Arousal modulates auditory attention and awareness: insights from sleep, sedation, and disorders of consciousness

Abstract

The interplay between attention and consciousness is frequently tested in altered states of consciousness, including transitions between stages of sleep and sedation, and in pathological disorders of consciousness (DoC; the vegetative and minimally conscious states; VS and MCS). One of the most widely used tasks to assess cognitive processing in this context is the auditory oddball paradigm, where an infrequent change in a sequence of sounds elicits, in awake subjects, a characteristic EEG event-related potential called the mismatch negativity, followed by the classic P300 wave. The latter is further separable into the slightly earlier, anterior P3a and the later, posterior P3b, thought to be linked to task-irrelevant "bottom-up" and task-oriented "top-down" attention, respectively. We discuss here the putative dissociations between attention and awareness in DoC, sedation and sleep, bearing in mind the recently emerging evidence from healthy volunteers and patients. These findings highlight the neurophysiological and cognitive parallels (and differences) across these three distinct variations in levels of consciousness, and inform the theoretical framework for interpreting the role of attention therein.

Keywords: P300; arousal; attention and awareness; disorders of consciousness; mismatch negativity; sedation; sleep.

Figure 1

Mismatch negativity (MMN) and P300 in healthy awake adults. (A) MMN evoked by 1032 Hz deviant tones (20% probability), when compared to 1000 Hz standard tones. Adapted from Sams et al. (1985). (B) P3a and P3b evoked by 500 Hz non-target and 2000 Hz target tones (each with 10% probability), presented amongst 1940 Hz standard tones. Adapted from Comerchero and Polich (1999).

Figure 2

Mismatch negativity (MMN) and P300 in disorders of consciousness. (A) MMN elicited in a VS patient by 247 Hz deviant tones (10% probability) relative to 440 Hz standard tones. Adapted from Kotchoubey et al. (2005). (B) P3a elicited in MCS patient by rare sinusoidal tones (20% probability). Adapted from Bekinschtein et al. (2009). (C) P3b generated by MCS patient when counting task-relevant, unfamiliar target names presented amongst other unfamiliar names. Adapted from Schnakers et al. (2008).

Figure 3

Mismatch negativity (MMN) and P300 in sleep. (A) MMN observed during REM and Non-REM sleep by deviants (6.7% probability) embedded in alternating tone sequences. Adapted from Sculthorpe et al. (2009). (B) P300 observed during REM sleep by intensity deviants (5% probability). Adapted from Cote and Campbell (1999). (C) Occipital P400 observed during tonic REM sleep only in participants instructed to respond to 2000 Hz deviant tones (10% probability) presented amongst 1000 Hz standard tones. Adapted from Takahara et al. (2006).

Figure 4

Mismatch negativity (MMN) and P300 in anesthesia. (A) MMN elicited at different levels of consciousness by 25 ms tones (15% probability) presented amongst 75 ms tones. Adapted from Simpson et al. (2002). (B) P3a observed for task-relevant timbre deviants (6.67% probability), alongside an absence of P3b during deep sedation. Adapted from Koelsch et al. (2006).