Inhalation of Stress Sweat Enhances Response to Neutral Faces
This study investigated whether human chemosensory-stress cues affect neural activity related to the evaluation of emotional stimuli. Chemosensory stimuli were obtained from the sweat of 64 male donors during both stress (first-time skydive) and control (exercise) conditions, indistinguishable by odor. We then recorded event-related potentials (ERPs) from an unrelated group of 14 participants while they viewed faces morphed with neutral-to-angry expressions and inhaled nebulized stress and exercise sweat in counter-balanced blocks, blind to condition. Results for the control condition ERPs were consistent with previous findings: the late positive potential (LPP; 400–600 ms post stimulus) in response to faces was larger for threatening than both neutral and ambiguous faces. In contrast, the stress condition was associated with a heightened LPP across all facial expressions; relative to control, the LPP was increased for both ambiguous and neutral faces in the stress condition. These results suggest that stress sweat may impact electrocortical activity associated with attention to salient environmental cues, potentially increasing attentiveness to otherwise inconspicuous stimuli.
The existence of alarm pheromones—chemosensory stress cues communicated between members of the same species—is well established in non-human mammals; when animals inhale odors secreted by acutely stressed conspecifics, they express neurobiological and behavioral changes consistent with heightened threat assessment (Fanselow, 1985; Zalaquett and Thiessen, 1991; Dielenberg and McGregor, 2001; Dielenberg et al., 2001; Kikusui et al., 2001). In our fMRI experiment and its subsequent replication, we showed that humans also activate the amygdala during inhalation of sweat taken from an independent sample of emotionally stressed individuals, with exercise sweat as a control (Mujica-Parodi et al., 2009). Importantly, participants were unable to perceptually differentiate between the sweat odors, suggesting that the amygdala response was specific to emotional, rather than olfactory, discrimination. Psychophysiological and behavioral research have additionally demonstrated that inhalation of human stress sweat augments the defensive startle reflex (Prehn et al., 2006; Pause et al., 2009) as well as enhancing perception and discrimination of fearful (Zhou and Chen, 2009) and angry (Mujica-Parodi et al., 2009) faces.
Based on this work, we tested the novel hypothesis that chemosensory stress cues may enhance neural activity that indexes perceptual salience and sustained attention. In particular, we focused on the late positive potential (LPP) component of the event-related potential (ERP). The LPP is observed as a sustained parietally maximal positivity that begins ~200 ms following stimulus presentation (Sutton et al., 1965; Foti et al., 2009). The LPP is larger (i.e. more positive) for emotional than neutral stimuli, and this effect is evident throughout the duration of picture presentation (Schupp et al., 2004; Leppanen et al., 2007; Holmes et al., 2008; Foti et al., 2009; Hajcak et al., 2009; MacNamara and Hajcak, 2009). In a series of studies, we have shown that the magnitude of the LPP is sensitive to stimulus meaning and salience: when pictures are preceded by negative compared to neutral descriptions, the LPP is increased (Foti and Hajcak, 2008; Macnamara et al., 2009). Further, directing attention to more or less arousing aspects within unpleasant pictures dynamically modulates the amplitude of the LPP (Dunning and Hajcak, 2009; Hajcak et al., 2009). Based on these and other similar data, we have argued that the LPP indexes sustained attention based on the appraised salience of visual stimuli (Hajcak et al., 2010). We hypothesized that stress sweat might generalize threat appraisal from angry faces (i.e. overt threat) to ambiguous and neutral faces (i.e. potential threat)—and that the increased salience of neutral and ambiguous faces under stress sweat conditions would be reflected in an increased LPP.
Abstract and Introduction
Abstract
This study investigated whether human chemosensory-stress cues affect neural activity related to the evaluation of emotional stimuli. Chemosensory stimuli were obtained from the sweat of 64 male donors during both stress (first-time skydive) and control (exercise) conditions, indistinguishable by odor. We then recorded event-related potentials (ERPs) from an unrelated group of 14 participants while they viewed faces morphed with neutral-to-angry expressions and inhaled nebulized stress and exercise sweat in counter-balanced blocks, blind to condition. Results for the control condition ERPs were consistent with previous findings: the late positive potential (LPP; 400–600 ms post stimulus) in response to faces was larger for threatening than both neutral and ambiguous faces. In contrast, the stress condition was associated with a heightened LPP across all facial expressions; relative to control, the LPP was increased for both ambiguous and neutral faces in the stress condition. These results suggest that stress sweat may impact electrocortical activity associated with attention to salient environmental cues, potentially increasing attentiveness to otherwise inconspicuous stimuli.
Introduction
The existence of alarm pheromones—chemosensory stress cues communicated between members of the same species—is well established in non-human mammals; when animals inhale odors secreted by acutely stressed conspecifics, they express neurobiological and behavioral changes consistent with heightened threat assessment (Fanselow, 1985; Zalaquett and Thiessen, 1991; Dielenberg and McGregor, 2001; Dielenberg et al., 2001; Kikusui et al., 2001). In our fMRI experiment and its subsequent replication, we showed that humans also activate the amygdala during inhalation of sweat taken from an independent sample of emotionally stressed individuals, with exercise sweat as a control (Mujica-Parodi et al., 2009). Importantly, participants were unable to perceptually differentiate between the sweat odors, suggesting that the amygdala response was specific to emotional, rather than olfactory, discrimination. Psychophysiological and behavioral research have additionally demonstrated that inhalation of human stress sweat augments the defensive startle reflex (Prehn et al., 2006; Pause et al., 2009) as well as enhancing perception and discrimination of fearful (Zhou and Chen, 2009) and angry (Mujica-Parodi et al., 2009) faces.
Based on this work, we tested the novel hypothesis that chemosensory stress cues may enhance neural activity that indexes perceptual salience and sustained attention. In particular, we focused on the late positive potential (LPP) component of the event-related potential (ERP). The LPP is observed as a sustained parietally maximal positivity that begins ~200 ms following stimulus presentation (Sutton et al., 1965; Foti et al., 2009). The LPP is larger (i.e. more positive) for emotional than neutral stimuli, and this effect is evident throughout the duration of picture presentation (Schupp et al., 2004; Leppanen et al., 2007; Holmes et al., 2008; Foti et al., 2009; Hajcak et al., 2009; MacNamara and Hajcak, 2009). In a series of studies, we have shown that the magnitude of the LPP is sensitive to stimulus meaning and salience: when pictures are preceded by negative compared to neutral descriptions, the LPP is increased (Foti and Hajcak, 2008; Macnamara et al., 2009). Further, directing attention to more or less arousing aspects within unpleasant pictures dynamically modulates the amplitude of the LPP (Dunning and Hajcak, 2009; Hajcak et al., 2009). Based on these and other similar data, we have argued that the LPP indexes sustained attention based on the appraised salience of visual stimuli (Hajcak et al., 2010). We hypothesized that stress sweat might generalize threat appraisal from angry faces (i.e. overt threat) to ambiguous and neutral faces (i.e. potential threat)—and that the increased salience of neutral and ambiguous faces under stress sweat conditions would be reflected in an increased LPP.
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