Different kinds of subjective experience during lucid dreaming may have different neural substrates

Recently, Allan Hobson published a brief essay in which he recognizes that lucid dreams are scientifically relevant and constitute a powerful tool for understanding the neurobiology of consciousness (Hobson, 2009). His statements are mostly based on the study by Voss et al. (2009), which employed refined mathematical analysis of electroencephalographic (EEG) recordings to tackle the neural basis of lucid dreaming. Several questions are open in this field, and we address one of them in this commentary. Lucid dreams occur during rapid eye movement sleep (REMS), and most people present REMS every night. Still, lucid dreams are uncommon. A likely explanation for this discrepancy is that there exists more than one kind of REMS, and that the specific kind of REMS during which lucid dreams occur is rare, with spectral features that differentiate it from non-lucid REMS. Early studies provided evidence of a relationship between the level of lucidity and the overall amount of EEG power in the alpha band (8-12 Hz) (Ogilvie et al., 1982; Tyson, et al., 1984). However, a subsequent study detected EEG power increase only within the beta band (13-20 Hz), restricted to the parietal region (Holzinger et al., 2006). More recent work found increased EEG power within the gamma band (peaking around 40 Hz) in frontal and fronto-lateral regions during lucid dreaming (Voss et al., 2009). Therefore, while there is evidence to suggest that lucid REMS present different spectral characteristics than non-lucid REMS, it is fair to say that there is substantial disagreement with regard to the brain regions and EEG frequency bands most activated during lucid dreams. To investigate this controversy, we are currently comparing the spatial and spectral properties of EEG oscillations during lucid and non-lucid REMS. We are also sorting apart spontaneous and induced episodes of lucidity. Although lucid dreaming is spontaneously rare, it is a learnable skill (Purcell et al., 1986) and can be induced by many techniques, like pre-sleep suggestion (Laberge, 1980) and incubation of auditory (Laberge et al., 1981) or visual (Laberge et al., 1988) stimulus into REMS. Of note, lucid dream induction has an important clinical application for people that suffer from recurrent nightmares, an ordinary symptom of severe depression (Agargun et al., 2007) and post-traumatic stress disorder (Mellman & Hipolito, 2006), and many studies have found that lucid dream induction therapy is related to a decrease in nightmares’ frequency (Spoomaker & van den Bolt, 2006; Tanner, 2004), intensity (Zadra & Phil, 1997; Blagrove et al., 2001) or both (Brylowski, 1990; Abramovitch, 1995). Our preliminary results suggest that lucid dreams present different EEG features depending on whether they are spontaneous or induced by either visual stimulation during REMS or pre-sleep suggestion (Mota-Rolim et al., 2008; unpublished data). These EEG differences seemingly correspond to different kinds of lucid dream report. During spontaneous lucid dreams (n = 3 subjects, all frequent lucid dreamers), we observed a significant increase in EEG power within the beta band in the parieto-occipital region, as well as a global increase in theta phase-gamma amplitude coupling. These effects may be respectively related to the increased level of visual attention and executive memory processing required for lucidity during dreaming (Wróbel, 2000; Tort et al., 2009; Jerbi et al., 2009). In contrast, two successfully induced lucid dreams presented a significant increase of gamma activity in the frontal lobe, as reported by Voss et al. (2009). These lucid dream episodes were associated with first person dream reports, i.e. narratives from the point of view of the dreamer, with a great degree of executive control. Another successfully induced lucid dream was concurrent with increased gamma activity in the right parieto-temporal region, a brain area related to self-consciousness and body imagery (Blanke et al., 2005; De Ridder et al., 2007). Interestingly, this latter lucid dream episode was associated with a third person dream report, i.e. a narrative in which the character corresponding to the dreamer is observed from the outside, from an exterDifferent kinds of subjective experience during lucid dreaming may have different neural substrates