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The Smell of Death: Evidence that Putrescine Elicits Threat Management Mechanisms

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The ability to detect and respond to chemosensory threat cues in the environment plays a vital role in survival across species. However, little is known about which chemical compounds can act as olfactory threat signals in humans. We hypothesized that brief exposure to putrescine, a chemical compound produced by the breakdown of fatty acids in the decaying tissue of dead bodies, can function as a chemosensory warning signal, activating threat management responses (e.g., heightened alertness, fight-or-flight responses). This hypothesis was tested by gauging people’s responses to conscious and non-conscious exposure to putrescine. In Experiment 1, putrescine increased vigilance, as measured by a reaction time task. In Experiments 2 and 3, brief exposure to putrescine (vs. ammonia and a scentless control condition) prompted participants to walk away faster from the exposure site. Experiment 3 also showed that putrescine elicited implicit cognitions related to escape and threat. Experiment 4 found that exposure to putrescine, presented here below the threshold of conscious awareness, increased hostility toward an out-group member. Together, the results are the first to indicate that humans can process putrescine as a warning signal that mobilizes protective responses to deal with relevant threats. The implications of these results are briefly discussed.
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The Smell of Death: Evidence that Putrescine Elicits Threat Management
Mechanisms
Arnaud Wisman and Ilan Shrira
Journal Name: Frontiers in Psychology
ISSN: 1664-1078
Article type: Original Research Article
Received on: 27 May 2015
Accepted on: 10 Aug 2015
Provisional PDF published on: 10 Aug 2015
Frontiers website link: www.frontiersin.org
Citation: Wisman A and Shrira I(2015) The Smell of Death: Evidence that
Putrescine Elicits Threat Management Mechanisms. Front. Psychol.
6:1274. doi:10.3389/fpsyg.2015.01274
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Emotion Science
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The Smell of Death:
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Evidence that Putrescine Elicits Threat Management Mechanisms
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Arnaud Wisman1*, Ilan Shrira2
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1School of Psychology, University of Kent, Canterbury, Kent, UK
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2Department of Behavioral Sciences, Arkansas Tech University, Russellville, AR, USA
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*Correspondence:
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Dr. Arnaud Wisman
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School of Psychology
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University of Kent
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Canterbury
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Kent CT2 7NP
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United Kingdom
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a.wisman@kent.ac.uk
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Keywords: olfaction, putrescine, threat, threat management, chemosensory cue
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Abstract
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The ability to detect and respond to chemosensory threat cues in the environment plays a vital
24
role in survival across species. However, little is known about which chemical compounds can
25
act as olfactory threat signals in humans. We hypothesized that brief exposure to putrescine, a
26
chemical compound produced by the breakdown of fatty acids in the decaying tissue of dead
27
bodies, can function as a chemosensory warning signal, activating threat management responses
28
(e.g., heightened alertness, fight-or-flight responses). This hypothesis was tested by gauging
29
people’s responses to conscious and non-conscious exposure to putrescine. In Experiment 1,
30
putrescine increased vigilance, as measured by a reaction time task. In Experiments 2 and 3, brief
31
exposure to putrescine (vs. ammonia and a scentless control condition) prompted participants to
32
walk away faster from the exposure site. Experiment 3 also showed that putrescine elicited
33
implicit cognitions related to escape and threat. Experiment 4 found that exposure to putrescine,
34
presented here below the threshold of conscious awareness, increased hostility toward an out-
35
group member. Together, the results are the first to indicate that humans can process putrescine
36
as a warning signal that mobilizes protective responses to deal with relevant threats. The
37
implications of these results are briefly discussed.
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1. Introduction
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When animals die they release an unpleasant smell. A pungent component of this scent is emitted
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by putrescine, a volatile diamine that results from the breakdown of fatty acids in the putrefying
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tissue of dead bodies (Hussain et al., 2013). Interestingly, animal research shows that putrescine
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can function as a powerful chemosensory signal that prompts the perceiver to leave or avoid the
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area (Prounis & Shields, 2013; Yao et al., 2009). The aim of the present research is to show that
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humans respond in a similar way to putrescine, and more generally, that exposure to putrescine
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triggers threat management behaviors (Blanchard et al., 2001; Neuberg et al., 2011).
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A growing body of research suggests that humans can identify threats via chemosignals
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(Ackerl et al., 2002; Chen & Haviland-Jones, 2000; de Groot et al., 2012; Mujica-Parodi et al.,
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2009; Prehn et al., 2006; Zhou & Chen, 2009). For instance, when people are exposed to sweat
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taken from donors during a fearful experience, perceivers show a heightened startle reflex (Pause
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et al., 2009; Prehn et al., 2006) and interpret ambiguous facial expressions as fearful (Zhou &
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Chen, 2009). This transmission of threat-arousing chemosignals is assumed to serve an adaptive
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function by orienting us to impending dangers. Indeed, the ability to detect and process
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chemosensory threat cues is vital for the survival of a wide range of species (Stevenson, 2010).
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However, thus far there is little evidence that humans can, like other organisms, detect olfactory
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threat cues in the environment through means other than the chemosignals (e.g., body sweat) of
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conspecifics.
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The decay of tissue and its resulting scent can function as a necromone cue that signals
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an animal’s death to conspecifics. Alarm and avoidance behaviors (necrophobic behaviors) in
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response to these scents are widespread in the animal kingdom and thought to have evolved at
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least 420 million years ago (Yao et al., 2009). In fact, recent research shows that necrophobic
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behavior may have innate underpinnings through the activation of trace amine-associated
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receptors (TAARs), a group of specialized scent receptors in the olfactory epithelium (Horowitz
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et al., 2014; Hussain et al., 2013; Li & Liberles, 2015). TAARs are known to detect specific
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chemicals that evoke behavioral responses, without the need for prior exposure to the scents. For
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example, in model vertebrates, certain TAARs respond to diamines (e.g., putrescine) by
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producing avoidant behaviors that likely serve to defend against immediate dangers (Yoon et al.,
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2015). Thus, it is feasible that we have a chemosensory sensitivity to diamines like putrescine (Li
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& Liberles, 2015), given that their detection can aid survival (Stevenson, 2010).
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A further advantage of examining putrescine as a threat stimulus is that we know what it
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is. Despite the impressive amount of indirect support for human chemosignals amassed in recent
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years, their chemical properties have yet to be identified (Wyatt, 2009). Focusing on a known
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compound, putrescine, enables us to directly test whether it plays a causal role in human threat
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responses. In a similar vein, although several studies have shown that chemosensory cues can
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elicit greater readiness for behavior (Bradley et al., 2001; Prehn et al., 2005), thus far there is
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little direct evidence that a specific chemical substance can cause overt behavioral changes in
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humans (Wysocki & Preti, 2004). Since exposure to putrescine elicits specific behaviors in
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animals (e.g., escape, avoidance), we can examine whether putrescine produces similar behaviors
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in humans. In sum, putrescine appears to be well-suited to test as a specific chemical compound
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that can act as a threat signal in humans.
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Chemosensory cues can convey danger in at least two fitness-relevant domains: microbial
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and predator threats (Stevenson, 2010). First, olfactory information is often central to identifying
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the presence of pathogens. For example, pathogens can alter the scent of those who become
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3
infected, which can be detected by conspecifics (Arakawa et al., 2010; Olsson et al., 2014; Tybur
1
et al., 2011). Similarly, the release of putrescine in decaying tissue co-occurs with the arrival of
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bacteria, a motivation for others to eschew physical contact with the dead body. A number of
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species exhibit necrophobic behaviors, and after detecting the scent emanating from dead bodies,
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usually respond by leaving or avoiding the area (Prounis & Shields, 2013). Second, putrescine
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released by decaying bodies can signal the risk of predation (Boissy et al., 1986). Since a large
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proportion of deaths in the wild are the result of predator attacks, putrescine would be a useful
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alarm cue to stay away (Misslin, 2003).
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In humans, responses to specific scents can develop through learned associations between
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odors and personal experiences (Degel et al., 2001; Stevenson et al., 1998). For example, based
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on the cultural expression that when “something smells fishy” it is viewed suspiciously, exposure
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to fish-like odors arouses suspicion toward others and reduces cooperation, an orientation that is
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assumed to result from conditioned reactions to this scent (Lee & Schwarz, 2012). Since
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putrescine can emanate from various sources (Yeoman et al., 2013), people may learn to
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associate the smell of putrescine with threats, and it is plausible that occasional exposure to
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putrescine, whenever it occurs, could lead to conditioned threat responses (Stevenson, 2010).
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However, we render it unlikely that modern humans have strong conscious meaningful
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associations with the scent of putrescine. Moreover, conscious scent evaluations are often
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inaccurate, context dependent, and colored by other sensory modalities (Sela & Sobel, 2010). In
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view of this, it is important to note that responses to aversive chemosensory cues do not require
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prior learning or conscious evaluation (Dielenberg et al., 2001; Li et al., 2013; Miller & Maner,
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2010). Indeed, scents can alter our perception, cognition, behavior, and physiology (e.g., heart
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rate, skin conductance) even when there is no conscious scent detection (Krusemark & Li, 2012;
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Li et al., 2007; Pause et al., 2009; Sela & Sobel, 2010), and even after olfactory adaptation has
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set in (de Groot et al., 2012; Smeets & Dijksterhuis, 2014). Thus, neither prior associations with
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olfactory signals, nor conscious processing, are necessary conditions for people to process them
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as threatening (Pause, 2012; Williams et al., 2006; Köster, 2002; Sela & Sobel, 2010; Smeets &
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Dijksterhuis, 2014).
