- Email: [email protected]
Current sources of the brain potentials before rapid eye movements in human REM sleep
International Congress Series 1270 (2004) 241 – 244
www.ics-elsevier.com
Current sources of the brain potentials before rapid eye movements in human REM sleep Takashi Abe, Hiroshi Nittono, Tadao Hori * Department of Behavioral Sciences, Faculty of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima 739-8521, Japan
Abstract. In a previous study, we reported that rapid eye movements (REMs) in REM sleep were not preceded by the presaccadic positivity commonly observed before saccades in wakefulness but by a slow negative potential we called pre-REM negativity. In the present study, we examined current sources of the presaccadic positivity and pre-REM negativity using low resolution brain electromagnetic tomography (LORETA). Fourteen young healthy volunteers participated in the study. Brain potentials were recorded from 26 scalp sites and time-locked to the onsets of saccades and REMs during a visually triggered saccade task and natural nocturnal sleep. Current sources of the presaccadic positivity were estimated to be in the bilateral medial frontal gyrus, whereas those of the pre-REM negativity were estimated to be in the right amygdala, right parahippocampal gyrus, and left orbital gyrus. Different sources of these potentials give further support to the idea that different neural processes are responsible for saccades and REMs. Moreover, the findings that current sources of the pre-REM negativity were estimated to be in the limbic part of the brain suggests that this negativity might be associated with memory and emotional processing in REM sleep. D 2004 Elsevier B.V. All rights reserved. Keywords: Presaccadic positivity; Pre-REM negativity; Electroencephalography; Event-related potentials; LORETA
1. Introduction Rapid eye movements (REMs) are one of the prominent features of REM sleep. The similarities and differences between saccades in wakefulness and REMs in REM sleep have been under debate [1]. In wakefulness, scalp-recorded electroencephalogram (EEG) studies have revealed that the presaccadic positivity, which reflects the oculomotor planning process, appears 100 –250 ms before the onset of saccades with a centro-parietal scalp distribution [2,3]. In a previous study, we found no presaccadic positivity but a slow negative potential (pre-REM negativity) before REMs in REM sleep [4]. The latter negativity had a prefrontal distribution and was larger in the right hemisphere. These * Corresponding author. Tel.: +81-82-424-6580; fax: +81-82-424-0759. E-mail address: [email protected] (T. Hori). 0531-5131/ D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.ics.2004.04.092
242
T. Abe et al. / International Congress Series 1270 (2004) 241–244
findings suggest that the generation of REMs does not involve the cortical process reflected in the presaccadic positivity but is associated with a different neural process probably reflected in the pre-REM negativity. In the present study, we examined current sources of the presaccadic positivity and pre-REM negativity using low resolution brain electromagnetic tomography (LORETA) [5]. 2. Methods We reanalyzed the data of our previous study; Abe et al. [4] described the procedure in details. Fourteen young healthy volunteers (7 women and 7 men, mean 22.8 years old) gave informed consent and participated in the study. Brain potentials associated with horizontal saccades and REMs were recorded during a visually triggered saccade task and natural nocturnal sleep after an adaptation night. EEG was recorded from 26 scalp sites (Fp1, Fp2, F3, F4, C3, C4, P3, P4, O1, O2, F7, F8, T7, T8, P7, P8, F9, F10, P9, P10, Fpz, Fz, Cz, Pz, POz, and Oz according to the extended 10 – 20 system). Electrooculogram (EOG) and submental electromyogram (EMG) were recorded simultaneously. The sampling rate was 1000 Hz. Time constants were 5.0 s for EEG and EOG and 0.03 s for EMG. High cut filter was set at 300 Hz. In the sleep session, only the periods scored as stage REM according to Rechtschaffen and Kales criteria [6] with Hori et al. supplements and amendments [7] were analyzed. EEG in the period 200 ms before and 50 ms after the onset of each eye movement were averaged. The first 50 ms of the average period was taken as a baseline. LORETA was used to estimate current source densities of the presaccadic positivity and pre-REM negativity using the mean amplitude of the period between 150 and 20 ms before eye movements. These values were compared with zero using voxel-wise paired t tests. The resultant t values were projected into LORETA images. Correction for multiple comparisons was performed via randomization using statistical non-parametric mapping (SnPM). Corrected p values are reported. 3. Results Fig. 1 shows the current sources of the presaccadic positivity and pre-REM negativity estimated by LORETA. In wakefulness, current sources of the presaccadic positivity were estimated in the bilateral medial frontal gyrus (BA 6), ts (13) = 9.3 and 9.3, p < 0.05, for the left and right hemispheres, respectively. In REM sleep, current sources of the pre-REM negativity were estimated in the right amygdala, right parahippocampal gyrus (BA 37), and left orbital gyrus (BA 11). The largest t value was found in the right amygdala and right parahippocampal gyrus, ts (13) = 11.9 and 11.9, p < 0.05, respectively, and the second largest t value was found in the left orbital gyrus, t (13) = 11.4, p < 0.05. 4. Discussion The presaccadic positivity and pre-REM negativity showed different current sources. This result gives further support to the idea that different neural processes are responsible for saccades in wakefulness and REMs in REM sleep [4,8].
