120-Hz high cut-off filtering was used and interelectrode impedances were kept below 5 KΩ. All electrophysiologic parameters were simultaneously recorded on an 18-channel polygraph (Model 1A97, NEC San-Ei, Tokyo, Japan) and a 14-channel FM tape recorder (SR-50, TEAC, Tokyo, Japan). Statistical Analysis A 2-tailed paired t test was used for comparing the reaction times between the 2 conditions: imagery and no imagery. Mean amplitudes of EEG frequency bands and peak amplitudes of ERP components were analyzed using a 2-way repeated measures analysis of variance. The independent variables were condition and electrode site. Significant levels were determined following the adjusted Greenhouse-Geisser approach for repeated observations.22 As for the posthoc test, all comparisons between individual cell means were performed using the Newman-Keuls procedure. All statistical significances of comparisons were based on a .05 level of confidence. RESULTS EEG Spectrum Analysis Rate of Imagery and Reaction Time A signal processor (Model 7T18A, NEC San-Ei) was used for the subsequent off-line analysis of EEG data reproduced by the FM recorder. EEGs were recorded during a 5000-milliseconds epoch prior to each stimulus tone. Autopower spectra with a 0.2Hz resolution were computed using a fast Fourier transform and smoothed with a Hanning window. Spectra that averaged more than 20 epochs, which corresponded to trials used for ERP calculation, were respectively computed for each condition. The average amplitudes (root power) for EEG frequency bands, delta (2.43.4 Hz) theta (3.6-7.4 Hz), alpha (7.6-13.4 Hz), beta (13.6-20.0 Hz) and sigma (13.0-14.8 Hz) were computed from each EEG channel. The average hit rate to tone stimuli was 96.9% (SEM=1.60%). Only trials with a behavioral response to tone were analyzed after this. The average frequencies and rates of hypnagogic experiences across subjects were as follows: Imagery: 65.5 trials (SEM=15.90), 54.1%; no imagery: 38.6 trials (SEM=6.84), 38.2%; others: 8.0 trials (SEM=1.65), 7.7%. Mean reaction times were not significantly different between the 2 conditions (imagery: 891.6 milliseconds, SEM=118.62 milliseconds; no imagery: 905.1 milliseconds, SEM=116.88 milliseconds). FFT Analysis Figure 2 shows the EEG spectra in the last 5000 milliseconds before the tone. The spectra of both conditions almost overlap each other at every site. Average amplitudes of each EEG frequency band were statistically analyzed. For all frequency bands, only the main effects of the electrode sites were significant, but significant differences between the conditions were not seen at every site. ERP Analysis Averaging over 20 times for ERP analysis was performed on each condition for EEG signals from 200 milliseconds before to 1,500 milliseconds after each stimulus tone at a 5-millisecond sampling rate. Peak amplitudes of the ERP components were measured from the baseline, which was determined as the mean voltage during the last 200 milliseconds prior to the tone. The peak latency windows of ERP were defined as follows: N100: 75150 milliseconds, P200: 150-250 milliseconds, N300: 200-400 milliseconds, P400: 300-500 milliseconds, N550: 400-750 milliseconds, and P900: 750-1200 milliseconds. ERP Analysis Figure 3 presents the grand average ERPs across all subjects at each site. Clear peaks of the P900 component did not appear at every site, although a slow positive potential, which followed N550 and did not return to the baseline, was observed at Fz and Table 1—Peak Amplitudes of Event-Related Potential Components Fz N100 P200 N300 P400 N550 Imagery -4.38 (1.18) 11.08 (2.37) -20.22 (3.50) -15.08 (5.23) -21.58 (5.67) Noimagery -3.68 (1.14) 11.96 (1.71) -20.70 (3.93) -20.21 5.11) -27.88* (5.48) Cz Imagery -6.69 (1.66) 13.70 (2.09) -22.13 (3.89) -2.28 (5.92) -7.62 (5.51) Noimagery -5.54 (1.33) 15.64 (1.93) -23.12 (4.50) -5.91 (5.08) -13.17* (4.99) Pz Imagery -4.90 (0.96) 12.65 (1.48) -10.41 (3.55) 15.25 (4.60) -3.69 (3.61) Oz Noimagery -4.02 (1.28) 13.96 (1.60) -11.61 (3.86) 10.78 (3.49) -7.35* (2.73) Imagery -2.31 (0.59) 6.71 (1.80) -0.91 (1.87) 18.57 (2.87) -10.15 (2.80) Noimagery -1.26 (0.88) 7.52 (1.51) -1.68 (1.92) 16.44 (2.05) -10.57 (1.96) T5 NoImagery imagery -1.13 -0.90 (0.40) (0.44) 3.35 3.71 (0.99) (0.68) -2.36 -3.28 (1.29) (1.13) 10.40 8.00 (2.39) (1.97) -6.94 -8.62 (2.05) (1.43) T6 NoImagery imagery -0.98 -0.69 (0.58) (0.87) 2.79 3.91 (1.07) (1.15) -3.64 -3.61 (1.66) (1.38) 9.95 8.26 (2.17) (1.93) -9.41 -10.19 (2.01) (1.81) Data are presented as mean (SEM) in 11 subjects. *Statistically significant at P<.05. SLEEP, Vol. 28, No. 7, 2005 815 Effects of Hypnagogic Imagery on the ERP—Michida et al Figure 3—Total averages of event-related potentials across all subjects. Black lines are the event-related potentials for the imagery condition. Gray lines are the event-related potentials for the no-imagery condition. onset period vary their amplitudes with the decline in arousal level. To put it concretely, N100 and P300 decrease in amplitude while P200 and N300 increase throughout the transitional period from arousal to definitive sleep. If experiences of hypnagogic imagery are associated with arousal level, it would be expected that each ERP component in the imagery condition