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At the most basic level, threat detection increases vigilance and sharpens our reactions to
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events in the environment (Williams et al., 2006). For instance, detection of a predator’s scent
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will interrupt foraging and increase behaviors (e.g., scanning the environment) that facilitate
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predator detection (Woody & Szechtman, 2011). Once the threat management system is
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engaged, it produces readiness for fight-or-flight behaviors (Blanchard et al., 1986; Cannon,
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1927; Gray & McNaughton, 2003; Mobbs et al., 2009). Flight responses seek to escape the
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situation, whereas fight responseswhether physical or verbal aggressionare typically only
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used when escape is not possible. In contrast to popular belief that the dominant response to
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threats is to fight, flight is actually far more common (Misslin, 2003), presumably because nature
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selects more strongly for strategies that minimize risk. In one study, for example, when people
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were confronted by a threatening out-group member, they responded with aggressive readiness
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(fight), but only when there was little possibility of escaping; when given the option, though,
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participants chose to distance themselves (flight) from the other person (Cesario et al., 2010).
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2. Overview and Hypotheses
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Coming full circle, we propose that putrescine can serve as a (non-conscious) signal that initiates
1
threat management responses. Specifically, we hypothesize that brief exposure to putrescine
2
increases vigilance, followed by the readiness to either escape (flight), or engage in aggressive
3
readiness (fight) when escape is not possible. Experiment 1 assessed whether putrescine (vs.
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ammonia and a neutral scent) increased vigilance as measured by faster responses in a simple
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reaction time task. Experiments 2 and 3 assessed whether brief exposure to putrescine (vs.
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ammonia and neutral scent) caused participants to walk away faster from the exposure site after
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completing the experiment (outdoors). Experiment 3 also tested whether putrescine evoked
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cognitions related to escape and threat. Finally, Experiment 4 examined whether non-conscious
9
exposure to putrescine increased aggressive readiness (e.g., defensiveness toward an out-group
10
member). All four experiments adhered to the Declaration of Helsinki guidelines, and gained the
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prior approval by the University Research Ethics Committee. Written consent was obtained from
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all participants involved in these experiments, and all were fully debriefed.
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3. Experiment 1: The effect of putrescine on vigilance
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In Experiment 1, we tested whether brief exposure to putrescine increased vigilance. To measure
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vigilance, we employed a task closely modeled after the shortened version of the Psychomotor
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Vigilance Task (PVT; Dinges & Powell, 1985) that assessed participants reaction times to a red
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dot that was presented at random intervals on a computer screen.
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In addition, Experiment 1 was designed to determine whether ammonia served as an
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appropriate aversive control condition. Our pilot testing revealed that ammonia, unlike other
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aversive scents we had examined (i.e., skatole
1
and indole), was rated similarly to putrescine on
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repugnance, familiarity, and intensity. Moreover, previous research has used ammonia (NH3;
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ammonium hydroxide) as an aversive scent prime (Rieser et al., 1976; Wise et al., 2005).
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Furthermore, ammonia can increase trigeminal nerve activation associated with vigilance and
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sensory rejection, via activation of the sympathetic nervous system (Hummel & Kobal, 1992;
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Sekizawa & Tsubone, 1994). However, some research suggests that unpleasant ambient odors
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can also decrease reaction times on simple tasks like the current PVT (Millot et al., 2002). In
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view of this, we made no specific prediction about whether ammonia, like putrescine, would
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enhance vigilance relative to our scentless control condition.
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3.1. Method
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3.1.1. Participants and Procedure
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A sample of sixty participants (43 females; Mage = 21.20, SD = 3.20) completed the study in
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return for a financial incentive of 3 pounds (approximately $5).
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1
In line with previous research (Wheatley & Haidt, 2005), we pilot-tested the so-called “fart spray” along with
skatole, indole, and ammonia, for suitability as an aversive control condition. These ratings are presented in Table 1.
As can be seen, ammonia and fart spray were rated similarly to putrescine on all three dimensions of repugnance,
familiarity, and intensity, whereas indole and skatole diverged from putrescine on at least one dimension. A
disadvantage of fart spray, however, is that we could not ascertain its precise chemical compoundsits
manufacturers were reluctant to disclose this information.
5
Participants were randomly assigned to one of three conditions: putrescine (C4H12N2;
1
Sigma-Aldrich), ammonia (5%; NH3; Sigma-Aldrich), or water. One hour before the start of the
2
experiment, cotton wool pads were blotted with 2 ml of one of the three compounds, and stored
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separately in small (100 ml) sealable amber jars. Participants were run in our lab individually,
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and seated in different cubicles to avoid carryover effects of scents. The refreshment rate in each
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cubicle was 4 to 5 air changes (cycles) per hour. Furthermore, participants were booked at least
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30 minutes apart in order to ventilate the rooms—by opening the lab room’s window—between
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sessions. When preparing materials for the experiment, one of the researchers marked the bottom
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of each jar with a number code, so that the experimenters were unaware of the meaning of these
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codes. This basic procedure was repeated in our subsequent experiments to keep the
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experimenters blind to the conditions.
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Participants were seated in front of a standard PC (equipped with Authorware 7.1
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software) with a 17-inch screen. They were given instructions (on-screen) to open the jar, sniff
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the scent inside for 10 seconds, and close the jar. After that, they rated the scent on its intensity
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(“This scent is intense”; 1 = strongly disagree and 9 = strongly agree), repugnance (“This scent
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is repugnant”; 1 = strongly disagree and 9 = strongly agree), and familiarity (“This scent is
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familiar”; 1 = strongly disagree and 9 = strongly agree). Repugnance was included as evaluative
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rating (alongside the standard measures of intensity and familiarity) because repugnance (or
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disgust) is often a central component of aversive scents. Participants were then introduced to the
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adapted PVT, which lasted about five minutes (see Loh et al., 2004). The task instructed them to
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click on a red dot as quickly as possible whenever they saw the dot on the screen. Ten dots (each
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measuring 1 cm) were shown at different locations on the screen, and the time between
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appearances was randomized at variable intervals (2-45 sec). As soon participants clicked on the
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red dot with the mouse, a screen appeared for five seconds with the message: prepare for next
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trial. Participants received two practice trials first, to get them familiar with the main task of ten
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trials. Finally, after completing the PVT and filling out a standard demographic questionnaire,
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they were fully debriefed and thanked for their participation.
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3.2. Results and Discussion
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3.2.1. Hedonic Evaluations
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We began by testing our prediction, based on our pilot testing, that putrescine and ammonia
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would not differ from each other on repugnance, familiarity and intensity. As predicted, separate
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one-way between-subjects ANOVAs revealed that there was no significant difference between
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ammonia and putrescine on repugnance, F(1, 38) = 0.38, p = .54, η² = .01, familiarity, F(1, 38) =
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0.26, p = .26, η² = .03, or intensity, F(1, 38) = 0.14, p = .71, η² = .004 (see Table 2, for
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descriptive statistics). Moreover, the analyses reported below were not altered when entering all
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hedonic evaluations as covariates.
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3.2.2. Reaction Times
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We examined our main prediction that putrescine, relative to the neutral control condition
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(water), would elicit faster reaction times. In line with previous PVT research, we applied
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reciprocal transformation to the raw data (i.e., 1/RT). This type of transformation is standard
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within the PVT paradigm, as it reduces the impact of extreme scores and brings them into an
46
6
acceptable range (Dinges et al., 1987; Dorrian et al., 2004). A one-way between-subjects
1
ANOVA revealed a difference between the scent conditions, F(2, 57) = 4.32, p = .018, η² = .13.
2
Post hoc comparisons, with the raw means reported here, showed that putrescine produced faster
3
reaction times (M = 1.04, SD = .10) than the neutral scent (M = 1.24, SD = .35; p = .013), but not
4
compared to ammonia (M = 1.12, SD = .20; p = .28). No difference was found between the
5
neutral and ammonia conditions (p = .14).
6
7
In sum, only putrescine caused participants to react more quickly compared to the neutral
8
condition, supporting our hypothesis that putrescine increases vigilance. At the same time,
9
ammonia did not increase vigilance relative to the scentless control condition. Importantly, the
10
findings show that, consistent with our pilot study, ammonia and putrescine are evaluated similar
11
on repugnance, familiarity, and intensity, and were similar in the degree of vigilance they
12
elicited. Consequently, together with previous research (Rieser et al., 1976; Wise et al., 2005),
13
Experiment 1 indicated that ammonia would serve as an appropriate aversive control condition.
14
Experiments 2 and 3 investigated our hypothesis that putrescine activates the motivation to
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escape the situation (flight).
