Odd Sound Processing in the Sleeping Brain
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Odd Sound Processing in the Sleeping Brain Perrine Ruby, Anne Caclin, Sabrina Boulet, Claude Delpuech, and Dominique Morlet Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/20/2/296/1760419/jocn.2008.20023.pdf by guest on 18 May 2021 Abstract & How does the sleeping brain process external stimuli, and in found in response to deviant tones, revealing for the first time particular, up to which extent does the sleeping brain detect and preserved sensory memory processing during almost the whole process modifications in its sensory environment? In order to night. Surprisingly, during Sleep Stage 2 and paradoxical sleep, address this issue, we investigated brain reactivity to simple both P3a-like and P3b-like components were identified after the auditory stimulations during sleep in young healthy subjects. MMN, whereas a P3a alone followed the MMN in wakefulness Electroencephalogram signal was acquired continuously during and in Sleep Stage 1. This totally new result suggests elaborated a whole night of sleep while a classical oddball paradigm with processing of external stimulation during sleep. We propose duration deviance was applied. In all sleep stages, except Sleep that the P3b-like response could be associated to an active Stage 4, a mismatch negativity (MMN) was unquestionably processing of the deviant tone in the dream’s consciousness. & INTRODUCTION cess which can be investigated in humans using electro- Although it was thought for a long time that the sleeping physiology. It was often investigated in the auditory brain is disconnected from the external world, many modality using an oddball paradigm in which trains of studies in the end of the last century have revealed that repetitive identical sounds (standards) are occasionally it is not the case. As an example, it was found in the late interspersed with slightly different sounds (deviants). 1980s that, during sleep, the brain produces stimulus- The potential evoked by the rare sound was shown to be related activity in the primary auditory cortex in response more negative than the one evoked by the frequent to simple sounds (Deiber, Ibanez, Bastuji, Fischer, & sound so that difference between the two was labeled Mauguie`re, 1989). Nowadays, the sleeping brain is less mismatch negativity (MMN) (Na¨a¨ta¨nen, Gaillard, & and less considered as a passive and isolated resting Mantysalo, 1978). This negative wave appears at fronto- organ but more and more as an active processor (gener- central electrodes around 150 msec and is considered ating dreams), with a modified functional organization to be an electrophysiological correlate of a comparison (e.g., with visual information processing flow going mechanism indicating a mismatch between a stored from associative to primary visual areas; Maquet et al., representation in sensory memory and an incoming 2004; Braun et al., 1998), and still interacting with the auditory event (Na¨a¨ta¨nen, 1985). The MMN can there- external world (e.g., processing auditory stimulations up fore be used to probe auditory sensory memory repre- to their semantic dimension; Bastuji, Perrin, & Garcia- sentations (Ritter, Deacon, Gomes, Javitt, & Vaughan, Larrea, 2002; Perrin, Bastuji, & Garcia-Larrea, 2002; 1995). Perrin, Garcia-Larrea, Mauguie`re, & Bastuji, 1999). But MMN was described to be an automatic wave, which to what extent is the sleeping brain responsive to the can be elicited even though the subject is not attending environment? Which sensory and cognitive processes are to the irregularities eliciting it (Woldorff, Hackley, & maintained? Hillyard, 1991; Giard, Perrin, Pernier, & Bouchet, Given the elaborated processing of external stimuli 1990). It seems to be associated with triggering the during sleep evidenced by the results of Bastuji et al. orienting response (for a recent review, see Kujala, (2002) and Perrin et al. (1999, 2002), one would expect Tervaniemi, & Schro¨ger, 2007). Actually, according to that basic mechanisms such as sensory memory are also the extent of stimulus change and to the task involved, preserved during sleep. These memory traces may in- the MMN can sometimes be followed by other event- deed be considered as a prerequisite for further and related potential (ERP) components such as P300 waves. more complex processing, as discussed by Na¨a¨ta¨nen and When subjects are involved in a distracting task and do Winkler (1999). Sensory memory is a short-lasting pro- not pay attention to the tones, the MMN tends not to be followed by any P300 components. However, in these unattended conditions, a P3a component (the early and INSERM, U821; Institut Fe´de´ratif des Neurosciences; and fronto-central component of the P300) or a N2b–P3a Universite´ Lyon 1, Lyon, France complex happens to be detected when the extent of D 2008 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 20:2, pp. 296–311 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2008.20023 