Elsevier

Biological Psychology

Volume 85, Issue 2, October 2010, Pages 331-337
Biological Psychology

The psychology of potential threat: Properties of the security motivation system

https://doi.org/10.1016/j.biopsycho.2010.08.003Get rights and content

Abstract

Results of three experiments support hypothesized properties of the security motivation system, a special motivational system for handling potential threats, as proposed by Szechtman and Woody (2004). First, mild stimuli suggesting potential harm produced a marked state of activation (evident in both objective and subjective measures), consistent with the hypothesis that the security motivation system is finely tuned for the detection of potential threat. Second, in the absence of corrective behavior, this evoked activation is persistent, supporting the hypothesis that once stimulated, the security motivation system produces an enduring motivational state involving the urge to engage in threat-reducing behavior. Third, engagement in corrective behavior was effective in returning activation levels to baseline, whereas cognitive reappraisal was not. These findings are consistent with the hypothesis that deactivation of the security motivation system depends on performance of security-related behaviors, rather than non-behavioral events such as cognitive re-evaluation of threat.

Research highlights

▶ Mild stimuli suggesting potential harm activate a security motivation system (SMS). ▶ The resulting motivational state can be indexed by respiratory sinus arrythmia change. ▶ Performance of appropriate security-related corrective behavior deactivates SMS. ▶ When SMS is activated, cognitive reappraisal of potential harm does not deactivate SMS.

Introduction

One important type of problem that organisms confront in the natural environment is the possibility of events that would have grave consequences if they occurred, yet happen only rarely and can be anticipated only with great uncertainty. Such potential dangers include the possibilities that a predator may be present and that contagion may occur. Potential dangers like these pose some unique challenges. For example, because potential dangers are often hidden (e.g., germs) or not yet present, detecting them must rely on indirect and uncertain cues. Similarly, because of the high cost of error in responding to potential dangers, including death, the possibilities for learning about them through natural consequences are limited; instead, the organism must rely on robust, precautionary responses.

In recognition of these relatively unique challenges, several investigators have proposed that there exists a special motivation system, shaped by evolution for the management of low-probability, high-consequence risks. This biologically ancient neural system has been labeled in various ways, including the “defense system” (Trower et al., 1990), the “hazard-precaution system” (Boyer and Lienard, 2006), the “involuntary risk scenario generating system” (Abed and de Pauw, 1998) and, in our own work, the “security motivation system” (Szechtman and Woody, 2004, Woody and Szechtman, 2005, Woody et al., 2005). The focus in these theories on uncertainty is related to but distinct from the focus on “threat imminence” in other theoretical approaches (Blanchard and Blanchard, 1988, Craske, 2003, Fanselow, 1994, McNaughton and Corr, 2004). Although distance to the source of danger may often be related to uncertainty, the two can be quite distinct, as in the instance of contact with a substance that may or may not be contaminated. Moreover, the concept of potential danger is more general than threat imminence, which tends to be based on analyses of predator threat. Potential threats take in not only predators, but also threats such as contagion and contamination (disease) and loss of crucial resources (such as food), as discussed in more detail elsewhere (Boyer and Bergstrom, in press, Neuberg et al., in press, Woody and Szechtman, in press).

The security motivation system is hypothesized to be a module in the brain that evolved to handle the adaptive problems presented by rare, potentially catastrophic risks such as the potential threats of predation and disease. According to evolutionary psychologists (Pinker, 1997, Tooby and Cosmides, 2006, Trower et al., 1990), such modules are devoted to the detection of relatively specific classes of stimuli, facilitating rapid processing of information of potential relevance for survival and functioning in a relatively automatic and encapsulated way. In addition, they operate as motivational systems, whose activation drives relevant responses and temporarily suppresses competing systems (Kavaliers and Choleris, 2001), and they have a characteristic set of species-typical output behaviors.

Research by ethological psychologists and ecologists across a variety of species has examined how animals manage potential threats, such as the danger of predation, and this work reveals the major properties of the security motivation system. First, animals use subtle and indirect cues of uncertain significance to gauge changes in potential danger (Blanchard and Blanchard, 1988, Lima and Bednekoff, 1999), and assessment of these cues occurs in the absence of any tangible evidence of the presence of a threat, such as a predator (Brown et al., 1999). Wingfield et al. (1998) called these indirect cues “labile perturbation factors,” to distinguish them from the presence of imminent danger, and similarly Curio (1993) argued that the diversity of “hidden-risk mechanisms” must be distinguished from predator detection. Thus, the security motivation system performs special types of perceptual processing that may be quite different from those for recognizing imminent danger.