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4. Experiment 2: The effect of putrescine on escape behavior
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Similar to Experiment 1, Experiment 2 first asked participants to rate a scent prime (putrescine
20
vs. ammonia vs. neutral) on three dimensions: intensity, familiarity, and repugnance, then we
21
observed whether it influenced the tendency to escape the situation. To avoid the biases
22
associated with some operationalizations of flight in prior research (e.g., self-reported intentions,
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Gilbert & Gilbert, 2003), we employed an overt behavioral measure of escape (e.g., Ellsworth et
24
al., 1972; Wisman & Koole, 2003). Specifically, we assessed whether putrescine would cause
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participants (who were under the impression the study was finished) to walk away more quickly
26
over a predetermined distance of 80 meters.
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4.1. Method
29
30
4.1.1. Participants and Procedure
31
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Forty-five participants (21 females and 24 males; Mage = 27.51, SD = 9.72) completed the study
33
on campus. We filled three empty felt-tip pens, each with one of the three compounds
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(putrescine, ammonia, or water). To fill each pen, 10ml of liquid odor was injected onto the
35
pen’s fiber rod inside the pen. The pens were then re-assembled and left to stand upside down for
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24 hours in order to allow the liquid to soak into the fiber rod. Just before the start of the
37
experiment, scent blotters were marked with the scent marker pens and stored in separate
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sealable containers.
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Participants were approached on a fixed spot on the campus and asked if they had time to
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participate in a brief scent test of approximately ten minutes. Participants were tested
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individually and randomly assigned to one of three conditions (putrescine, ammonia, or water).
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The experimenter, blind to the conditions, presented one of the three containers to the
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participant, who rated the scent on intensity (“This scent is strong”; 1 = strongly disagree and 5
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= strongly agree), repugnance (“This scent is repugnant”; 1 = strongly disagree and 5 = strongly
46
7
agree), and familiarity (“This scent is familiar”; 1 = strongly disagree and 5 = strongly agree).
1
After finishing and being thanked for their participation, a second experimenter blind to the
2
condition and hypotheses of the experiment and out of sight of the participants used a standard
3
stopwatch to time how many seconds it took participants to walk away over a distance of 80
4
meters (pre-measured before the experiment began). The recorded time constituted our
5
dependent variable. After they reached this distance, participants were re-approached, fully
6
debriefed and thanked again.
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4.2. Results and Discussion
9
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4.2.1. Hedonic Evaluations
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Consistent with Experiment 1, separate one-way between-subjects ANOVAs revealed that there
13
was no significant difference between ammonia and putrescine on repugnance, F(1, 28) = 2.30, p
14
= .14, η² = .07, and familiarity, F(1, 28) = 0.04, p = .75, η² = .01. However, ammonia was rated
15
as relatively more intense (M = 4.73; SD = 0.46) compared to putrescine (M = 4.27; SD = 0.70; p
16
= .04; see Table 3). Once again, the results reported below were not altered when we entered the
17
intensity (nor the other hedonic) ratings into the analyses as covariates. We also note that the
18
results are similar whether participants rate how “intense” or “strong” the scent smells (see
19
Experiment 3 below).
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4.2.2. Escape Behavior
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To test our hypothesis that putrescine elicited an escape motivation, we compared our scent
24
conditions in a one-way ANOVA, using gender as a covariate
2
. The results yielded a significant
25
effect of the scent prime on the time it took to walk 80 meters, F(2, 41) = 19.03, p < .001, η² =
26
.48. The only significant differences occurred between putrescine (M = 56.40 seconds; SD =
27
4.19) and ammonia (M = 59.93, SD = 5.04), and between putrescine and the neutral scent prime
28
(M = 60.00, SD = 4.42; both ps < .005; see Figure 1). Thus, putrescine caused participants to
29
walk away more quickly, supporting our assumption that putrescine evoked a stronger
30
motivation to escape. Experiment 3 was conducted to replicate this finding, and furthermore to
31
test whether putrescine elicited implicit cognitions related to escape and threat.
32
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5. Experiment 3: The effect of putrescine on escape behavior and thoughts
34
35
The procedure for Experiment 3 was similar to Experiment 2’s. First, we asked participants to
36
evaluate the scents on the different dimensions (repugnance, familiarity, intensity). In addition,
37
we gauged participants’ implicit threat-related associations using a word stem-completion task.
38
Specifically, this task measured the implicit accessibility of thoughts related to “escape” and
39
threat.” We predicted that only putrescine would increase the accessibility of these cognitions.
40
Finally, we assessed whether putrescine would cause participants to walk away more quickly
41
over a predetermined distance of 60 meters.
42
2
Because previous research has shown that men and women tend to walk at different speeds (Chumanov, Wall-
Scheffler, & Heiderscheit, 2008), the results of Experiments 2 and 3 included gender as a covariate. In addition, we
analyzed the results of Experiments 2 and 3 with gender as a separate factor and this did not alter the significance of
the results.
8
1
5.1. Method
2
3
5.1.1. Participants and Procedure
4
5
Sixty participants (32 females and 28 males, Mage = 21.57, SD = 1.12) completed the study on
6
campus. Individuals were approached just outside campus on a path sloping downhill and asked
7
if they had time to participate in a brief scent test for about 15 minutes.
8
9
Participants were randomly assigned to one of the three scent conditions, then they rated
10
the scent on intensity, repugnance, and familiarity (“This scent is intense”; 1 = strongly disagree
11
and 9 = strongly agree), repugnance (“This scent is repugnant”; 1 = strongly disagree and 9 =
12
strongly agree), and familiarity (“This scent is familiar”; 1 = strongly disagree and 9 = strongly
13
agree). Then, to assess cognitions relevant to the concepts of “escape” and “threat, participants
14
completed the word-stem completion task, a widely used and well-established measurement that
15
gauged the thought accessibility of these two concepts (Arndt et al., 1997; Greenberg et al.,
16
1994; Lozito & Mulligan, 2010; Migo et al., 2010). Participants were asked to complete 30 word
17
fragments, 20 of which were neutral (e.g., B_ NK could be BANK or BUNK) in terms of any
18
particular theme, five of which could be words related to escape (e.g., the fragment RU_ could
19
be completed as RUN or RUB, the latter a neutral word), and another five could be completed
20
with a word related to threat (e.g., _ _ RROR could be TERROR or MIRROR). We summed
21
the number of escape- (M = 2.73, SD = 1.07) and threat-related words (M = 1.90, SD = .66) that
22
participants completed to assess the thought accessibility of these concepts. Finally, participants
23
were again timed by a second experimenter, who was blind to the conditions and the hypotheses,
24
for how long it took them to walk away over a distance of 60 meters (Due to natural constraints a
25
slightly shorter distance than in Experiment 2).
26
27
5.2. Results and Discussion
28
29
5.2.1. Hedonic Evaluations
30
31
Separate one-way between-subjects ANOVAs revealed no difference between the chemosensory
32
primes on repugnance, F(1, 38) = .35 , p = .56, η² = .01, familiarity, F(1, 38) = .04, p = .85, η² =
33
.001, and intensity, F(1, 38) = 0.29, p =.59, η² = .008 (see Table 4). Thus, participants rated
34
ammonia and putrescine similarly to one another on intensity, repugnance, and familiarity.
35
Again, the results reported below were did not differ when we entered the hedonic evaluations
36
into the analyses as covariates.
37
38
5.2.2. Escape- and Threat-Related Cognitions
39
40
To test our hypothesis that putrescine elicited implicit cognitions related to escape and threat, we
41
analyzed the escape and threat word-completion results separately. The results revealed a
42
significant effect of scent prime on escape thought accessibility, F(2, 57) = 10.90, p < .001, η² =
43
.28 (see Table 5). Putrescine caused participants to complete word stems more frequently with
44
escape related words (M = 3.45, SD = .69) than both the ammonia (M = 2.45, SD = 1.05) and the
45
neutral scent (M = 2.15, SD = .99) primes (both ps < .005). Similarly, the scent primes affected
46
9
the accessibility of threat-related thoughts, F(2, 57) = 8.39, p < .001, η² = .23. Putrescine led to
1
more threat word-stem completions (M = 2.55, SD = .94) than ammonia (M = 1.73, SD = .64)
2
and the neutral scent (M = 1.68, SD = .65; all ps < .005).
3
4
5.2.3. Escape Behavior
5
6
Like Experiment 2, the analyses showed a significant effect of chemosensory primes on walking
7
speed, F(2, 56) = 9.11, p < .001, η² = .24 (see Figure 2). The pattern of results again showed that
8
putrescine (M = 33.38, SD = 2.99) caused people to walk more quickly than ammonia (M =
9
35.92, SD = 3.38) and the neutral scent prime (M = 37.67, SD = 3.13; p < .05). Again, no
10
difference was found between the ammonia and the neutral scent condition (p = .87).
11
12
Experiment 3 revealed that putrescine elicited implicit cognitions of escape and threat. In
13
addition, Experiment 3 replicated the finding that putrescine increased walking speed. Thus,
14
taken together, the results of Experiments 2 and 3 indicated that putrescine motivated (automatic)
15
escape behavior. An important feature of the settings in Experiments 2 and 3 was that
16
participants were outdoors and in a context that facilitated the possibility that they could distance
17
themselves from the scent.
