May 24, 2002
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Neuroendocrinology Letters incl. Psychoneuroimmunology & Chronobiology

NEUROENDOCRINOLOGY LETTERS
including Psychoneuroimmunology, Neuro
psychopharmacology,
Reproductive Medicine, Chronobiology
and Human Ethology
ISSN 0172–780X

NEL, Vol. 23 No. 2

ORIGINAL RESEARCH REPORT

References

2002; 23:79-84
pii: NEL230102R01
PMID:

full text pdf [103 kb]


The Scent of Fear   

Kerstin Ackerl,
Michaela Atzmueller,
Karl Grammer

Ludwig-Boltzmann-Institute for Urban Ethology at the Institute of Anthropology/University of Vienna.

Submitted: April 2, 2002
Accepted: April 3, 2002

Key words:
fear, human pheromones, cortisol,
olfactory communication, alarm substances

Abstract

In this study we tried to find out if fear can be detected from human body odours. Female subjects wore under-arm axillary pads while watching a terryfying film. Saliva cortisol samples were taken before and after the film presentation as a hormonal measure for the fear response. The fear experience itself was measured by Spielberger’s State-Trait Anxiety Inventory. A “neutral” film, shown one day after the “fear” film, was used as a control in a repeated measures design. In part two of the experiment, the axillary pads were presented to female subjects in a triple forced choice test. Results show that subjects were able to discriminate between fear and non-fear axillary pads, suggesting that women are indeed able to detect “the scent of fear”. A direct correlation between induced fear, changes in cortisol levels and smell ratings could not be established. Thus cortisol levels are probably not the inducer of the scent of fear and a hypothetical fear pheromone could have other origins.

... ...

People have always used scents to either mask their body odour or to express and emphasize their moods or appearance. The possibility that odours can also provide relevant biological information about their “sender” has only in recent years become the focus of scientific attention. Doty [1] described the advantages of olfactory communication as follows: the sense of smell even works if the other two “major” senses (visual and acoustic) are functionally restricted (for example if it is too dark or too loud). Moreover, odourous substances can easily be spread over large areas and can last for a long time. Intensity, distribution, and quality of scent marks can give information about size, reproductional and nutritional status, etc. of an individual without immediately drawing unwanted attention to the sender (e.g. detection from a predator via the loud noise, etc. of a sender). Another advantage in communication through odours lies in the fact that sender and receiver don’t have to be in close spatial distance in order to communicate.

The question then becomes prominent: if olfactory communication is useful in other animals, why is it not used by human as well?
In recent years this assumption has undergone major revision. Several studies indicate that humans do indeed seem to use olfactory communication and are even able to produce and perceive certain pheromones (for a detailed overview see [2]). Up to now most studies were looking at human pheromones linked to the sex hormones, the question of whether humans are or are not able to communicate other than sex-related information through odours has yet to be raised.

Fear arises in stressful situations that are subjectively perceived as threatening. The intensity of the induced negative feeling corresponds to the subjective perception of threat in a situation. If the negative feeling becomes too intense, a seeking-reaction for stress-relieving mechanisms is initiated [3].
Fear can be induced by external, objective threats (e. g. predators), as well as by internal, subjective threats, called “free floating anxieties”[4]. Free floating anxieties can be generated by conscious or subconscious memories of threatening experiences in the past, or by the mere anticipation of a stressful situation.

The assumption that fear is a learned avoidance reaction to potentially dangerous situations is gradually being questioned. Recent studies show that fear may be a genetically determined function of the nervous system [4]. This hypothesis receives support from an evolutionary point of view. The ability to detect and anticipate dangerous situations seems to be crucial for survival, and individual learning might not be entirely quick enough to ensure survival chances. Moreover, even potentially dangerous stimuli might be rare and thus impossible to learn – leading an individual into danger when the stimulus is encountered for the first time.

Panksepp [4] describes a “major fear circuit” in the brain located within the lateral and central parts of the amygdala in the lobus temporalis, the periaquaeductal grey (PAG) of the diencephalon and mesencephalon, and as “output-generating” parts the brain stem and the medulla.
Fear leads to reactions that are both behavioral and physiological. Behavioral reactions include either a “freeze”, “flight”, or “fight” response. Underlying physiological processes include an increase in heart rate, muscular tension, sweating, etc., and, most important, a response of the adrenal gland via the pituitary-hypothalamus-adrenal-axis (HHN) which leads to the release of cortisol. The cortisol level rises as a consequence of the production of corticotropin releasing hormone and ACTH [5]. Thus in many experiments the assessment of changes in cortisol levels is used as an indicator of potentially experienced fear. In a study by Hubert & de Jong-Meyer [6] male subjects showed an increase in cortisol levels (measured from saliva) while they were watching a horror film. Kirschbaum & Hellhammer [7] found similar results. In contrast, Hubert, Möller, & de Jong-Meyer [8] showed that subjects experienced an increase in cortisol levels in response to a funny movie. The authors speculate that every kind of affective arousal and change of mood, positive as well as negative, could be linked to cortisol secretion.

Besides fear inducing situations, everyday stressors, the so-called “daily hassles”, can also provoke a raise in cortisol levels [9; 10]. In fact, it seems that the mere anticipation of a stressful experience can have this effect [11].
It thus remains doubtful that cortisol secretions might function solely as a result of experiencing fear. Cortisol raises in such situations could also be due to the stressing effects of fear.