In addition, vigilance and apprehension are readily activated by relatively weak cues suggesting potential danger, and even in the absence of further such cues, this activation dissipates only gradually (Brown et al., 1999, Wingfield et al., 1998, Curio, 1993, Marks and Nesse, 1994, Masterson and Crawford, 1982). Furthermore, activation of the system drives security-related behaviors that are inherently open-ended, in the sense that the animal's environment does not provide any clear consummatory stimulus to signal goal attainment (Szechtman and Woody, 2004). For example, a predator's disappearance from view is not a clear sign of reduced risk (Curio, 1993). Instead, it is the engagement in security-related behavior in itself that appears to generate the internal signal for terminating security motivation (Glickman and Schiff, 1967, Szechtman and Woody, 2004). These behaviors include probing the environment to collect further information about the potential danger and precautionary acts that would help counteract its effects if were to occur. For shutting down security motivation, it is evolutionarily adaptive to rely on performance of such behavior rather than other processes such as cognitive reappraisal, because threat cues may be difficult to evaluate and the costs of inaction are potentially grave (Woody and Szechtman, in press).

Finally, research addressing other behavioral systems that protect animals from noxious events clarifies the ways in which the security motivation system is distinct from them. Ohman and Mineka (2001) have hypothesized that the “fear module” manages escape and avoidance learning through the conditioning of its core motive state of fear to cues of imminent danger, such as the presence of a predator. The security motivation system differs from the fear module in three crucial respects: it operates on subtler, unconditioned stimuli suggesting hidden risk, typically in the absence of manifest danger; its motive state is vigilance and apprehension rather than fear; and its characteristic behavioral output involves probing the environment and precautionary behaviors, rather than avoidance. Likewise, Wingfield et al. (1998) argued that unpredictable environmental changes that may indicate potential danger elicit a pattern of responses that are quite distinct from the fight-or-flight response, both in the kinds of behaviors and their longer time course.

Just as the engagement of other motivational systems produces physiological changes that prepare the body for relevant behavior, activation of the security motivation system should yield physiological changes that facilitate engagement in security-related behavior. Because the motor activity engendered by security motivation, such as probing for predators and precautionary washing, is not physically strenuous, it requires relatively modest energy resources. However, there is the possibility that potential danger could rapidly become real, which would necessitate high energy for engagement in fight-or-flight (Cannon, 1927). In preparation for this possibility, security motivation should mobilize the physiological mechanisms for energy delivery into a state of high preparedness; nonetheless, it should not fully engage them in fuel delivery, because the immediate responses to potential threat, such as precautionary and probing behaviors, do not require strenuous muscular exertion.

This energy preparedness is mediated, at least in part, by the autonomic nervous system. The sympathetic and parasympathetic systems generally work in opposition to each other to regulate internal organs such as the heart and lungs, with the sympathetic system tending to mobilize energy resources and body metabolism for rapid, intense exertion, and the parasympathetic system tending to conserve and replenish energy resources. Security motivation calls for a physiological state lying between these two extremes: a state of high readiness to rapidly support maximal exertion, should this turn out to be needed, while at the same time supporting the relatively modest metabolic demands of ongoing security-related behavior.

Polyvagal theory, as advanced by Porges, 2001, Porges, 2007b, Porges, 2009, explains how the autonomic nervous system produces such a state. The requisite state lies between a state dominated by parasympathetic influence, which facilitates social interactions in environments safe from danger, and a state dominated by sympathetic influence, which facilitates flight-or-flight responses in the face of imminent danger. According to polyvagal theory, there exists an intermediate stage in which attention is directed to the environment because of novelty or potential threat, and parasympathetic influence over the viscera, including the heart and lungs, is attenuated, so that the sympathetic system can be set off quickly if required later.

This potential-threat stage of autonomic function can be indexed objectively by monitoring its effects on heart-rate variability. Specifically, the time series of the intervals between the peaks of the R wave in the electrocardiogram shows oscillations in the frequencies associated with spontaneous breathing (0.12–0.4 Hz), and these oscillations are known as respiratory sinus arrhythmia (RSA). It is the RSA component of heart-rate variability that is sensitive to transitions between safe and potential-threat autonomic stages, and thus can serve as an index of the activation of security motivation.

In particular, RSA is a reflection of neural activity in the nucleus ambiguus-vagal circuit, which exerts an inhibitory effect on the cardiac pacemaker (Porges, 1995). This “vagal brake” (Porges, 2007a) restrains the heart from beating at its intrinsically higher rhythm; in addition, removal of this brake reduces heart-rate variability, because the interval between beats becomes less modulated and hence more regular. Thus, lower variance in the beat-to-beat intervals (as indexed by decreased RSA amplitude in ln ms2) indicates a shift from a safe toward a potential-threat autonomic stage. In summary, observed changes in RSA toward less variability should indicate activation of the security motivation system—that is, a state of biological preparedness or readiness, rather than full mobilization. In addition, RSA change has the advantage of being a relatively pure index of vagal brake removal, whereas heart rate is also influenced by other vagal and sympathetic factors.