18
19
6. Experiment 4: The effects of putrescine on defensive responses toward an out-group
20
21
Experiment 4 sought to extend our understanding of the effects of putrescine in two important
22
respects. First, we tested the hypothesis that non-conscious (unobtrusive) exposure to putrescine
23
could elicit threat management responses. As we highlighted in the Introduction, this possibility
24
is consistent with evidence that scent primes, even when presented at sub-threshold levels, can
25
influence brain activation (Sobel et al., 1999), learning (Koster et al., 2002), and physiological
26
state (Stern & McClintock, 1998). This applies similarly to aversive scent primes, which for
27
example, have the ability to alter skin conductance (Jacquot et al., 2004), social preferences (Li
28
et al., 2007), and cognitive performance (Epple & Herz, 1999) in ways that correspond to
29
supraliminal exposure to aversive stimuli (Sela & Sobel, 2010). Thus, we predicted that
30
subliminal presentation of putrescine would be capable of activating threat responses.
31
32
Second, Experiment 4 focused on the fight rather than the flight component of alarm
33
responses. Consistent with previous research showing that implicit threat cues increase
34
intolerance toward out-group members (Holbrook et al., 2011) and defensive responses
35
(Blanchard et al., 2001; Wheatley & Haidt, 2005), we hypothesized that putrescine would
36
increase defensiveness toward an out-group member, in a situation where there was no
37
immediate opportunity to escape (Cesario et al., 2010). Like Experiment 1, we conducted this
38
experiment in a laboratory setting. After priming the participants with one of the scents, they
39
filled out a standard positive and negative affect scale that gauged their mood. Although, our
40
pilot study (see Table 1) and some research (e.g., Knasko, 1993) revealed that aversive scent
41
primes do not alter mood on a conscious level, we intended to rule out the possibility that the
42
subliminal primes influenced participants’ feelings at a conscious level. After that, they read
43
about an out-group member—a foreign student who criticized the participants’ value system—
44
and were asked to evaluate the target. This evaluation was designed to assess how much hostility
45
participants felt toward the target.
46
10
1
6.1. Method
2
3
6.1.1. Participants and Procedure
4
5
Sixty-nine participants (39 females and 30 males, Mage = 24.00, SD = 8.38) were run in our lab
6
individually, in different cubicles (randomized) to avoid carryover effects of scents. Furthermore,
7
participants were booked at least 30 minutes apart in order to ventilate the rooms between
8
sessions. Upon arrival, participants were given the first of two questionnaire packets to complete.
9
This first questionnaire consisted of demographic questions and a number of filler items. We
10
then randomly assigned participants to their condition by marking one of the three liquid scents
11
(putrescine, ammonia, water) to the top of each page (0.5 ml) of the second questionnaire
12
participants were given. In the putrescine and ammonia conditions, this amounted to a very
13
subtle scent prime that was not meant to be detected. At the conclusion of the experiment, we
14
funnel debriefed participants to determine whether they noticed or smelled anything unusual
15
during the study. None of them reported being aware of the scents.
16
17
The second questionnaire assessed participants’ mood, and our dependent variables. First,
18
to rule out the possibility that our results could be explained by generalized affect, participants
19
began the second part of the questionnaire by completing the 20-item Positive and Negative
20
Affect Scale (PANAS; Tellegen et al., 1988). This scale measured the extent to which each of 10
21
positive affect descriptors (α = .86) and 10 negative affect descriptors (α = .85) reflected how
22
they felt at that moment (1 = very slightly or not at all, 5 = extremely). We computed the average
23
positive affect (M = 3.31, SD = .68) and negative affect (M = 1.61, SD =.59) scores for
24
everybody.
25
26
This was followed by the description and evaluation of the out-group member (Greenberg
27
et al., 2001; Navarrete et al., 2004; Norenzayan et al., 2007). Specifically, participants read an
28
essay supposedly written by a college student from the Middle East who was visiting the United
29
Kingdom to study English. In this essay, the student went on to criticize Western values,
30
predicting its eventual decline (see Norenzayan et al., 2007). Participants were then asked to
31
evaluate the author and his message by responding to four questions on a 9-point Likert scale
32
(To what extent do you like the author”; ‘To what extent would you like to be friends with the
33
author; How much would you oppose the author teaching your (future) children”; and How
34
much do you want the ideas of the author to be publicized; 1 = very much, 9 = not at all). We
35
derived an overall out-group hostility index (M = 5.82, SD = 1.63) by averaging all items
36
together (α = .77), such that larger values indicated greater hostility. Finally, we measured
37
motivation to escape the situation by timing how long it took participants to complete the second
38
(scented) questionnaire followed by a standard demographic questionnaire (91% of the
39
participants were native to England, 3% Greece, 4% Ireland, and 1% to the United States).
40
41
6.2. Results and Discussion
42
43
6.2.1. Ancillary Analyses
44
45
11
A one-way ANOVA tested whether the chemosensory primes elicited different levels of self-
1
reported affect across the three conditions. However, the primes had no impact on positive affect
2
F(2, 66) = 1.87, p >.16, nor negative affect, F(2, 66) = .36, p > .70. Moreover, the analyses
3
below were no different when we used these affect measures as covariates, showing that any
4
effect of our primes on out-group defense was not mediated by mood.
5
6
6.2.2. Out-group Defense
7
8
As predicted, we found a significant effect of scent prime on defensiveness toward the author of
9
the essay, F(2, 66) = 11.83, p < .001, η² = .26 (see Figure 3). Post-hoc analyses found that
10
putrescine led to greater hostility (M = 6.98, SD = 1.42) compared to ammonia (M = 5.05, SD =
11
1.54) and the neutral conditions (M = 5.43, SD = 1.30; both ps < .005). There was no significant
12
difference between the ammonia and control conditions, p > .6.
13
14
Experiment 4 supported the hypothesis that non-conscious exposure to putrescine evoked
15
defensive responses toward an out-group member, and this effect was not due to conscious
16
awareness of the scents, mood, or to the motivation to escape the aversive scent primes
3
.
17
Although these results suggest that the scent primes elicited an odor percept (non-consciously),
18
future studies may wish to control the precise intensities of the stimulus odors that are presented
19
(e.g., using an olfactometer).
20
21
7. General Discussion
22
23
This research was designed to test the hypothesis that putrescine could serve as a warning signal
24
that mobilizes protective responses to deal with threats. In four experiments, we found support
25
for this idea: conscious and non-conscious exposure to putrescine elicited distancing and
26
defensive reactions (e.g., fight and flight responses). Putrescine increased vigilance (Experiment
27
1), heightened the accessibility of escape- and threat-relevant cognitions (Experiment 3), and
28
increased the speed participants walked away from the location of the scent (Experiments 2 and
29
3). Experiment 4 created a situation where immediate escape was not likely and gave participants
30
the opportunity to evaluate an out-group member. Subtle exposure to putrescine produced greater
31
defensiveness toward the out-group member, suggesting an aggressive readiness in participants
32
(Cesario et al., 2010). As a whole, the findings indicate that even brief exposure to putrescine
33
mobilizes threat management responses designed to cope with environmental threats.
34
35
These are the first results to show that a specific chemical compound (putrescine) can be
36
processed as a threat signal. Thus far, nearly all the evidence for threat chemosignals has come
37
from those that are transmitted by body sweat (de Groot et al., 2012; Pause et al., 2012).
38
Moreover, these are among the first studies that show that a specific chemical compound can
39
cause overt behavior in humans (Wysocki & Preti, 2004). Furthermore, an advantage of isolating
40
putrescine in threat management processes is that it may help in determining which sensory and
41
brain pathways are involved in chemosensory threat detection and processing. For instance,
42
research suggests that the central nucleus of the amygdala projects to the midbrain
43
3
When the amount of time participants took to complete the questionnaire was used as a covariate, the results
remained significant, F(2, 65) = 13.13, p < .001, η² = .29).
12
periaqueductal gray, the hypothalamus and the brainstem, which together coordinate to prepare
1
fight-or-flight responses to threatening stimuli (Misslin, 2003). We speculate that putrescine
2
activates a similar neurological pathway. Future research could include physiological
3
measurements (e.g., systolic blood pressure, heart rate) to test the thesis that the observed effects
4
of putrescine are modulated by processes originating in the sympathetic nervous system.
5
6
An important direction for future research will be to understand the precise nature of the
7
threat produced by putrescine (e.g., microbial, predatory). Our view is that putrescine is relevant
8
to both of these domains, though the immediate context should determine which type of threat is
9
more primary. Recent work on trace amine receptors (TAARs) has the potential to shed light on
10
some of these mechanisms, as the activation of different receptors may function to detect specific
11
threats, such as predators and pathogens (Li & Liberles, 2015; Pérez-Gómez et al., 2015). In
12
addition, this research suggests that cadaverine (a compound with a similar chemical structure as
13
putrescine; both are diamines) activates a similar pathway and produces similar escape and
14
avoidance responses (Hussain et al., 2013; Oliveira et al., 2014) in animals. Thus, we render it
15
likely that cadaverine evokes a similar threat response as putrescine (see Li & Liberles, 2015).