would show a distinctive feature that reflects the difference of the arousal level. ERP components preceding N550 indicated that the arousal level did not differ between the with- and without-imagery conditions. This was supported by the results of the behavioral reaction time and fast Fourier transform analysis mentioned above. On the other hand, N550 amplitudes in the imagery condition were observed to be smaller than those in the no-imagery condition at Fz, Cz and Pz. The differences in ERPs between the with- and without-imagery conditions showed that experiences of hypnagogic imagery during the sleep-onset period exerted some influence on the information processes of external tone stimuli. The N550 amplitude was the largest at Fz as a main effect of the site. That is, the difference of the N550 amplitude between the conditions appeared where N550 was dominant. Using a loudspeaker as the stimulus-input medium might have produced a less-constant tone to the subject’s ear than using earphones. However, the difference between these 2 conditions appeared only in 1 component in spite of the emergence of various components in the ERPs. Therefore, the difference of N550 can be explained by the influence of imagery rather than by the position of the ear. N550 is regarded as one of the major components of the Kcomplex, along with an earlier N300 and a later P900.6,13,23-35 The K-complex occurs in the non-rapid eye movement sleep state at standard sleep stage 2 or deeper. EEG stage 4, at which the tone was presented in this study, is included in standard sleep stage 1. In fact, the detection rate of the stimuli was more than 96%. This provided evidence that EEG stage 4 trials in this study did not enter standard sleep stage 2, regarded as definitive sleep. Therefore, the N550 of this study is probably not a component of the K-complex, or at least the K-complex defined as the negativepositive complex that can only be elicited in definitive sleep. This EEG stage 4 should not show the K-complex; however, it was reported that the appearance of N550 was already observed at EEG stage 2 of the simplified 5-stages criterion and then grew in proportion as the arousal level declined.7,8 According to Peszka Figure 2—Electroencephalogram spectra averaged across all subjects. Black lines are the spectra for the imagery condition. Gray lines are the spectra for the no-imagery condition. Cz. Table 1 shows the mean peak amplitudes of all subjects. Amplitudes of 5 components except P900 were statistically analyzed. All components, with the exception of N550, only showed the significant main effect of the sites but no main effect for the conditions or interactive effect. For the N550 amplitudes, both main effects of the sites and conditions were found to be significant. A significant effect of conditions (F1,10=9.74, P<.05) indicated that the amplitude in the imagery condition (-9.90µV) was smaller than that in the no-imagery condition (-12.96µV). A significant interaction effect was also observed (F5,50=4.20, ε=0.284, P<.05). Newman-Keuls comparisons between conditions showed significant differences at Fz, Cz, and Pz. At these sites, N550 amplitudes in the imagery condition (Fz: -21.58, Cz: -7.62, Pz: -3.69µV) were smaller than those in the no-imagery condition (Fz: -27.88, Cz: -13.17, Pz: -7.35 µV). DISCUSSION Reaction Time and FFT Analysis The behavioral reaction time and the EEG power spectrum are well known as indicators of fluctuations of the arousal level. In this study, significant differences in the reaction times between the with- and without-imagery conditions were not seen. On the other hand, the mean amplitudes of all frequency bands showed a significant main effect only of the sites but no main effect of the conditions or interactive effect. It follows from the results of reaction time and fast Fourier transform analysis that arousal levels of behavior and EEG did not differ between the 2 conditions (with and without imagery). ERP Analysis All observed components except N550 did not show significant differences between the conditions of with and without imagery. According to previous studies, ERP components during the sleepSLEEP, Vol. 28, No. 7, 2005 816 Effects of Hypnagogic Imagery on the ERP—Michida et al cognitive activity. Sallinen et al41 suggested that the threshold of perceiving external stimuli should be higher during phasic than tonic rapid eye movement sleep because of immersion in internal mental activity (dreaming). The function of hypnagogic imagery is unknown but very interesting. From the difference in N550 amplitude according to the condition, it can be said that the sleep-protective mechanism against the arousal associated with the processing of tone stimuli was weakened when hypnagogic imagery was experienced. However, the behavioral reaction times in these 2 conditions were not different. That is, the tolerance to the disturbance of sleep while experiencing hypnagogic imagery did not differ from that without imagery in spite of a lower function of the sleep-protective mechanism reflected in the N550. This led to the conjecture that an allocation of cognitive-processing resources to hypnagogic imagery during the sleep-onset period should support a smooth transition