by guest on 25 September 2021 deviance is large enough to trigger a switch of attention results in these studies (subjects were awakened repeat- (Escera, Alho, Winkler, & Na¨a¨ta¨nen, 1998). In active edly in Sabri et al., 2003; Sabri, De Lugt, & Campbell, 2000, paradigms, when the deviant tones are to be drawn to in order to investigate sleep onset; subjects were awak- the subject’s attention, a task-relevant target P3b (the ened as soon as they entered in Sleep Stage 3 in Nittono late and parietal component of the P300) is obtained et al., 2001, in order to investigate Sleep Stage 2; Sallinen (Squires, Squires, & Hillyard, 1975a). A P3b can even et al., 1996 focused on the comparison between phasic arise in passive paradigms if the extent of deviance is and tonic PS). very large (Polich, 1989; Na¨a¨ta¨nen, Simpson, & Loveless, Given the lack of convincing data regarding the 1982). possibility to obtain an MMN during sleep with classical In an attempt to investigate sensory memory during oddball paradigms (with ISI typically around 600 msec), Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/20/2/296/1760419/jocn.2008.20023.pdf by guest on 18 May 2021 sleep, several studies have used oddball paradigms in Sabri and Campbell (2005) and Sabri et al. (2003) sleeping healthy subjects. They resulted in divergent hypothesized that, during non-rapid eye movement conclusions as revealed by the review of the literature sleep, MMN generators remain active but a rapid mem- presented in Table 1, so that the issue of a preserved ory decay prevents the brain to detect the deviance. In ability of the sleeping brain to evoke an MMN in order to test this hypothesis, they used a faster rate of response to a deviant tone is still under debate. Some stimuli presentation (i.e., every 150 msec; Sabri et al., authors concluded to the absence of MMN in all sleep 2003). With this noncanonical paradigm they managed to stages tested (Sleep Stages 1 to 4 in Paavilainen et al., evidence significant DRN in response to large frequency 1987), whereas, more recently, Sabri, Labelle, Gosselin, deviants, in all sleep stages (Sabri & Campbell, 2005). and Campbell (2003) detected a deviant-related negativ- However, the authors stated that the DRN probably ity (DRN) in each of these stages. However, because reflects a contribution of both the N1 and MMN intra- they used a rapid rate of stimulus presentation, it is cranial sources (Sabri & Campbell, 2005) so that their quite difficult to conclude whether this DRN is a mere study did not fully solve the issue of the possibility to N1 enhancement effect, a genuine MMN, or a combina- detect a ‘‘true’’ MMN during sleep. Hence, we cannot say tion of the two. During paradoxical sleep (PS; also called today, based on the results in the literature, whether an rapid eye movement [REM] sleep) several authors MMN can be elicited during each stage of natural sleep. (Atienza & Cantero, 2001; Atienza, Cantero, & Gomez, One direction to ensure reliable results may be found 1997, 2000; Nashida et al., 2000; Loewy, Campbell, & in the use of a robust procedure in ecological condi- Bastien, 1996), although not all of them (Loewy, Campbell, tions. To the best of our knowledge, only one study de Lugt, Elton, & Kok, 2000; Sallinen, Kaartinen, & (Nashida et al., 2000) looked for MMN in all sleep stages, Lyytinen, 1996), found an MMN. This absence of clear however, their results (no significant detection of MMN positive results, suggesting a loss or an attenuation of in Sleep Stages 2, 3, and 4) were issued from only 4 hr of sensory memory function during sleep, is quite puzzling EEG recordings. In addition, most of the studies, which given that an MMN can be detected in some comatose looked for an MMN during sleep, used frequency devi- patients. In this context, the positive detection of this ants. Tervaniemi et al. (1999), however, showed that wave was further shown to be a very efficient predictive among frequency, intensity, and duration, the deviance factor of awakening and recovery, even in deeply coma- in duration elicited the MMN with the most replicable tose patients (Fischer, Luaute´, Adeleine, & Morlet, 2004; amplitude and latency. Duration deviance protocols also Fischer et al., 1999). These results, demonstrating the have a number of advantages with regard to potential possibility of a spared auditory sensory memory in a path- confounds of the MMN. The traditional deviant-minus- ological altered state of consciousness, lead to predict standard ERP can indeed be contaminated by a number that such ability should also be preserved in a physio- of other negativities overlapping the MMN. Most partic- logical altered state of consciousness such as sleep. ularly, differences in the evoked sensory responses To explain the apparent inconsistency between the (such as the N1) for the standard and deviant tones results reported in Table 1, many reasons could be might artificially enhance measures of the MMN.