16
17
It would also be interesting to examine how putrescine detection affects sensitivity to
18
particular types of threat and whether it produces elevated responses to certain stimuli more than
19
others (e.g., fear- vs. disgust-based sensitivities). For instance, further research could elucidate
20
how putrescine activates sensory acquisition (typically associated with fear experiences) and
21
sensory rejection (associated with disgust) processes (Susskind et al., 2008), and whether
22
exposure to putrescine augments physiological responses (e.g., heart rate, pupil dilation) that
23
typically co-occur with adaptive responses to threats. This type of research would benefit from
24
including individual differences in both disgust and fear sensitivity (Garfinkel et al., 2014; Haidt
25
et al., 1994). By the same token, future work could clarify whether putrescine elicits discrete
26
emotions (e.g., fear versus disgust) or less specific affective states associated with negative
27
valence and high arousal (see also Li & Liberles, 2015; Smeets & Dijksterhuis, 2014). Our
28
findings, which showed that responses to putrescine were automatic, occurred after various
29
lengths of delay (Experiments 1-3), and when presented at sub-threshold levels (Experiment 4),
30
suggested that conscious evaluations are not at the heart of the observed responses to putrescine.
31
This is consistent with our theorizing and ample work showing that chemosensory cues influence
32
psychological and physiological operations outside conscious awareness (for extended reviews,
33
see Sela & Sobel, 2010; Smeets & Dijksterhuis, 2014). However, we hasten to add that more
34
research is needed to specify the exact nature of the effects produced by the sub-threshold
35
priming of putrescine, for instance, by varying the exposure times to putrescine, the delay after
36
the primes, and the intensity of the putrescine stimulus.
37
38
Another important question is how specific threat management responses develop.
39
Within non-olfactory sensory channels, for example, there may be an innate bias for humans to
40
detect certain biologically-relevant stimuli as threatening, such as the sight of snakes and spiders
41
(Ohman & Mineka, 2001). Although controversial in human research, some work suggests that
42
responses to chemosensory stimuli are innate (Hussain et al., 2013; Misslin, 2003; Dielenberg et
43
al., 2001). For instance, Soussignan et al. (1997) showed that soon after birth, butyric acid (a
44
malodorous scent) evoked disgust reactions in neonates, a finding they claim is consistent with
45
an innate predisposition toward ecologically-relevant scents. To test for possibility of innate
46
13
biases toward threatening chemosensory cues, it would be interesting to examine whether
1
putrescine triggers facial expressions associated with fear in infants. In fact, research indicates
2
that adults do not habituate so readily to the scent of putrescine emitted from rotting flesh
3
(Roberson et al., 2008), suggesting that there might be a bias to respond warily to it.
4
5
Although the innateness of responses to chemosignals is still controversial, humans
6
ability to incorporate learned information into cultural practices is beyond question (Boyd &
7
Richerson, 2005). Consequently, the magnitude of specific chemosensory threat responses could
8
be different in cultures where people are exposed to putrescine more frequently. Likewise,
9
reactions to putrescine may differ between cultures with different burial practices (e.g.,
10
embalming practices, the duration before burial). These factors should remind us that the context
11
is critical to how people react to putrescine. How olfactory information modulates other sensory
12
inputs (Zhou et al., 2012) is no doubt central to whether it will be interpreted as threatening.
13
14
One alternative theoretical perspective of our findings on the effects of putrescine is
15
Terror Management Theory (TMT; Greenberg et al., 1994). According to this theory, reminders
16
of death are regulated by a cultural anxiety buffer that consists of beliefs and values that imbue
17
life with meaning and the promise of immortality. Interestingly, TMT argues that a great deal of
18
the darker side of human behavior (e.g., aggression, out-group prejudice, religious intolerance)
19
stems from the need to maintain and defend the integrity of this cultural anxiety buffer, due to its
20
vital role in managing existential angst. In this view, putrescine could function as a reminder of
21
mortality, and subsequently elicits similar defensive processes, as activated by reminders of
22
death. We do not rule out this possibility, but render it unlikely that chemosensory threats trigger
23
the same type of processes as those that originate from the unique human ability to reflect on the
24
conundrum of life and death (Landau et al., 2007). Nevertheless, examining whether putrescine
25
can be used as a subtle reminder of death, and whether it influences cultural beliefs, values, and
26
practices, would open up fascinating directions of research.
27
28
Most research has shown that humans process threats either visually or audibly, while
29
other animals inhabit the inaccessible world of scents. At the same time, we know that humans
30
are guided by many of the same olfactory processes, especially when they involve fitness-
31
relevant information. We believe that by identifying putrescine as one of these signals, a further
32
understanding of its mechanisms can shed light on more general processes that modulate
33
chemosensory signaling and threat management responses.
34
35
36
14
8. Conflict of Interest Statement
1
2
The authors declare that the research was conducted in the absence of any commercial or
3
financial relationships that could be construed as a potential conflict of interest.
4
5
6
15
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Table 1
1
Hedonic evaluations of putrescine, ammonia, indole, “fart spray,” and skatole1 (Pilot study).
2
3
Scent primes Putrescine Ammonia Indole Skatole Fart spray
4
5
Intensity2
6
M 5.98b 6.60b 5.25a 7.23c 5.52b
7
SD 2.50 2.46 2.15 2.08 2.07
8
Familiarity
9
M 4.98a 5.10a 6.88b 5.21a 4.90a
10
SD 2.71 2.95 2.46 2.56 2.69
11
Repugnance
12
M 5.94b 5.94b 3.65a 6.54b 5.31b
13
SD 2.65 2.55 1.78 2.94 2.63
14
Positivity
15
M 2.63b 2.69b 3.81a 2.50b 2.67b
16
SD 1.55 1.78 2.05 1.87 1.77
17
N 48 48 48 48 48
18
19
20
1 “How intense is this scent?”, 1 = Not at all and 10 = Very much; “How familiar is this
21
scent?”, 1 = Not at all and 10 = Very much; “How repugnant is this scent?”, 1 = Not at all and 10
22
= Very much; “How positive does this scent make you feel?”, 1 = Not at all and 10 = Very much.
23
2 Different subscripts on a hedonic dimension (within a row) indicate a significant
24
difference of p < .05.
25
26
27
21
Table 2
1
Scent ratings for the chemosensory primes (Experiment 1)
2
3
Chemosensory primes Neutral Ammonia Putrescine
4
5
Intensity
6
M 3.30 4.73 4.27
7
SD 1.81 1.45 1.92
8
9
Familiarity
10
M 6.00 5.10 4.40
11
SD .86 2.25 1.60
12
13
Repugnance
14
M 2.35 5.90 5.65
15
SD 1.46 1.34 1.23
16
N 20 20 20
17
18
22
Table 3
1
Scent ratings for the chemosensory primes (Experiment 2)
2
3
Chemosensory primes Neutral Ammonia Putrescine
4
5
Intensity
6
M 1.53 4.73 4.27
7
SD .64 .46 .70
8
9
Familiarity
10
M 4.75 1.60 1.67
11
SD .46 .51 .62
12
13
Repugnance
14
M 1.73 4.47 4.80
15
SD .70 .74 .41
16
N 15 15 15
17
18
23
Table 4
1
Scent ratings for the chemosensory primes (Experiment 3)
2
3
Chemosensory primes Neutral Ammonia Putrescine
4
5
Intensity
6
M 1.85 3.20 3.40
7
SD .99 1.32 .99
8
9
Familiarity
10
M 2.95 2.20 2.15
11
SD .83 .89 .75
12
13
Repugnance
14
M 2.60 3.70 3.50
15
SD .60 .98 1.15
16
N 20 20 20
17
18
19
24
Table 5
1
The ratings of escape-related and threat-related cognitions for the chemosensory primes
2
(Experiment 3).
3
4
Chemosensory primes Neutral Ammonia Putrescine
5
6
Escape cognitions
7
M 2.15 2.45 3.45
8
SD 0.99 1.05 0.69
9
10
Threat cognitions
11
M 1.68 1.73 2.55
12
SD 0.65 0.64 0.94
13
N 20 20 20
14
15
25
1
2
3
Figure 1. The number of seconds it took participants to walk 80 meters after exposure to the
4
scent prime (Experiment 2). Asterisks denote that two groups differ at **p < .005.
5
6
7
8
**
**
50
55
60
65
neutral ammonia putrescine
Walking time in seconds
26
1
2
3
4
Figure 2. The number of seconds it took participants to walk 60 meters after exposure to the
5
scent prime (Experiment 3). Asterisks denote that two groups differ at *p < .05.
6
7
8
9
10
11
12
*
*
25
30
35
40
neutral ammonia putrescine
walking time in seconds
27
1
2
3
Figure 3. Mean scores on the worldview defense scale for all three conditions (Experiment 4).
4
Higher scores reflect greater hostility toward the target. Asterisks denote two groups differ at **p
5
< .005.
6
7
8
9
10
11
**
**
0
1
2
3
4
5
6
7
8
9
neutral ammonia putrescine
outgroup defense

Supplementary resource (1)

... Modern mechanisms of putrescine action may involve scent receptors called trace amine-associated receptors, which are associated with innate behavioral responses to olfactory chemosignals (Hussain et al. 2013). Wisman and Shrira (2015) found that subliminal exposure to putrescine increased behaviors related to threat management: vigilance, flight behaviors, and outgroup hostility. One theoretical explanation of these findings is in evolutionary theoryhuman beings may have an inborn evolutionary mechanism that prompts us to avoid the smell of decay (Wisman & Shrira, 2015). ...
