AUTOPHaGic PUncTUM

aRTiclE addEndUM

Communicative & Integrative Biology 3:6, 525-527; November/December 2010; 2010 Landes Bioscience

Salivary a-amylase levels as a biomarker of experienced fear

Tony W. Buchanan,1,* David Bibas2 and Ralph Adolphs3
1

Department of Psychology; Saint Louis University; Saint Louis, MO USA; 2California Science Center; Los Angeles, CA USA; 3Departments of Biology and Humanities and Social Sciences; California Institute of Technology; Pasadena, CA USA

Key words: emotion, affect, facial expression, sympathetic nervous system, alphaamylase, cortisol, museum Submitted: 06/06/10 Accepted: 06/06/10 Previously published online: www.landesbioscience.com/journals/cib/ article/12606 DOI: 10.4161/cib.3.6.12606
*Correspondence to: Tony W. Buchanan; Email: tbuchan7@slu.edu Addendum to: Buchanan TW, Bibas D, Adolphs R. Associations between feeling and judging the emotions of happiness and fear: findings from a large-scale field experiment. PLoS ONE 2010; 5:10640; PMID 20498838; DOI:10.1371/journal. pone.0010640.

e recently reported data related to emotions collected in conjunction with a museum exhibit on emotion (Goose Bumps!The Science of Fear).1 In this addendum, we present additional data collected as part of that study. We collected two commonly measured indices of emotional arousal, salivary cortisol and a-amylase, before and after participants had gone through a realistic fear challenge course as part of the exhibit. We found that a-amylase, but not cortisol, showed a highly specic increase only for those participants who endorsed both emotional arousal and negative valence. By contrast, the fear-inducing course resulted in high arousal but positive valence in some participants; in these, no increased a-amylase was measured. We conclude that salivary a-amylase is a promising biomarker for fearful experiences, and suggest that it is important to pay attention to positively valenced arousal that may be induced by fearful stimuli in a laboratory setting. How can human emotion be measured in an ecologically valid setting? Research on the topic typically falls into one of two categories: studies in the laboratory with precise experimental control but often poor validity, and eld research that is difcult to control and often correlational in nature. We conducted a study that measured indices of emotion in a setting somewhat intermediate to these two extremes: participation in a museum exhibit on fear. We acquired subjective and physiological responses to a museum exhibit designed to induce a fear response. Forty-nine museum-goers (26 men,

23 women; a subset of the larger group tested in our previous study) between the ages of 18 to 70 (mean age: 34.1 14.6) completed the Fear Challenge Course, part of Goose Bumps!The Science of Fear, a hands-on exhibit focusing on the biology, psychology and sociology of emotion with an emphasis on fear, developed by the California Science Center. The Fear Challenge Course consisted of four separate activities designed to elicit a fear response: (1) In the Fear of Animals exhibit, participants are exposed to terrariums lled with snakes and tarantulas and are invited to insert their hands into a black box to feel and recognize models of these animals. (2) In the Fear of Electric Shock exhibit, participants insert a nger into a device that appears to be attached to a buzzing Jacobs ladder and are asked to press a button to send a (very mild) electric shock to the nger. There is a delay between pressing the button and receiving the shock, which demonstrates the effects of anticipation of fear. (3) In the Fear of Loud Noises exhibit, participants sit in front of a computer monitor equipped with a camera and are asked to keep a straight face as spooky music is played back; then suddenly a loud shot res and a high speed camera captures their facial expression. (4) In the Fear of Falling exhibit, participants are strapped to a plank before a staff member unexpectedly releases the plank. The participants fall is cushioned at the last moment. Before and after completing the challenge course, participants gave saliva samples for measure of cortisol and a-amylase (sAA). Cortisol is one of the primary human stress hormones and sAA is an enzyme, which serves as an index of

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Figure 1. Emotional experience during a fear challenge determines physiological response. (A) The affect grid questionnaire color coded to indicate the four quadrants in which participants could describe their experience during the fear challenge: high arousal and low pleasantness corresponds to the negatively aroused quadrant (N = 9); high arousal and high pleasantness corresponds to the positively aroused quadrant (N = 33); low arousal and high pleasantness corresponds to the positively calm quadrant (N = 7); none of the participants rated themselves in the low arousal low pleasantness quadrant. (B) Salivary a-amylase responses (post-challenge minus pre-challenge levels) for participants in each quadrant (color-coded to match the corresponding quadrant in A, above). Negatively aroused participants showed a pronounced a-amylase response to the fear challenge (indicative of sympathetic nervous system activity).

sympathetic nervous system activity.2,3 Both of these serve as indices of the ght or ight response associated with states of fear.4 At the end of the exhibit viewing, participants completed an emotional

state questionnaire, the affect grid,5 which provides an index of both valence (pleasant versus unpleasant) and arousal (calm versus excited). Participants were asked to rate how they felt during the

challenge course by placing an X in one box on a grid that varied in one direction along the valence axis and in the other direction along the arousal axis. Participants who placed themselves in the negatively aroused quadrant of the affect grid showed a pronounced sympathetic nervous system response to the challenge course as indexed by sAA levels [t(8) = 3.4, p < 0.05; see Fig. 1]. Those who rated their experience as falling within one of the other quadrants of the grid did not show a sympathetic nervous system response (in fact, their sAA levels were signicantly reduced, p < 0.05). None of the groups showed a signicant cortisol response to the challenge course (ps > 0.2), nor were there any differences between mens and womens responses to the challenge course using either cortisol or sAA levels as the dependent measure (ps > 0.3). These results demonstrate that a naturalistic fear challenge can elicit a sympathetic nervous system response normally associated with fear, but only in those participants who experience the challenge in a negatively arousing way. Positive arousal, by contrast, did not elicit such a response. This pattern is surprising given the typical pattern of sympathetic nervous system activity in response to arousing situations. The controlled environment of a museum most likely reduced the intensity of the emotion for some participants or triggered instead an arousing but pleasurable experience. This appears to be consistent with the design intent of the exhibit developers who set out to create experiences that are scary but fun. Emotion research consistently demonstrates considerable individual differences in how people respond to emotional situations.6,7 These differences may explain the variability in valence of the experiences in our study also. The ndings are particularly important, because fear-inducing, but ultimately safe, stimuli are typically used in all experimental studies of fearusing stimuli such as lm clips, for instance. The reason people seek out roller coasters and horror movies is likely due in part to the ability of such stimuli to trigger sympathetic arousal in the face of a positively valenced experienced; they may not be a valid model of actual fear, however.

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References
1. Buchanan TW, Bibas D, Adolphs R. Associations between feeling and judging the emotions of happiness and fear: findings from a large-scale field experiment PLoS ONE 2010; 5:10640. 2. Kirschbaum C, Hellhammer DH. Salivary cortisol in psychobiological research: an overview. Neuropsychobiology 1989; 22:150-69. 3. Nater UM, Rohleder N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology 2009; 34:486-96. 4. Cannon WB. Bodily changes in pain, hunger, fear and rage: an account of recent research into the function of emotional excitement. New York, NY: Appleton-Century-Crofts 1929.

5. Russell JA, Weiss A, Mendelsohn GA. Affect grid: a single-item scale of pleasure and arousal. J Pers Soc Psychol 1989; 57:493-502. 6. Davidson RJ, Irwin W. The functional neuroanatomy of emotion and affective style. Trends Cogn Sci 1999; 3:11-21. 7. Heller W. Neuropsychological mechanisms of individual differences in emotion, personality and arousal. Neuropsychology 1993; 7:476-89.

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