T. Abe et al. / International Congress Series 1270 (2004) 241–244
243
Fig. 1. Current sources of the presaccadic positivity and pre-REM negativity calculated using LORETA. Upper and lower panels show current sources of the presaccadic positivity and pre-REM negativity, respectively. Left panels show grand mean waveforms time-locked to the onsets of saccades and REMs. Recording sites were the parietal midline (Pz) and prefrontal midline (Fpz) sites, respectively, referenced to digitally linked earlobes. Vertical axes indicate the onset of eye movements. Solid and open triangles indicate the presaccadic positivity and pre-REM negativity, respectively.
The presaccadic positivity had its origin in the bilateral medial frontal gyrus. The current sources of the presaccadic positivity calculated in this study were located in somewhat upper regions above the supplementary eye fields (SEF) observed in fMRI studies [9,10]. However, considering the relatively small number of electrodes used in this study (26 sites), the current sources of the presaccadic positivity estimated in the present study might be bilateral SEFs. In REM sleep, current sources of the pre-REM negativity were identified in the right amygdala, right parahippocampal gyrus, and left orbital gyrus. Functional imaging studies using positron emission tomography have revealed that the activations of the amygdala associated with REM sleep [11] and the right parahippocampal gyrus correlated positively with the number of REMs [12,13]. Magnetoencephalographic study showed activation in the right amygdala, right parahippocampal gyrus, and left orbitofrontal cortex in the last 100 ms before REMs [14]. Our estimation using LORETA is consistent with these
244
T. Abe et al. / International Congress Series 1270 (2004) 241–244
findings and suggests that the pre-REM negativity reflects the activity that occurred in the limbic part of the brain and is possibly associated with memory and emotional processing in REM sleep. Acknowledgements This study was supported by a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (No. 14201011). References [1] J.A. Hobson, E.F. Pace-Schott, R. Stickgold, Dreaming and the brain: toward a cognitive neuroscience of conscious states, Behav. Brain Sci. 23 (6) (2000) 793 – 842. [2] S. Everling, P. Krappmann, H. Flohr, Cortical potentials preceding pro- and antisaccades in man, Electroencephalogr. Clin. Neurophysiol. 102 (4) (1997) 356 – 362. [3] J.E. Richards, Cortical sources of event-related potentials in the prosaccade and antisaccade task, Psychophysiology 40 (6) (2003) 878 – 894. [4] T. Abe, et al., Lack of presaccadic positivity before rapid eye movements in human REM sleep, NeuroReport 15 (4) (2004) 735 – 738. [5] R.D. Pascual-Marqui, C.M. Michel, D. Lehmann, Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain, Int. J. Psychophysiol. 18 (1) (1994) 49 – 65. [6] A. Rechtschaffen, A. Kales, A manual of standardized terminology, techniques and scoring system for sleep stage of human subjects, UCLA, Brain Information Service/Brain Research Institute, Los Angeles, 1968. [7] T. Hori, et al., Proposed supplements and amendments to ‘A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects’ the Rechtschaffen and Kales (1968) standard, Psychiatry Clin. Neurosci. 55 (3) (2001) 305 – 310. [8] G. Vanni-Mercier, et al., Eye saccade dynamics during paradoxical sleep in the cat, Eur. J. Neurosci. 6 (8) (1994) 1298 – 1306. [9] B. Luna, et al., Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study, Cereb. Cortex 8 (1) (1998) 40 – 47. [10] M.H. Grosbras, et al., An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging, Cereb. Cortex 9 (7) (1999) 705 – 711. [11] P. Maquet, et al., Functional neuroanatomy of human rapid-eye-movement sleep and dreaming, Nature 383 (6596) (1996) 163 – 166. [12] A.R. Braun, et al., Dissociated pattern of activity in visual cortices and their projections during human rapid eye movement sleep, Science 279 (5347) (1998) 91 – 95. [13] P. Peigneux, et al., Generation of rapid eye movements during paradoxical sleep in humans, NeuroImage 14 (3) (2001) 701 – 708. [14] A.A. Ioannides, et al., MEG tomography of human cortex and brainstem activity in waking and REM sleep saccades, Cereb. Cortex 14 (1) (2004) 56 – 72.