... Wisman and Shrira (2015) found that subliminal exposure to putrescine increased behaviors related to threat management: vigilance, flight behaviors, and outgroup hostility. One theoretical explanation of these findings is in evolutionary theoryhuman beings may have an inborn evolutionary mechanism that prompts us to avoid the smell of decay (Wisman & Shrira, 2015). Our innate response to putrescine may have an ancient history that stretches as far back in the evolutionary tree as certain arthropods (Yao et al. 2009). ...
... Rights reserved. Shrira (2015) in which participants were randomly assigned to three odorant conditions (i.e., putrescine, ammonia, or water). As in Wisman and Shrira (2015), we used ammonia as an aversive control condition because it has shown similar scores in ratings of the intensity, familiarity, and repugnance of the scent, as compared to putrescine (Anes et al., 2020;Wisman & Shrira 2015). ...
Article
Full-text available
Introduction Previous research suggests that putrescine — the chemical compound that gives decomposing organic matter its distinctive odor — may trigger an inborn evolutionary mechanism that prompts individuals to avoid the smell of decay. The purpose of these two experiments was to investigate the effects of exposure to putrescine on human cognition. Methods Two between-subjects experiments (experiment 1 N = 109; experiment 2 N = 108) compared individuals exposed to either putrescine, ammonia, or water. Experiment 1 measures included odorant ratings (i.e., intensity, familiarity, repugnance, goodness), implicit measures (i.e., word completion task, moral judgment vignettes, and opinions on the death penalty), and explicit measures (i.e., death attitudes, self-esteem, and life satisfaction); experiment 2 measures included odorant ratings and life satisfaction. Results In experiment 1, there were no differences by odorant condition on implicit measures; however, those exposed to putrescine reported higher life satisfaction than those exposed to water. These results were replicated in experiment 2. Conclusions Exposure to putrescine may activate psychological threat management processes, which are then interpreted as higher life satisfaction. Implications Human olfactory perception is sensitive to putrescine, and putrescine may exert some subtle psychological effects on human cognition.
... Wisman (2006) notes that the existential escape hypothesis provides a framework that can account for several anomalies within terror management theory Wisman & Koole, 2003) and synthesises a wide range of theoretical perspectives into one comprehensive framework of existential self-regulation. Furthermore, the majority of previous research on existential escape used mortality salience as a candidate meaning threat (e.g., Wisman & Koole, 2003;Wisman & Shrira, 2015). Based on meaning threats shared foundation of meaninglessness (Heine et al., 2006), the processes of existential escape (Wisman, 2006) may also be applicable to how people deal with other meaning threats such as boredom (Van Tilburg & Igou, 2017a). ...
... That is, participants sought to lose themselves in a group rather than defend or attack their own worldviews (i.e., use their symbolic self-awareness). Later, Wisman and Shrira (2015) found that brief exposure to putrescine, a chemical compound produced by the breakdown of fatty acids in the decaying tissue of dead bodies, can function as a chemosensory warning signal, activating threat management responses (i.e., walking away quicker from experimental settings; completing more escape-related word-stem completion tasks). Finally, found that these escape behaviours in response to mortality salience were more likely among people low in self-esteem and could be exhibited through behaviours such as less implicit self-activation, choosing to write about others rather than the self, and alcohol consumption. ...
... In relation, most existential escape studies, with the exception of and Wisman and Shrira (2015), did not test whether the dependent measures used actually allows people to escape self-awareness, the facility that highlights the meaninglessness of meaning threats. Although the desire to escape self-awareness has been associated with endorsing escape behaviours (e.g., Heatherton & Baumeister, 1991;Twenge et al., 2003), we believe that more research should be conducted in this regard. ...
Article
Boredom is a common, unpleasant emotion that conveys meaninglessness in life and compels people to escape from this adverse existential experience. Within the paradigm of social psychology frameworks, previous research found that bored people endorse cultural sources of meaning as compensation against this state (e.g., nostalgia, political ideologies). In recent years, another form of defence against meaning threats has been identified. An existential escape hypothesis relating to boredom claims that people seek to avoid meaninglessness when people encounter meaning threats such as boredom. By engaging in behaviours with low self-awareness, people counteract awareness of their bored and meaningless self. In this article, we review the current literature on boredom in light of such acts of existential escape. We also provide suggestions for future research to highlight under which circumstances people are more likely to engage in existential escape and identify phenomena that need to be tested within the escape process.
... The breakdown of fatty acids in the decomposing tissues of dead bodies produces a foul smelling chemical compound called putrescine. There is evidence that this chemical compound elicits threat management mechanisms (Wisman et al. 2015). While the smell of putrescine occupies a biochemical and chemosensory niche in the domain of DEATH, the technical term putrescine is not part of the vocabulary of an average native speaker. ...
... It is worth noting that death is the most frequent noun in the metonymic construction [the smell/stench/odor of NOUN] in the iWeb corpus with a total of 886 tokens, 488 collocating with smell, 342 with stench, and 56 with odor. This suggests the experiential salience of olfactory perception associated with death as the ultimate threat to life and survival (Wisman et al. 2015), similar to the way that the scent of blood serves as a survival relevant olfactory cue (Moran et al. 2015). ...
Article
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This article is concerned with metonymy as a cognitive mechanism underlying our best and worst instincts. In particular, I consider two seemingly opposite processes of metonymy: (1) conceptual bypassing of sensory percepts, which leads to an intuitive leap to abstract insights and judgments and (2) conceptual oversimplification of a social category by stereotyping. By directing attention to that which metonymy is apt to obscure, I encourage the reader to rethink existing models of metonymy that focus on its referential and mental access functions. I offer an complementary account of the functions of metonymy by arguing that mental simplism is central to conceptual bypassing and social stereotyping and by pointing out the social psychological reality of an expressive function of metonymy.
... In general, the sweet taste is associated with the presence of energy-rich food; the bitter taste is usually linked to potentially dangerous compounds and unpleasant flavor; umami is connected with the protein content in food; sour helps in the detection of spoiled food and acid tastants in general; finally, salty taste monitors the intake of sodium and other minerals [5]. Moreover, the taste is also supported by the sense of smell in the evaluation of foods or substances, and chemosignal detection is used by animals and humans to identify threats [6,7]. As an example, repulsive odors to humans, such as the ones generated from cadaverine, putrescine, and other biogenic diamines, indicate the presence of bacterial contamination [8]. ...
Article
Full-text available
Taste is a sensory modality crucial for nutrition and survival, since it allows the discrimination between healthy foods and toxic substances thanks to five tastes, i.e., sweet, bitter, umami, salty, and sour, associated with distinct nutritional or physiological needs. Today, taste prediction plays a key role in several fields, e.g., medical, industrial, or pharmaceutical, but the complexity of the taste perception process, its multidisciplinary nature, and the high number of potentially relevant players and features at the basis of the taste sensation make taste prediction a very complex task. In this context, the emerging capabilities of machine learning have provided fruitful insights in this field of research, allowing to consider and integrate a very large number of variables and identifying hidden correlations underlying the perception of a particular taste. This review aims at summarizing the latest advances in taste prediction, analyzing available food-related databases and taste prediction tools developed in recent years. Supplementary information: The online version contains supplementary material available at 10.1007/s00217-022-04044-5.
... L'odorat permet également l'évitement d'autres dangers en induisant une répulsion visà-vis d'autres odeurs telles que celle du dioxyde de carbone (Hu et al. 2007; Liberles 2015) et des cadavres d'animaux en décomposition (Hussain et al. 2013) chez l'animal ou encore du feu, de la fumée, des produits chimiques toxiques et des aliments avariés chez l'Homme (Santos et al. 2004;Wisman et Shrira 2015). Nous pouvons par exemple détecter le mercaptan, la molécule odorante du qui est utilisé pour donner une odeur au gaz, à une concentration infime de 0,2x10 -6 g/L (Yeshurun et Sobel 2010). ...