Further discussion of polyvagal theory and its relation to other theories, such as Gray's motivation theory (Gray, 1982, Gray and McNaughton, 2000), is provided in Beauchaine (2001) and Brenner et al. (2005). More detailed consideration of the neural and physiological bases for the security motivation system is provided in Woody and Szechtman (in press).

Here, in a series of three experiments, we advance a paradigm to activate security motivation and test the prediction that performance of security-related behavior generates the negative feedback signal necessary to terminate such activation. An additional goal was to establish an experimental paradigm that can be used in future work to test the theory that some types of psychopathology are disorders of security motivation (Flannelly et al., 2007, Szechtman and Woody, 2006), including obsessive–compulsive disorder (Boyer and Lienard, 2006, Szechtman and Woody, 2004). The present experiments examine the following research questions:

  • A.

    Does exposure to potential-threat stimuli and engagement in precautionary behavior lead to activation and deactivation, respectively, of the security motivation system?

  • B.

    Can RSA be used to provide an objective index of changes in activation of security motivation?

  • C.

    Does activation of the security motivation system vary as a function of low to high levels of potential threat, and does such activation persist over time in the absence of precautionary behavior?

  • D.

    Finally, is performance of precautionary behavior necessary as a terminator of security motivation, or can cognitive reappraisal of threat substitute for it?

Section snippets

Experiment 1

To examine the properties of the SMS, we needed an experimental paradigm to measure how activity of the system changes as a function of exposure to stimuli suggesting potential threat and subsequent engagement in corrective behavior. Experiment 1 compared RSA measured at four successive times: (1) resting baseline; (2) after hand contact with a stimulus; (3) after engagement in a prescribed behavior; and (4) after a final free washing of the hands. There were two experimentally manipulated

Experiment 2

To examine how activation of the SMS varies as a function of low to high potential threat, Experiment 2 contrasted five stimulus conditions designed to represent a graded range of levels of potential threat. It also tracked RSA for a more extended period of time (22 min) in the absence of corrective behavior. The exploration of such across-time dynamics is consistent with Davidson's concept of “affective chronometry,” in which the time course of a particular type of emotional response is mapped

Experiment 3

The results of the previous two experiments demonstrated the following properties of the SMS: (1) contact with the stimulus must suggest potential harm to activate the system; (2) in the absence of corrective action, activation of the system persists strongly (for at least 22 min); and (3) corrective action is very effective in returning the system to baseline. The SMS theory postulates that performance of precautionary behavior is necessary to deactivate security motivation. Thus, an important

General discussion

Taken together, the results of these experiments provide support for important hypothesized properties of the SMS, a special motivational system designed to handle potential threats (Szechtman and Woody, 2004). First, even quite mild stimuli suggesting potential harm produced a marked state of activation (evident in both objective and subjective measures). This finding is consistent with the hypothesis that the SMS is finely tuned for the detection of potential threat. Second, in the absence of

Acknowledgments

We thank Dr. Stephen Porges for training in MxEdit and consultation. Supported by Canadian Institutes of Health Research grant MOP134450. M.C. was supported by an NSERC Undergraduate Scholarship.

References (44)

  • T. Beauchaine

    Vagal tone, development, and Gray's motivational theory: toward an integrated model of autonomic nervous system functioning in psychopathology

    Development and Psychopathology

    (2001)
  • D.C. Blanchard et al.

    Ethoexperimental approaches to the biology of emotion

    Annual Review of Psychology

    (1988)
  • Boyer, P., Bergstrom, B., in press. Threat-detection in child development: an evolutionary perspective. Neuroscience...
  • P. Boyer et al.

    Why ritualized behavior? Precaution systems and action parsing in developmental, pathological and cultural rituals

    Behavioral and Brain Sciences

    (2006)
  • S.L. Brenner et al.

    A comparison of psychophysiological and self-report measures of BAS and BIS activation

    Psychophysiology

    (2005)
  • J.S. Brown et al.

    The ecology of fear: optimal foraging, game theory, and trophic interactions

    Journal of Mammalogy

    (1999)
  • W.B Cannon

    Bodily Changes in Pain, Hunger, Fear, and Rage: An Account of Recent Researches into the Function of Emotional Excitement

    (1927)
  • M.G. Craske

    Origins of Phobias and Anxiety Disorders: Why More Women than Men?

    (2003)
  • R.J. Davidson

    Affective style and affective disorders: perspectives from affective neuroscience

    Cognition & Emotion

    (1998)
  • J.H. Dwyer

    Statistical Models for the Social and Behavioral Sciences

    (1983)
  • M.S. Fanselow

    Neural organization of the defensive behavior system responsible for fear

    Psychonomic Bulletin and Review

    (1994)
  • K.J. Flannelly et al.

    Beliefs, mental health, and evolutionary threat assessment systems in the brain

    Journal of Nervous and Mental Disease

    (2007)
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