www.ics-elsevier.com
Current sources of the brain potentials before rapid eye movements in human REM sleep Takashi Abe, Hiroshi Nittono, Tadao Hori * Department of Behavioral Sciences, Faculty of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima 739-8521, Japan
Abstract. In a previous study, we reported that rapid eye movements (REMs) in REM sleep were not preceded by the presaccadic positivity commonly observed before saccades in wakefulness but by a slow negative potential we called pre-REM negativity. In the present study, we examined current sources of the presaccadic positivity and pre-REM negativity using low resolution brain electromagnetic tomography (LORETA). Fourteen young healthy volunteers participated in the study. Brain potentials were recorded from 26 scalp sites and time-locked to the onsets of saccades and REMs during a visually triggered saccade task and natural nocturnal sleep. Current sources of the presaccadic positivity were estimated to be in the bilateral medial frontal gyrus, whereas those of the pre-REM negativity were estimated to be in the right amygdala, right parahippocampal gyrus, and left orbital gyrus. Different sources of these potentials give further support to the idea that different neural processes are responsible for saccades and REMs. Moreover, the findings that current sources of the pre-REM negativity were estimated to be in the limbic part of the brain suggests that this negativity might be associated with memory and emotional processing in REM sleep. D 2004 Elsevier B.V. All rights reserved. Keywords: Presaccadic positivity; Pre-REM negativity; Electroencephalography; Event-related potentials; LORETA
1. Introduction Rapid eye movements (REMs) are one of the prominent features of REM sleep. The similarities and differences between saccades in wakefulness and REMs in REM sleep have been under debate [1]. In wakefulness, scalp-recorded electroencephalogram (EEG) studies have revealed that the presaccadic positivity, which reflects the oculomotor planning process, appears 100 –250 ms before the onset of saccades with a centro-parietal scalp distribution [2,3]. In a previous study, we found no presaccadic positivity but a slow negative potential (pre-REM negativity) before REMs in REM sleep [4]. The latter negativity had a prefrontal distribution and was larger in the right hemisphere. These * Corresponding author. Tel.: +81-82-424-6580; fax: +81-82-424-0759. E-mail address: [email protected] (T. Hori). 0531-5131/ D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.ics.2004.04.092
242
T. Abe et al. / International Congress Series 1270 (2004) 241–244
findings suggest that the generation of REMs does not involve the cortical process reflected in the presaccadic positivity but is associated with a different neural process probably reflected in the pre-REM negativity. In the present study, we examined current sources of the presaccadic positivity and pre-REM negativity using low resolution brain electromagnetic tomography (LORETA) [5]. 2. Methods We reanalyzed the data of our previous study; Abe et al. [4] described the procedure in details. Fourteen young healthy volunteers (7 women and 7 men, mean 22.8 years old) gave informed consent and participated in the study. Brain potentials associated with horizontal saccades and REMs were recorded during a visually triggered saccade task and natural nocturnal sleep after an adaptation night. EEG was recorded from 26 scalp sites (Fp1, Fp2, F3, F4, C3, C4, P3, P4, O1, O2, F7, F8, T7, T8, P7, P8, F9, F10, P9, P10, Fpz, Fz, Cz, Pz, POz, and Oz according to the extended 10 – 20 system). Electrooculogram (EOG) and submental electromyogram (EMG) were recorded simultaneously. The sampling rate was 1000 Hz. Time constants were 5.0 s for EEG and EOG and 0.03 s for EMG. High cut filter was set at 300 Hz. In the sleep session, only the periods scored as stage REM according to Rechtschaffen and Kales criteria [6] with Hori et al. supplements and amendments [7] were analyzed. EEG in the period 200 ms before and 50 ms after the onset of each eye movement were averaged. The first 50 ms of the average period was taken as a baseline. LORETA was used to estimate current source densities of the presaccadic positivity and pre-REM negativity using the mean amplitude of the period between 150 and 20 ms before eye movements. These values were compared with zero using voxel-wise paired t tests. The resultant t values were projected into LORETA images. Correction for multiple comparisons was performed via randomization using statistical non-parametric mapping (SnPM). Corrected p values are reported. 3. Results Fig. 1 shows the current sources of the presaccadic positivity and pre-REM negativity estimated by LORETA. In wakefulness, current sources of the presaccadic positivity were estimated in the bilateral medial frontal gyrus (BA 6), ts (13) = 9.3 and 9.3, p < 0.05, for the left and right hemispheres, respectively. In REM sleep, current sources of the pre-REM negativity were estimated in the right amygdala, right parahippocampal gyrus (BA 37), and left orbital gyrus (BA 11). The largest t value was found in the right amygdala and right parahippocampal gyrus, ts (13) = 11.9 and 11.9, p < 0.05, respectively, and the second largest t value was found in the left orbital gyrus, t (13) = 11.4, p < 0.05. 4. Discussion The presaccadic positivity and pre-REM negativity showed different current sources. This result gives further support to the idea that different neural processes are responsible for saccades in wakefulness and REMs in REM sleep [4,8].