Thesis
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Les informations sensorielles que nous percevons suscitent des réponses émotionnelles qui guident notre comportement d’approche ou de retrait, c’est le reflet de ce que l'on appelle la valeur hédonique du stimulus sensoriel. La dimension hédonique est un paramètre dominant de la perception olfactive. En effet, notre première réaction face à une odeur est en général "j’aime" ou "je n’aime pas" avant même d’essayer de l’identifier. Il est bien établi que la valeur hédonique des odorants possède une composante innée mais elle peut être également modifiée par un certain nombre de paramètres dont le vieillissement. L’altération par l’âge de la valeur hédonique des odorants n’est pas sans conséquence puisqu’elle peut affecter la qualité de vie notamment au niveau de la prise alimentaire. Pendant ma thèse, je me suis intéressée aux mécanismes neuronaux sous-tendant l’attraction induite par les odorants plaisants et à leurs altérations lors du vieillissement. L’équipe a mis en évidence dans une précédente étude que les odorants plaisants étaient représentés dans la région postérieure du bulbe olfactif, premier relai cortical de l’information olfactive. Ces données soulèvent la question de comment l’information hédonique présente dans le bulbe olfactif est traitée par le reste du cerveau pour générer un comportement d’attraction. Comme les comportements motivés sont connus pour être sous-tendus par système de récompense, nous avons recherché dans une première étude le rôle de ce circuit dans l’attraction olfactive. Nous avons tout d’abord mis en évidence que l’activation optogénétique du bulbe olfactif postérieur induit un comportement d’autostimulation intracérébrale accompagné d’une activation neurale de l’aire tegmentale ventrale et du tubercule olfactif, révélant la capacité de cette région à recruter le système de récompense. Le tubercule olfactif fait partie du striatum ventral et est donc au carrefour entre le système olfactif et celui de la récompense. Par la technique d’iDISCO, nous avons montré que le bulbe olfactif postérieur projette préférentiellement vers le tubercule olfactif. De plus, nous avons révélé que les odorants attractifs activent de façon spécifique le tubercule olfactif et induisent une préférence de place conditionnée sous contrôle du système dopaminergique. La mise en évidence du pouvoir récompensant de certains odorants avec une implication forte du tubercule olfactif a pu être étendue à l’Homme grâce à des expériences menées en living lab et à l’IRMf. Dans une deuxième étude, je me suis intéressée à l’impact de l’âge sur la perception des odeurs plaisantes et aux bases neurales qui la sous-tendent. Nous avons montré qu’en accord avec des études précédemment menées chez l’Homme, le caractère plaisant de certains odorants s’altère au cours du vieillissement chez la souris. En effet, certains odorants restent encore attractifs et activent toujours le bulbe olfactif postérieur et le tubercule olfactif alors que ce pattern neural n’est plus observé pour les odorants qui ont perdu leur pouvoir attractif. De plus, l’activation optogénétique du bulbe olfactif postérieur chez la souris âgée est capable d’induire un comportement d’autostimulation intracérébrale mais de façon moins robuste que chez la jeune puisque les animaux âgés ont besoin de plus d’essais pour se conditionner et que l’extinction est plus rapide. Enfin, ce conditionnement est accompagné d’une activation du tubercule olfactif, sans activation de l’aire tegmentale ventrale, révélant un recrutement seulement partiel du système de récompense. Ainsi, lors de ma thèse, j’ai pu mettre en évidence l’existence d’une voie d’entrée directe et privilégiée entre le système olfactif et celui de la récompense conférant à certaines odeurs un effet récompensant qui pourrait expliquer leur fort pouvoir attractif. De plus, j’ai montré une altération de cette voie qui pourrait être à l’origine de l’anhédonie olfactive sélective constatée au cours du vieillissement.
... In fact, the subconscious processing of smells has been noted for its capacity to shift behavior (Gustavson et al., 1987;Holland et al., 2005;Mas et al., 2019;Olsson et al., 2006). Several studies have shown correct recollection behaviors without explicit recognition (Degel et al., 2001;Degel & Köster, 1999;Olsson & Cain, 2003) and findings suggest that odors alter cognition and behavior largely at a subconscious level (Prehn et al., 2006;Wisman & Shrira, 2015;Ye et al., 2019;Zhou et al., 2014;Zhou & Chen, 2008). This is, even when odors are not consciously perceived, they do impact our mood and behavior (Köster, 2002). ...
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Research has shown that conflicting multisensory signals may alter embodiment to the point of self-identifying with a foreign body, but the role of olfaction in this process has been overlooked. Here, we study in healthy participants how sex (male and female sweat odors) and gender (male and female cosmetic scents) olfactory stimuli contribute to embodiment. Participants saw from the perspective of a sex mismatching person in virtual reality and received synchronous visuo-tactile stimulation to elicit illusory embodiment of the seen body while smelling either sex- or gender- congruent stimuli. We assessed implicit (skin conductance responses to visual threats) and explicit (questionnaire) measures of embodiment. Stronger responses to threat were found when participants smelled the sex-congruent compared to the sex-incongruent odor, while no such differences were found for the cosmetic scents. According to the questionnaire, embodiment did not differ between conditions. Post-experimental assessment of the presented cues, suggest that while both sweat odors were considered generally male, cosmetic scents were not. The presented scents were generally not associated to the embodied body. Our results suggest that sex-related body odors influence implicit but not explicit aspects of embodiment and are in line with unique characteristics of olfaction in other aspects of cognition.
... An alternative interpretation of this effect is that the presence of a negative tactile stimulus limits how pleasant any other sensory perception or the multimodal sensory whole can be. The lack of a modulatory effect on negative odors could indicate a form of negative dominance, evolutionary explained by the importance of chemosensory threat detection (Wisman and Shrira 2015). A particularly intriguing result is the dominant interaction between the tactile stimulation and gender; the influence of tactile valence is entirely absent for men. ...
Article
Due to the complex stimulation methods required, olfaction and touch are two relatively understudied senses in the field of perceptual (neuro-)science. In order to establish a consistent presentation method for the bimodal stimulation of these senses we combined an olfactometer with the newly developed Unimodal Tactile Stimulation Device (UniTaSD). This setup allowed us to study the influence of olfaction on tactile perception and opened up an unexplored field of research by examining the crossmodal influence of tactile stimuli on olfaction. Using a pseudorandomized design, we analyzed how positive or negative tactile and olfactory stimuli influenced the opposing modality’s perceived intensity and pleasantness. By asking participants to rate tactile stimuli we were able to reproduce previously reported differences indicating that bimodal presentation with an olfactory stimulus increases or reduces perceived tactile pleasantness in an odor-dependent manner, while highlighting that this effect appears unique to women. Furthermore, we found first evidence for the influence of tactile stimuli on perceived odor pleasantness, an effect which is also driven primarily by women in our study. Based on these findings we believe that future neurophysiological studies, using controlled stimulus presentation can help unravel how and why olfactory and tactile perception interact in the human brain.
... However, they also tend to work under the anthropocentric 4 assumption that the only possible way of thinking 3 These two types of responses to death (stereotypical vs cognitive) are not mutually exclusive in a single species. In humans, for instance, we find both sophisticated cognitive and emotional responses to death and an automatic activation of threat-management responses in reaction to the chemical cues of corpses (Wisman and Shrira 2015). 4 We take anthropocentrism to be something distinct from anthropomorphism. ...
Article
Full-text available
Comparative thanatologists study the responses to the dead and the dying in nonhu-man animals. Despite the wide variety of thanatological behaviours that have been documented in several different species, comparative thanatologists assume that the concept of death (CoD) is very difficult to acquire and will be a rare cognitive feat once we move past the human species. In this paper, we argue that this assumption is based on two forms of anthropocentrism: (1) an intellectual anthropocentrism, which leads to an over-intellectualisation of the CoD, and (2) an emotional anthropocentrism, which yields an excessive focus on grief as a reaction to death. Contrary to what these two forms of anthropocentrism suggest, we argue that the CoD requires relatively little cognitive complexity and that it can emerge independently from mourning behaviour. Moreover, if we turn towards the natural world, we can see that the minimal cognitive requirements for a CoD are in fact met by many nonhuman species and there are multiple learning pathways and opportunities for animals in the wild to develop a CoD. This allows us to conclude that the CoD will be relatively easy to acquire and, so, we can expect it to be fairly common in nature.
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As in many other species of nonhuman primates, chimpanzee mothers with a dead infant may continue to care for and transport the infant for days, weeks, or even longer. The bereaved females do this despite what humans perceive as the foul odour from the putrefying corpse. Putrescine is a major contributor to the “smell of death,” and it elicits behaviours aimed at getting rid of the source of the smell, or escape responses in mammals including humans. However, it has never been shown that the odour of putrescine is aversive to chimpanzees. To address this question, we visually presented six adult chimpanzees with the corpse of a small bird, or a stuffed glove, in association with putrescine, ammonia, or water, and recorded the chimpanzees’ reactions. The apes spent significantly less time near the object when it was paired with putrescine than the other substances, although they showed no signs of increased arousal or anxiety. We interpret the findings as evidence of an aversion to the smell of death in chimpanzees, discuss the implications for understanding the continued maternal-like behaviour of bereaved female chimpanzees, and suggest future research directions for the field of comparative evolutionary thanatology.
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Humans were once considered unique in having a concept of death but a growing number of observations of animal responses to dying and dead conspecifics suggests otherwise. Complex arrays of behaviors have been described ranging from corpse removal and burial among social insects to quiet attendance and caregiving among elephants and primates. Less frequently described, however, are behavioral responses of individuals from different age/sex classes or social position toward the death of conspecifics. We describe behavioral responses of mountain gorillas (Gorilla beringei beringei) to the deaths of a dominant silverback and a dominant adult female from the same social group in Volcanoes National Park in Rwanda and the responses of Grauer's gorillas (Gorilla b. graueri) to the corpse of an extra-group silverback in Kahuzi-Biega National Park, Democratic Republic of Congo. In gorillas, interactions between groups or with a lone silverback often result in avoidance or aggression. We predicted that: (i) more individuals should interact with the corpses of same-group members than with the corpse of the extra-group silverback; (ii) adult females with infants should avoid the corpse of the extra-group silverback; and (iii) in the mountain gorilla cases, individuals that shared close social relationships with the dead individual should spend more time with the corpse than other individuals in the group. We used a combination of detailed qualitative reports, photos, and videos to describe all occurrences of affiliative/investigative and agonistic behaviors observed at the corpses. We observed similar responses toward the corpses of group and extra-group individuals. Animals in all three cases showed a variety of affiliative/investigative and agonistic behaviors directed to the corpses. Animals of all age/sex classes interacted with the corpses in affiliative/investigative ways but there was a notable absence of all adult females at the corpse of the extra-group silverback. In all three cases, we observed only silverbacks and blackbacks being agonistic around and/or toward the corpses. In the mountain gorilla cases, the individuals who spent the most time with the corpses were animals who shared close social relationships with the deceased. We emphasize the similarity in the behavioral responses around the corpses of group and extra-group individuals, and suggest that the behavioral responses were influenced in part by close social relationships between the deceased and certain group members and by a general curiosity about death. We further discuss the implications close interactions with corpses have for disease transmission within and between gorilla social groups.