Alarm pheromones were found in fish as early as 1941 by Von Frisch [12] and have since then been found in many species. Today we know that at least insects, annelids, and fish use olfactory signals to inform their conspecifics about stress, alarm, and fear. In ants, for example, alarm substances can cause aggregation, dispersion, or defense of the colony depending on the sender’s status [13]. The use of alarm pheromones has also been demonstrated in bees (Apis mellifera) [14] and lice (Acyrthosiphon pisum) [15]. On “defective stimulation” earthworms (Lumbricus terrestris) give off a substance that makes their conspecifics avoid their area and thus potential predators [16]. Among vertebrates, fish are the best known example for the use of alarm substances: fathead minnows (Pimephales promelas) that have never before been confronted with a pike (Esox lucius) immediately “know” that it is a dangerous predator because the pike seems to get marked by an “odour label” by every minnow it actually catches [17]. Sources of alarm substances in minnows are for example urine, feces, and mucus.
Mammals also seem to use olfactory alarm signals. Valenta & Rigby [18] were able to show that rats can distinguish between the odour of stressed and “relaxed” conspecifics. Carr, Martorano & Krames [19] found that male mice prefer the smell of conspecifics that have just won a fight over the smell conspecifics that have not won a fight, and the smell of conspecifics that haven’t been experimentally shocked, over the smell of conspecifics that have been treated with electric shocks.

In predator-prey-interactions between Mongolian jirds (Meriones unguiculatus) and cats it was shown that the stressed mice mark the “dangerous areas” with their scent and thus tell their conspecifics to avoid these areas, while cats orientated themselves by the scent of stressed mice in order to find them [20].
If other mammals are able to warn their conspecifics – or at least send out the information that they are in a frightening situation – by emitting odourous substances, the question becomes prominent: Do humans possess similar mechanisms? If so, how are these mechanisms related to cortisol release? The current research aims to address these questions.

Methods
... ...


REFERENCES

1 Doty RL. Odor guided behavior in mammals. Experentia 1986; 42: 257–71.

2 Kohl J, Atzmueller M, Fink B, & Grammer K. Human Pheromones: Integrating Neuro­endocrinology and Ethology. Neuroendocrinol Lett 2001; 22(5): 319–31.

3 Spielberger CD, Gorsuch RL, Lushene RE. Manual for the State-Trait Anxiety Inventory. Palo Alto. Consulting Psychologists Press; 1983.

4 Panksepp J. Affective neuroscience: The foundations of human and animal emotions. New York, Oxford. Oxford Plenum Press; 1998.

5 Kirschbaum C, Hellhammer DH. Salivary cortisol in psychoneuroendocrine research: Recent developments and applications. Psychoneuroendocrinol 1994; 19(4): 313–33.

6 Hubert W, de Jong-Meyer R. Emotional stress and saliva cortisol response. J Clin Chem Clin Biochem 1989; 27: 235–7.

7 Kirschbaum C, Hellhammer DH. Response variability of salivary cortisol under psychological stimulation. J Clin Chem Clin Biochem 1989; 27: 237.

8 Hubert W, Möller M, de Jong-Meyer R. Film-induced amusement changes in saliva cortisol levels. Psychoneuroendocrinol 1993; 18: 265–72.

9 Ockenfels M, Smyth J, Porter L, Kirschbaum C. Der Einfluß alltäglicher Stressoren (daily hassles) auf die Cortisolkonzentration im Speichel. Verhaltenstherapie 1995; 5 (suppl 1); 16–20.

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12 Von Frisch, K. Über einen Schreckstoff der Fischhaut und seine biologische Bedeutung: Z vergl Physiol 1941; 29: 46–145.

13 Wilson, EO. The sociogenesis of insect colonies. Science 1985; 228: 1489–95.

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15 Mc Allister MK, Roitberg BD. Adaptive suicidal behaviour in pea aphids. Nature 1987; 328: 797–9.

16 Ressler RH, Cialdini RB, Ghoca ML, Kleist SM. Alarm pheromone in the earthworm Lumbricus terrestris. Science 1968; 161: 597–9.

17 Brown GE, Chivers DP, Smith R, Jan F. Localized defecation by pike: A response to labelling by cyprinid alarm pheromone? Behav Ecol Sociobiol 1995; 36(2): 105–10.

18 Valenta JG, Rigby MK. Discrimination of the odor of stressed rats. Science 1968; 161: 599–601.

19 Carr WC, Martorano RD, Krames L. Responses of mice to odors associated with stress. J Comp Physiol Psych 1970; 71(2): 223–8.

20 Cocke R, Thiessen DD. Chemocommunication among prey and predator species. Anim Learn Behav 1986; 14: 90–2.

21 Aitken RCB. A growing edge of measurement of feelings. P Roy Soc Med 1969; 62: 989–93.

22 Kirschbaum C, Hellhammer DH. Salivary cortisol in psychobiological research: An overview. Neuropsychobiology 1989; 22(3): 150–69.

23 Hubert W, de Jong-Meyer R. Saliva cortisol responses to unpleasant film stimuli differ between high and low trait anxious subjects. Neuropsychobiology 1992; 25: 115–20.

 

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