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Chemosensory cues to conspecific emotional stress activate amygdala in humans.

Mujica-Parodi LR, Strey HH, Frederick B, Savoy R, Cox D, Botanov Y, Tolkunov D, Rubin D, Weber J - PLoS ONE (2009)

Bottom Line: In an fMRI experiment and its replication, we showed that scanned participants showed amygdala activation in response to samples obtained from donors undergoing an emotional, but not physical, stressor.An odor-discrimination experiment suggested the effect was primarily due to emotional, and not odor, differences between the two stimuli.A fourth experiment investigated behavioral effects, demonstrating that stress samples sharpened emotion-perception of ambiguous facial stimuli.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Engineering, Stony Brook University School of Medicine, Stony Brook, New York, United States of America. lmujicaparodi@gmail.com

ABSTRACT
Alarm substances are airborne chemical signals, released by an individual into the environment, which communicate emotional stress between conspecifics. Here we tested whether humans, like other mammals, are able to detect emotional stress in others by chemosensory cues. Sweat samples collected from individuals undergoing an acute emotional stressor, with exercise as a control, were pooled and presented to a separate group of participants (blind to condition) during four experiments. In an fMRI experiment and its replication, we showed that scanned participants showed amygdala activation in response to samples obtained from donors undergoing an emotional, but not physical, stressor. An odor-discrimination experiment suggested the effect was primarily due to emotional, and not odor, differences between the two stimuli. A fourth experiment investigated behavioral effects, demonstrating that stress samples sharpened emotion-perception of ambiguous facial stimuli. Together, our findings suggest human chemosensory signaling of emotional stress, with neurobiological and behavioral effects.

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Breathing stress-derived sweat modulates the amygdala, the primary brain region associated with emotional processing.The unmasked activation map (a) reflects the STRESS−EXERCISE contrast, and was produced using height threshold t = 3.7, p<0.001 (uncorrected) and extent threshold k = 5 voxels. The MNI coordinates of the maximally activated voxel, located in the left amygdala, are [x = −27, y = −6, z = −12] (t = 5.21/Z = 3.88; p(small-volume-corrected) = 0.008). Inspection of the mean response to STRESS-REST and EXERCISE-REST contrasts (b) initially appeared to suggest mean deactivation in response to EXERCISE sweat. However, once we factored in the variance (c), it became clear that the effect for the STRESS-EXERICISE contrast was predominantly due to activation in response to the STRESS condition, rather than to deactivation in response to the EXERCISE condition, as only the former showed statistically significant changes from baseline.
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pone-0006415-g002: Breathing stress-derived sweat modulates the amygdala, the primary brain region associated with emotional processing.The unmasked activation map (a) reflects the STRESS−EXERCISE contrast, and was produced using height threshold t = 3.7, p<0.001 (uncorrected) and extent threshold k = 5 voxels. The MNI coordinates of the maximally activated voxel, located in the left amygdala, are [x = −27, y = −6, z = −12] (t = 5.21/Z = 3.88; p(small-volume-corrected) = 0.008). Inspection of the mean response to STRESS-REST and EXERCISE-REST contrasts (b) initially appeared to suggest mean deactivation in response to EXERCISE sweat. However, once we factored in the variance (c), it became clear that the effect for the STRESS-EXERICISE contrast was predominantly due to activation in response to the STRESS condition, rather than to deactivation in response to the EXERCISE condition, as only the former showed statistically significant changes from baseline.

Mentions: In the original experiment, we presented sweat from 40 male donors to 16 participants (50% female) while their brains were scanned using fMRI. In a replication experiment, using different participants and scanners, we presented sweat from an additional 40 donors (50% female) to a different group of 16 participants (50% female) undergoing fMRI, increasing power by doubling the number of stimulus presentations. Because we hypothesized that perception of emotional stress would modulate activity in a brain area related to emotion, our analyses focused on the amygdala; all values were corrected for multiple-comparisons using small-volume correction (SVC). For both experiments, these revealed significant activation of the left amygdala (Original Experiment: t = 4.80/Z = 3.68, p(svc) = 0.02 [MNI x, y, z = −16, −10, −18], N = 16; Replication Experiment: t = 5.21/Z = 3.88, p(svc) = 0.008, [MNI x, y, z = −27, −6, −12], N = 16; Figure 2) in response to the stress sweat as compared to the exercise sweat. For both experiments, activity was concentrated most strongly in the superficial, or corticoid, amygdala (Original Experiment: t = 4.80/Z = 3.68, p(svc) = 0.008, N = 16; Replication Experiment: t = 5.21/Z = 3.88, p(svc) = 0.008, N = 16)—a region known to have substantial olfactory inputs in primates; homologous structures in other mammals have been implicated in pheromonal processing [29]. Activation patterns were equivalent for same-sex and opposite-sex donor-detector pairs (repeated-measures ANOVA: Original Experiment: F = 1.76, p = 0.21, N = 16; Replication Experiment: Donor Sex: F = 0.21, p = 0.65, N = 16; Detector Sex: F = 1.31, p = 0.27, N = 16; Donor Sex*Detector Sex: F = 0.004, p = 0.952, N = 16), suggesting that reproductive chemosignals, known to be sex-specific in both animals [30] and humans [13], were not the likely cause. Whole-brain random-effects analyses for the STRESS-EXERICISE contrast (Figure 3, Table 1) included the amygdala with no significant de-activations.