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The 10-min psychomotor vigilance task (PVT) has often been used to assess the impact of sleep loss on performance. Due to time constraints, however, regular testing may not be practical in field studies. The aim of the present study was to examine the suitability of tests shorter than 10 min. in duration. Changes in performance across a night of sustained wakefulness were compared during a standard 10-min PVT, the first 5 min of the PVT, and the first 2 min of the PVT. Four performance metrics were assessed: (1) mean reaction time (RT), (2) fastest 10% of RT, (3) lapse percentage, and (4) slowest 10% of RT. Performance during the 10-min PVT significantly deteriorated with increasing wakefulness for all metrics. Performance during the first 5 min and the first 2 min of the PVT deteriorated in a manner similar to that observed for the whole 10-min task, with all metrics except lapse percentage displaying significant impairment across the night. However, the shorter the task sampling time, the less sensitive the test is to sleepiness. Nevertheless, the 5-min PVT may provide a viable alternative to the 10-min PVT for some performance metrics.
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Observational studies have suggested that with time, some diseases result in a characteristic odor emanating from different sources on the body of a sick individual. Evolutionarily, however, it would be more advantageous if the innate immune response were detectable by healthy individuals as a first line of defense against infection by various pathogens, to optimize avoidance of contagion. We activated the innate immune system in healthy individuals by injecting them with endotoxin (lipopolysaccharide). Within just a few hours, endotoxin-exposed individuals had a more aversive body odor relative to when they were exposed to a placebo. Moreover, this effect was statistically mediated by the individuals’ level of immune activation. This chemosensory detection of the early innate immune response in humans represents the first experimental evidence that disease smells and supports the notion of a “behavioral immune response” that protects healthy individuals from sick ones by altering patterns of interpersonal contact.
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The olfactory system translates a vast array of volatile chemicals into diverse odor perceptions and innate behaviors. Odor detection in the mouse nose is mediated by 1,000 different odorant receptors (ORs) and 14 trace amine-associated receptors (TAARs). ORs are used in a combinatorial manner to encode the unique identities of myriad odorants. However, some TAARs appear to be linked to innate responses, raising questions about regulatory mechanisms that might segregate OR and TAAR expression in appropriate subsets of olfactory sensory neurons (OSNs). Here, we report that OSNs that express TAARs comprise at least two subsets that are biased to express TAARs rather than ORs. The two subsets are further biased in Taar gene choice and their distribution within the sensory epithelium, with each subset preferentially expressing a subgroup of Taar genes within a particular spatial domain in the epithelium. Our studies reveal one mechanism that may regulate the segregation of Olfr (OR) and Taar expression in different OSNs: the sequestration of Olfr and Taar genes in different nuclear compartments. Although most Olfr genes colocalize near large central heterochromatin aggregates in the OSN nucleus, Taar genes are located primarily at the nuclear periphery, coincident with a thin rim of heterochromatin. Taar-expressing OSNs show a shift of one Taar allele away from the nuclear periphery. Furthermore, examination of hemizygous mice with a single Taar allele suggests that the activation of a Taar gene is accompanied by an escape from the peripheral repressive heterochromatin environment to a more permissive interior chromatin environment.
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Sensory cues that predict reward or punishment are fundamental drivers of animal behavior. For example, attractive odors of palatable food or a potential mate predict reward, while aversive odors of pathogen-laced food or a predator predict punishment. Aversive and attractive odors can be detected by intermingled sensory neurons that express highly related olfactory receptors and display similar central projections. These findings raise basic questions of how innate odor valence is extracted from olfactory circuits, how such circuits are developmentally endowed and modulated by state, and how innate and learned odor responses are related. Here, we review odors, receptors and neural circuits associated with stimulus valence, discussing salient principles derived from studies on nematodes, insects and vertebrates. Understanding the organization of neural circuitry that mediates odor aversion and attraction will provide key insights into how the brain functions. Copyright © 2015 Elsevier Ltd. All rights reserved.
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An evolved module for fear elicitation and fear learning with 4 characteristics is proposed. (a) The fear module is preferentially activated in aversive contexts by stimuli that are fear relevant in an evolutionary perspective. (b) Its activation to such stimuli is automatic. (c) It is relatively impenetrable to cognitive control. (d) It originates in a dedicated neural circuitry, centered on the amygdala. Evidence supporting these propositions is reviewed from conditioning studies, both in humans and in monkeys; illusory correlation studies; studies using unreportable stimuli; and studies from animal neuroscience. The fear module is assumed to mediate an emotional level of fear learning that is relatively independent and dissociable from cognitive learning of stimulus relationships.
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To test the hypothesis that longevity of odor memory is due to strong proactive interference (reduction of new learning by prior learning) and to absence of retroactive interference (reduction of prior memory by new learning), subjects, matched in age and gender with those of a previous experiment, were unknowingly exposed in two sessions to the weak concentrations of lavender or orange used before. Implicit odor memory was later tested in a separate experiment. Comparison of the results with those of the previous experiment showed that both proactive and retroactive interference occurred. These results have implications for the general theory about implicit memory for new associations, which may have to be amended when non-verbal material is used. The longevity of odor memory should be explained by the improbability of occurrence of incidences that provoke retroactive interference rather than by the absence of the retroactive interference itself.
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One hundred and fifty-two subjects, divided into eight groups, were exposed to a room with a low concentration of either orange or lavender and to an odorless room. In a careful double-blind procedure, neither the subjects nor the experimenters were made aware of the presence of the odors in the experimental conditions. Later they were asked to indicate how well each of 12 odor stimuli, including the experimental and control odors, befitted each of 12 visual contexts, including the exposure rooms. At the end of this session they rated the pleasantness and the familiarity of the odors, and identified them by name. Finally they were debriefed and asked specifically whether they had perceived the experimental odors anywhere in the building. The results of four subjects who answered positively to the latter question were omitted. The results confirm the earlier finding that non-identifiers implicitly link odor and exposure room, whereas identifiers do not show such a link. It is suggested that episodic information is an essential constituent of olfactory memory and that its function is comparable to that of form and structure in visual and auditory memory systems.
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The existence of innate predator aversion evoked by predator-derived chemostimuli called kairomones offers a strong selective advantage for potential prey animals. However, it is unclear how chemically diverse kairomones can elicit similar avoidance behaviors. Using a combination of behavioral analyses and single-cell Ca(2+) imaging in wild-type and gene-targeted mice, we show that innate predator-evoked avoidance is driven by parallel, non-redundant processing of volatile and nonvolatile kairomones through the activation of multiple olfactory subsystems including the Grueneberg ganglion, the vomeronasal organ, and chemosensory neurons within the main olfactory epithelium. Perturbation of chemosensory responses in specific subsystems through disruption of genes encoding key sensory transduction proteins (Cnga3, Gnao1) or by surgical axotomy abolished avoidance behaviors and/or cellular Ca(2+) responses to different predator odors. Stimulation of these different subsystems resulted in the activation of widely distributed target regions in the olfactory bulb, as assessed by c-Fos expression. However, in each case, this c-Fos increase was observed within the same subnuclei of the medial amygdala and ventromedial hypothalamus, regions implicated in fear, anxiety, and defensive behaviors. Thus, the mammalian olfactory system has evolved multiple, parallel mechanisms for kairomone detection that converge in the brain to facilitate a common behavioral response. Our findings provide significant insights into the genetic substrates and circuit logic of predator-driven innate aversion and may serve as a valuable model for studying instinctive fear [1] and human emotional and panic disorders [2, 3]. Copyright © 2015 Elsevier Ltd. All rights reserved.
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The mammalian olfactory system detects a plethora of environmental chemicals that are perceived as odors or stimulate instinctive behaviors. Studies using odorant receptor (OR) genes have provided insight into the molecular and organizational strategies underlying olfaction in mice. One important unanswered question, however, is whether these strategies are conserved in primates. To explore this question, we examined the macaque, a higher primate phylogenetically close to humans. Here we report that the organization of sensory inputs in the macaque nose resembles that in mouse in some respects, but not others. As in mouse, neurons with different ORs are interspersed in the macaque nose, and there are spatial zones that differ in their complement of ORs and extend axons to different domains in the olfactory bulb of the brain. However, whereas the mouse has multiple discrete band-like zones, the macaque appears to have only two broad zones. It is unclear whether the organization of OR inputs in a rodent/primate common ancestor degenerated in primates or, alternatively became more sophisticated in rodents. The mouse nose has an additional small family of chemosensory receptors, called trace amine-associated receptors (TAARs), which may detect social cues. Here we find that TAARs are also expressed in the macaque nose, suggesting that TAARs may also play a role in human olfactory perception. We further find that one human TAAR responds to rotten fish, suggesting a possible role as a sentinel to discourage ingestion of food harboring pathogenic microorganisms.