from wakefulness to sleep. If hypnagogic imagery has the role of sleep protection from arousal associated with the processing of external stimuli, it is no wonder that the sleep-protective mechanism reflected by the N550 was more evident in the no-imagery condition to compensate for the role of imagery. and Harsh,36 N550 was evident in waking EEG state trials, sleep stage 1 trials and without K-complex trials in sleep stage 2. They stated that the N550 and K-complex may be closely related but are separable phenomena. These previous studies indicated that the appearance of N550 in this study is possible. On the other hand, Colrain et al.13 did not report the appearance of N550 in sleep stage 1, which was divided into alpha and theta divisions, although their stage 1-theta division was similar to this study in respect to the vertex sharp wave emergence. This contradiction of the N550 emergence in sleep stage 1 can be explained by the different ways of arousal level division. Sleep stage 1 is a transition period from wakefulness to sleep and its state rapidly varies. For example, stage 1-theta of the Colrain group surely included stage 3 and 4 of the simplified 5-stage EEG criterion. EEG stage 4 is even later sleep stage 1, just prior to stage 2, rather than EEG stage 3. Another explanation is the differences in the properties of the stimulus presentations. The tone is probably more salient in the single tone paradigm, in which the stimulus frequency may be lower, than in the odd-ball paradigm. It is still unclear whether the N550 at EEG stage 4 of this study (in standard sleep stage 1) is related to the K-complex or not, and this requires further investigation. What brought about the difference in the N550 amplitude between the two conditions should be considered. According to recent studies, delta frequency large waveforms, such as the N550 and K-complex, is a phasic manifestation of slow wave sleep pressure and reflects the “sleep protective” mechanism.35-38 This theory, that the underlying mechanism facilitates the initiation and maintenance of sleep, can be applied to explain why N550 increased accompanied by the progress of sleep in previous studies.7,8,9,39 Concerning the results of the present study, it was interpreted that the arousal associated with the processing of tone stimuli in the no-imagery condition was blunter than in the imagery condition. In the imagery condition, the sleep protective mechanism was weaker than in the no-imagery condition. According to previous studies of auditory ERP in non-rapid eye movement sleep, the N550 amplitude becomes larger when the frequency of stimuli presentation is lower,13,23-25,39 when deviance from standard stimuli is larger,25-27 and when the button press task of reacting to stimuli is set.24,39 These stimuli can be rephrased as physically and/or psychologically salient stimuli. That is, the sleep-protective mechanism reflected in N550 is strengthened when external stimuli are salient to facilitate the initiation and maintenance of sleep. In this study, the N550 reflecting this mechanism was smaller in the imagery than in the no-imagery condition; therefore, it can be considered that the same tone was less prominent when imagery was perceived. If so, the reason why the sensitivity to external tone stimuli was lower in the imagery condition than in the no-imagery condition should be clarified. Although the relationship between internal mental activity and physiologic sleep-protective mechanisms such as N550 has not yet been sufficiently clarified in this study, the possibility that internal processes related to the experience of hypnagogic imagery attenuate the sensitive response to external stimuli was observed. It can be considered that a part of the resources for cognitive processes at EEG stage 4 is allocated to hypnagogic imagery, resulting in the allocation of processing resources to the tone stimuli being diminished. This idea is neither unusual nor unexpected. Burton et al40 indicated that the reduced responsiveness to external stimulation during sleep is, at least in part, due to ongoing SLEEP, Vol. 28, No. 7, 2005 CONCLUSION In this study, we investigated how hypnagogic imagery influenced the information processes of external tone stimuli in the sleep-onset period. The behavioral results of button pressing did not differ between the with- or without-imagery conditions. Also, there was no difference in the EEG spectral indexes between whether or not hypnagogic imagery was experienced. Based on these behavioral and physiologic results, it can be said with fair certainty that there was no difference in the arousal level during the periods when stimuli were presented between the 2 conditions—with hypnagogic imagery and without hypnagogic imagery. On the other hand, in ERP analysis, the N550 amplitudes at Fz, Cz, and Pz in the imagery condition were lower than in the noimagery condition. The results show that experiences of hypnagogic imagery during the sleep-onset period exert some influence on information processes to external tone stimuli. It is possible that the underlying sleep-protective mechanism is weaker when hypnagogic imagery is experienced than when not. 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