1 INSERM-EMI 342, Federative Institut of Neurosciences (INSERM IFR 19), Unité dHypnologie, Hôpital Neurologique, 59 bd Pinel, 69003 Lyon, France, 2 EA 1880, Federative Institut of Neurosciences (INSERM IFR 19), Service de Neurologie Fonctionnelle et dEpileptologie, Hôpital Neurologique, 59 bd Pinel, 69003 Lyon, France
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Abstract |
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Key Words: cortex, dreaming, electrophysiology, human, paradoxical sleep, thalamus
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Introduction |
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Materials and Methods |
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Thalamic and cortical recordings were obtained from 11 patients. All of them presented with refractory temporal lobe epilepsy and necessitated a stereotactic EEG (SEEG) presurgical evaluation before functional surgery. All patients gave informed consent for the implantation of intracerebral electrodes and the recordings performed for this study. They presented with seizures suggesting a rapid propagation of epileptic discharges between limbic areas and posterior temporal neocortex, based on non-invasive video-scalp EEG recordings performed prior to intracerebral implantation of recording electrodes.
Implantation of SEEG electrodes
The electrode implantation procedure was carried out using multiple contact electrodes introduced into the brain perpendicular to the midsagittal plane, according to the stereotactic technique of Talairach and Bancaud (1973). Coordinates of relevant targets were determined on the patients brain magnetic resonance (MR) images according to previously described procedures (Frot and Mauguière, 1999
, 2003; Ostrowsky et al., 2002
). The medial pulvinar nucleus (PuM) was one of the targets of stereotactic implantation because, due to its reciprocal connections with cortical areas involved in seizures, it was suspected to be an important relay in the building of epileptic discharges. Moreover, intracortical exploration of target temporal neo-cortical areas and of the PuM nucleus was possible using stereotactic implantation of a single multi-contact electrode, so that PuM exploration did not increase the risk of the procedure by adding one further electrode track specifically devoted to the study of PuM activity. Anatomical localization of the thalamic and cortical electrode contacts was counterchecked using fusion of skull X-ray after electrode implantation with the appropriate coronal MR slice of the patients brain. The placement of two to four contacts within the PuM was assessed using the Morel atlas of the human thalamus (Morel et al., 1997
).
Recording Conditions
Night recording under video-EEG monitoring was conducted after a minimum delay of 5 days after electrode implantation. At that time, anticonvulsant drug intake had been drastically reduced for at least 1 week in order to record spontaneous epileptic seizures. Bipolar EEG signals and electro-oculograms were amplified, filtered (band pass: 0.33300 Hz) and stored with a sampling frequency of 128 Hz. The different states of vigilance were visually identified according to the criteria of Rechtschaffen and Kales (1968). In each patient, the thalamic PuM activity was recorded simultaneously with 312 cortical derivations selected for absent or limited interictal epileptic activities. In each state (i.e. waking, stage 2, SWS and PS), periods of 34 min were selected after discarding the remaining interictal epileptic activities. These periods were further subdivided in 4 s epochs, the power spectra of which were calculated using a fast Fourier transform (10% tapered-cosine window; frequency resolution 0.25 Hz) and averaged. Cortical and thalamic spectra were then normalized and the average relative power of each standard electroencephalographic frequency band [slow oscillation (SO), 0.51.25 Hz, delta, 1.54.5 Hz, theta, 4.757.75 Hz, alpha, 812 Hz, sigma, 12.2515 Hz, beta, 15.2530 Hz, gamma, 30.2560 Hz] was calculated. Finally, a grand average of the relative power of each frequency band was obtained by pooling the 11 thalamic PuM and 91 cortical (temporal lobe, 53; frontal lobe, 16; parietal lobe, 10; insula, 7; occipital lobe, 5) recordings and submitted to statistical analysis.
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Results |
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Striking preponderant oscillations in the delta (1.54.5 Hz) frequency band were apparent on rough recordings in PuM during PS, without any counterpart during the three other vigilance states (Fig. 1a). A few sporadic cycles of these delta oscillations were occasionally present in the final decay of sleep stage 4 (Fig. 1b). They were interspersed in, but distinct from, the previously described SO (<1.25 Hz) frequency oscillation characteristic of this sleep stage (Steriade et al., 1993; Achermann and Borbély, 1997
; Simon et al., 2000
). As cortical activity became desynchronized, indicating the beginning of a PS period, PuM delta oscillations occurred more and more frequently before becoming stable (Fig. 1b). Nevertheless, all along a PS period, they were interrupted by
20 short (220 s) periods of rapid activity similar to that observed in wakefulness. At the end of the PS period, the delta oscillations ceased abruptly to be replaced by an activity corresponding to the next state of vigilance (Fig. 1b). This phenomenon was observed in the 11 patients without exception, during all recorded PS periods, although the amplitude of these delta oscillations showed a high degree of interindividual variation.
