Abstract
BackgroundEmotional information is frequently processed below the level of consciousness, where subcortical regions of the brain are thought to play an important role. In the absence of conscious visual experience, patients with visual cortex damage discriminate the valence of emotional expression. Even in healthy individuals, a subliminal mechanism can be utilized to compensate for a functional decline in visual cognition of various causes such as strong sleepiness. In this study, sleep deprivation was simulated in healthy individuals to investigate functional alterations in the subliminal processing of emotional information caused by reduced conscious visual cognition and attention due to an increase in subjective sleepiness. Fourteen healthy adult men participated in a within-subject crossover study consisting of a 5-day session of sleep debt (SD, 4-h sleep) and a 5-day session of sleep control (SC, 8-h sleep). On the last day of each session, participants performed an emotional face-viewing task that included backward masking of nonconscious presentations during magnetic resonance scanning.ResultsFinally, data from eleven participants who were unaware of nonconscious face presentations were analyzed. In fear contrasts, subjective sleepiness was significantly positively correlated with activity in the amygdala, ventromedial prefrontal cortex, hippocampus, and insular cortex, and was significantly negatively correlated with the secondary and tertiary visual areas and the fusiform face area. In fear-neutral contrasts, subjective sleepiness was significantly positively correlated with activity of the bilateral amygdala. Further, changes in subjective sleepiness (the difference between the SC and SD sessions) were correlated with both changes in amygdala activity and functional connectivity between the amygdala and superior colliculus in response to subliminal fearful faces.ConclusionSleepiness induced functional decline in the brain areas involved in conscious visual cognition of facial expressions, but also enhanced subliminal emotional processing via superior colliculus as represented by activity in the amygdala. These findings suggest that an evolutionally old and auxiliary subliminal hazard perception system is activated as a compensatory mechanism when conscious visual cognition is impaired. In addition, enhancement of subliminal emotional processing might cause involuntary emotional instability during sleep debt through changes in emotional response to or emotional evaluation of external stimuli.
Highlights
Emotional information is frequently processed below the level of consciousness, where subcortical regions of the brain are thought to play an important role
As with the presentation of neutral facial images, subjective sleepiness was significantly negatively correlated with activity in the secondary and tertiary visual cortices and the fusiform face area (FFA) [left visual cortex: x = −16, y = −98, z = 24, t(20) = 4.61; right visual cortex: x = 24, y = −96, z = 22, t(20) = 5.13; left FFA: x = −40, y = −46, z = −10, t(20) = 4.41; right FFA: x = 40, y = −54, z = −12, t(20) = 5.15 (Figure 2A)]
Changes in amygdala activation and changes in FcAMG-SCo by sleep debt (SD) were positively correlated with changes in the Discussion The results of this study revealed that the subjective feeling of strong sleepiness significantly altered participants’ emotional brain reaction toward negative emotional stimuli presented under nonconscious conditions
Summary
Emotional information is frequently processed below the level of consciousness, where subcortical regions of the brain are thought to play an important role. Representative findings in support of the subliminal processing of emotions indicate that when presented with emotional facial expressions, patients with visual cortex damage discriminated emotional valence of facial expressions in the absence of conscious visual experience [9], showed different physiological responses for each emotion [10], and had an activated subcortical pathway on functional brain imaging [11]. Such phenomena were once thought to be special examples of an otherwise hidden mechanism in healthy individuals that is only exposed by a loss of conscious visual cognition. This subliminal process might be utilized in healthy individuals with temporally or functionally impaired visual cognition
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