T. Abe et al. / International Congress Series 1270 (2004) 241–244
243
Fig. 1. Current sources of the presaccadic positivity and pre-REM negativity calculated using LORETA. Upper and lower panels show current sources of the presaccadic positivity and pre-REM negativity, respectively. Left panels show grand mean waveforms time-locked to the onsets of saccades and REMs. Recording sites were the parietal midline (Pz) and prefrontal midline (Fpz) sites, respectively, referenced to digitally linked earlobes. Vertical axes indicate the onset of eye movements. Solid and open triangles indicate the presaccadic positivity and pre-REM negativity, respectively.
The presaccadic positivity had its origin in the bilateral medial frontal gyrus. The current sources of the presaccadic positivity calculated in this study were located in somewhat upper regions above the supplementary eye fields (SEF) observed in fMRI studies [9,10]. However, considering the relatively small number of electrodes used in this study (26 sites), the current sources of the presaccadic positivity estimated in the present study might be bilateral SEFs. In REM sleep, current sources of the pre-REM negativity were identified in the right amygdala, right parahippocampal gyrus, and left orbital gyrus. Functional imaging studies using positron emission tomography have revealed that the activations of the amygdala associated with REM sleep [11] and the right parahippocampal gyrus correlated positively with the number of REMs [12,13]. Magnetoencephalographic study showed activation in the right amygdala, right parahippocampal gyrus, and left orbitofrontal cortex in the last 100 ms before REMs [14]. Our estimation using LORETA is consistent with these
244
T. Abe et al. / International Congress Series 1270 (2004) 241–244
findings and suggests that the pre-REM negativity reflects the activity that occurred in the limbic part of the brain and is possibly associated with memory and emotional processing in REM sleep. Acknowledgements This study was supported by a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (No. 14201011). References [1] J.A. Hobson, E.F. Pace-Schott, R. Stickgold, Dreaming and the brain: toward a cognitive neuroscience of conscious states, Behav. Brain Sci. 23 (6) (2000) 793 – 842. [2] S. Everling, P. Krappmann, H. Flohr, Cortical potentials preceding pro- and antisaccades in man, Electroencephalogr. Clin. Neurophysiol. 102 (4) (1997) 356 – 362. [3] J.E. Richards, Cortical sources of event-related potentials in the prosaccade and antisaccade task, Psychophysiology 40 (6) (2003) 878 – 894. [4] T. Abe, et al., Lack of presaccadic positivity before rapid eye movements in human REM sleep, NeuroReport 15 (4) (2004) 735 – 738. [5] R.D. Pascual-Marqui, C.M. Michel, D. Lehmann, Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain, Int. J. Psychophysiol. 18 (1) (1994) 49 – 65. [6] A. Rechtschaffen, A. Kales, A manual of standardized terminology, techniques and scoring system for sleep stage of human subjects, UCLA, Brain Information Service/Brain Research Institute, Los Angeles, 1968. [7] T. Hori, et al., Proposed supplements and amendments to ‘A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects’ the Rechtschaffen and Kales (1968) standard, Psychiatry Clin. Neurosci. 55 (3) (2001) 305 – 310. [8] G. Vanni-Mercier, et al., Eye saccade dynamics during paradoxical sleep in the cat, Eur. J. Neurosci. 6 (8) (1994) 1298 – 1306. [9] B. Luna, et al., Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study, Cereb. Cortex 8 (1) (1998) 40 – 47. [10] M.H. Grosbras, et al., An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging, Cereb. Cortex 9 (7) (1999) 705 – 711. [11] P. Maquet, et al., Functional neuroanatomy of human rapid-eye-movement sleep and dreaming, Nature 383 (6596) (1996) 163 – 166. [12] A.R. Braun, et al., Dissociated pattern of activity in visual cortices and their projections during human rapid eye movement sleep, Science 279 (5347) (1998) 91 – 95. [13] P. Peigneux, et al., Generation of rapid eye movements during paradoxical sleep in humans, NeuroImage 14 (3) (2001) 701 – 708. [14] A.A. Ioannides, et al., MEG tomography of human cortex and brainstem activity in waking and REM sleep saccades, Cereb. Cortex 14 (1) (2004) 56 – 72.