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In all patients, power spectra of PuM activity during PS periods showed a clear peak in the delta frequency band (Fig. 2, solid arrow). This peak corresponded to the delta oscillations described above and its average frequency value was 2.38 ± 0.43 Hz. In 9 of the 11 patients, the power spectra exhibited a second peak in the SO (<1.25 Hz) frequency band (mean frequency: 0.84 ± 0.3 Hz; Fig. 2, open arrow). This phenomenon, when present, was highly variable in amplitude between patients. The average frequencies of the SO and delta peaks were statistically different (paired t-test, two-tailed P < 0.0001).
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Another interesting observation concerned the mean relative power of the beta and gamma frequency bands. At the thalamic PuM level, our data analysed with repeated-measures ANOVA revealed a marked vigilance state effect on power of the beta [F(3,10) = 22.78, P < 0.0001] and gamma [F(3,10) = 9.65, P < 0.0001] frequency bands due to a significant increased activity during waking with respect to the three other vigilance states (TukeyKramer post hoc pairwise comparisons: beta, P < 0.001; gamma, P < 0.01; Fig. 3). At the cortical level, statistical analysis showed a clear vigilance state effect for these two high-frequency bands [beta, F(3,10) = 12.99, P < 0.0001; gamma, F(3,10) = 4.26, P < 0.01] due to a selective decreased activity during SWS (beta, P <0.01; gamma, P < 0.05; Fig. 3).
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Discussion |
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Possible Origin of the Discrepancy between Thalamic PuM and Cortical Activities during PS
The increase of cerebral high-frequency (>30 Hz) activities known to occur during PS is mainly consecutive to the activation of widespread brainstem cholinergic projections terminating at both thalamic and cortical levels (Steriade et al., 1997). In contrast to the other thalamic nuclei, PuM exhibits an extremely weak cholinergic innervation (Hirai and Jones, 1989
). Thus, the low power in high-frequency bands we observed in this nucleus during PS could be related to a lack of cholinergic activation during PS. In addition, the thalamic PuM nucleus remaining in a non-activated state would be in a situation favourable to the development of preponderant delta activities.
Putative Functional Consequences with Respect to Dream Contents
The possible functional implications of a discrepant level of activity between PuM and cortical areas can be interpreted with reference to the presumed relationship linking cerebral activity and cognitive experience. During wakefulness, the spatio-temporal binding of high-frequency activities at several locations within the cerebral cortex and in the thalamic nuclei to which they project has been proposed as the underlying mechanism of cognitive events (Singer, 1998; Rodriguez et al., 1999
; Jones, 2001
). The similarity of cerebral activity between awake and PS states makes plausible the assumption that oneiric cognitive events could arise from a similar mechanism. However, contents of dreams present bizarre features. These features resemble the altered perceptions experienced during waking by brain-damaged patients (Schwartz and Maquet, 2002
), in whom the spatio-temporal binding of high-frequency activities could occur only partially between the remaining uninjured cortical areas. One might thus hypothesize that, in normal subjects, altered perceptive experiences reported in dreaming are the result of an imperfect high-frequency spatio-temporal binding.
In this context, our results could find a possible functional counterpart. Connections linking the cerebral cortex and the thalamus make them a unified oscillatory entity in which each constituent influences the other (Steriade, 1997). The preponderant delta and the depleted beta and gamma frequency activities we observed in PuM during PS are thus able to interfere with activation of associated cortical areas connected with this thalamic nucleus. Recent data support this hypothesis by showing that three cortical areas densely connected with PuM (posterior cingulate, dorso-lateral prefrontal and parietal cortices; Baleydier and Mauguière, 1987
; Romanski et al., 1997
; Gutierrez et al., 2000
), exhibit a distinct behaviour during PS. They present a lack of increased blood flow, i.e. a deficient activation, contrasting with the rest of the cerebral cortex (Maquet et al., 1996
; Maquet, 2000
) in this state. This situation could reflect an incomplete binding in the high-frequency range of different cortical areas, a phenomenon resulting in the vagaries typical of oneiric contents.
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Notes |
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Address correspondence to M. Magnin, INSERM-EMI 342, Unité dHypnologie, Hôpital Neurologique, 59 bd Pinel, 69677 Bron, France. Email: michel.magnin{at}univ-lyon1.fr.
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