Chemosensory cues to conspecific emotional stress activate amygdala in humans.

Mujica-Parodi LR, Strey HH, Frederick B, Savoy R, Cox D, Botanov Y, Tolkunov D, Rubin D, Weber J - PLoS ONE (2009)

Breathing stress-derived sweat modulates the amygdala, the primary brain region associated with emotional processing.The unmasked activation map (a) reflects the STRESS−EXERCISE contrast, and was produced using height threshold t = 3.7, p<0.001 (uncorrected) and extent threshold k = 5 voxels. The MNI coordinates of the maximally activated voxel, located in the left amygdala, are [x = −27, y = −6, z = −12] (t = 5.21/Z = 3.88; p(small-volume-corrected) = 0.008). Inspection of the mean response to STRESS-REST and EXERCISE-REST contrasts (b) initially appeared to suggest mean deactivation in response to EXERCISE sweat. However, once we factored in the variance (c), it became clear that the effect for the STRESS-EXERICISE contrast was predominantly due to activation in response to the STRESS condition, rather than to deactivation in response to the EXERCISE condition, as only the former showed statistically significant changes from baseline.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2713432&req=5

pone-0006415-g002: Breathing stress-derived sweat modulates the amygdala, the primary brain region associated with emotional processing.The unmasked activation map (a) reflects the STRESS−EXERCISE contrast, and was produced using height threshold t = 3.7, p<0.001 (uncorrected) and extent threshold k = 5 voxels. The MNI coordinates of the maximally activated voxel, located in the left amygdala, are [x = −27, y = −6, z = −12] (t = 5.21/Z = 3.88; p(small-volume-corrected) = 0.008). Inspection of the mean response to STRESS-REST and EXERCISE-REST contrasts (b) initially appeared to suggest mean deactivation in response to EXERCISE sweat. However, once we factored in the variance (c), it became clear that the effect for the STRESS-EXERICISE contrast was predominantly due to activation in response to the STRESS condition, rather than to deactivation in response to the EXERCISE condition, as only the former showed statistically significant changes from baseline.
Mentions: In the original experiment, we presented sweat from 40 male donors to 16 participants (50% female) while their brains were scanned using fMRI. In a replication experiment, using different participants and scanners, we presented sweat from an additional 40 donors (50% female) to a different group of 16 participants (50% female) undergoing fMRI, increasing power by doubling the number of stimulus presentations. Because we hypothesized that perception of emotional stress would modulate activity in a brain area related to emotion, our analyses focused on the amygdala; all values were corrected for multiple-comparisons using small-volume correction (SVC). For both experiments, these revealed significant activation of the left amygdala (Original Experiment: t = 4.80/Z = 3.68, p(svc) = 0.02 [MNI x, y, z = −16, −10, −18], N = 16; Replication Experiment: t = 5.21/Z = 3.88, p(svc) = 0.008, [MNI x, y, z = −27, −6, −12], N = 16; Figure 2) in response to the stress sweat as compared to the exercise sweat. For both experiments, activity was concentrated most strongly in the superficial, or corticoid, amygdala (Original Experiment: t = 4.80/Z = 3.68, p(svc) = 0.008, N = 16; Replication Experiment: t = 5.21/Z = 3.88, p(svc) = 0.008, N = 16)—a region known to have substantial olfactory inputs in primates; homologous structures in other mammals have been implicated in pheromonal processing [29]. Activation patterns were equivalent for same-sex and opposite-sex donor-detector pairs (repeated-measures ANOVA: Original Experiment: F = 1.76, p = 0.21, N = 16; Replication Experiment: Donor Sex: F = 0.21, p = 0.65, N = 16; Detector Sex: F = 1.31, p = 0.27, N = 16; Donor Sex*Detector Sex: F = 0.004, p = 0.952, N = 16), suggesting that reproductive chemosignals, known to be sex-specific in both animals [30] and humans [13], were not the likely cause. Whole-brain random-effects analyses for the STRESS-EXERICISE contrast (Figure 3, Table 1) included the amygdala with no significant de-activations.

Bottom Line: In an fMRI experiment and its replication, we showed that scanned participants showed amygdala activation in response to samples obtained from donors undergoing an emotional, but not physical, stressor.An odor-discrimination experiment suggested the effect was primarily due to emotional, and not odor, differences between the two stimuli.A fourth experiment investigated behavioral effects, demonstrating that stress samples sharpened emotion-perception of ambiguous facial stimuli.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Engineering, Stony Brook University School of Medicine, Stony Brook, New York, United States of America. lmujicaparodi@gmail.com

ABSTRACT
Alarm substances are airborne chemical signals, released by an individual into the environment, which communicate emotional stress between conspecifics. Here we tested whether humans, like other mammals, are able to detect emotional stress in others by chemosensory cues. Sweat samples collected from individuals undergoing an acute emotional stressor, with exercise as a control, were pooled and presented to a separate group of participants (blind to condition) during four experiments. In an fMRI experiment and its replication, we showed that scanned participants showed amygdala activation in response to samples obtained from donors undergoing an emotional, but not physical, stressor. An odor-discrimination experiment suggested the effect was primarily due to emotional, and not odor, differences between the two stimuli. A fourth experiment investigated behavioral effects, demonstrating that stress samples sharpened emotion-perception of ambiguous facial stimuli. Together, our findings suggest human chemosensory signaling of emotional stress, with neurobiological and behavioral effects.

Show MeSH
Related in: MedlinePlus