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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/313204781 Thinking about threats: Memory and prospection in human threat management Article  in  Consciousness and Cognition · January 2017 DOI: 10.1016/j.concog.2017.01.005 CITATIONS READS 6 503 3 authors, including: Adam Bul
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  See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/313204781  Thinking about threats: Memory and prospection in human threatmanagement Article   in   Consciousness and Cognition · January 2017 DOI: 10.1016/j.concog.2017.01.005 CITATIONS 6 READS 503 3 authors , including: Some of the authors of this publication are also working on these related projects: Reddit AMA Human Uniqueness   View projectStrategic reminder setting   View projectAdam Bulley The University of Queensland 21   PUBLICATIONS   97   CITATIONS   SEE PROFILE  Thomas Suddendorf  The University of Queensland 128   PUBLICATIONS   5,566   CITATIONS   SEE PROFILE All content following this page was uploaded by Adam Bulley on 30 September 2017.  The user has requested enhancement of the downloaded file.  Review article Thinking about threats: Memory and prospection in humanthreat management Adam Bulley ⇑ , Julie D. Henry, Thomas Suddendorf  The University of Queensland, St. Lucia, Brisbane, Queensland 4072, Australia a r t i c l e i n f o  Article history: Received 24 February 2016Revised 10 September 2016Accepted 22 January 2017 Keywords: Episodic foresightEpisodic memorySemantic memoryMental time travelThreat detectionAnxietyWorryEvolutionEvolutionary psychologyCounterfactual thinking a b s t r a c t Humans have evolved mechanisms for the detection and management of possible threatsin order to abate their negative consequences for fitness. Internally generated (‘detached’)cognition may have evolved in part because of its contributions to this broad function, butimportant questions remain about its role in threat management. In this article, we there-fore present a taxonomy of threat-related internally generated cognition comprising episo-dic and semantic formats of memory and prospection. We address the proximatemechanisms of each of the capacities in this taxonomy, and discuss their respective contri-butions to adaptive threat management in humans. For instance, mental time travelempowers people to contemplate and learn from threats experienced long ago, as wellas to plan for dangers that might arise in the distant future. However, despite their func-tional benefits, these thought processes are also central to contemporary anxiety disordersand may be a potent source of distress.   2017 Elsevier Inc. All rights reserved. Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 542. What are threats? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 543. Semantic and episodic processes in internally generated thinking. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 554. Prospection and preparation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 564.1. Episodic threat prospection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 564.2. Semantic threat prospection. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 585. Retrospective memory and threats. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 595.1. Episodic threat memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 595.2. Semantic threat memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 606. Retrieval processes and adaptive responses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 617. Further directions and remaining questions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 627.1. Phylogeny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 627.2. Adaptive significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 627.3. Proximate mechanisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 637.4. Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 http://dx.doi.org/10.1016/j.concog.2017.01.0051053-8100/   2017 Elsevier Inc. All rights reserved. ⇑ Corresponding author at: The University of Queensland, St. Lucia, Brisbane, Queensland 4072, Australia. E-mail address:  adam.bulley@uqconnect.edu.au (A. Bulley).Consciousness and Cognition 49 (2017) 53–69 Contents lists available at ScienceDirect Consciousness and Cognition journal homepage: www.elsevier.com/locate/concog  8. Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 1. Introduction Fear keeps pace with hope. Nor does their so moving together surprise me; both belong to a mind in suspense, to a mind in astate of anxiety through looking into the future. Both are mainly due to projecting our thoughts far ahead of us instead of adapt-ing ourselves to the present. Thus it is that foresight, the greatest blessing humanity has been given, is transformed into a curse.Wild animals run from the dangers they actually see, and once they have escaped them worry no more. We however are tor-mented alike by what is past and what is to come. A number of our blessings do us harm, for memory brings back the agony of  fear while foresight brings it on prematurely .[Seneca 60AD]Some capacityfordefence inthe face of immediatedangeris perhapsa universalattribute of all animalspecies. It haslongbeen recognised that humans,like many other animals, have evolved complex suites of physiological and cognitiveprocessesto detect and manage potential threats to fitness (Cannon, 1916; Darwin, 1872). The distinction between immediately per-ceptible or  manifest   threats, on the one hand, and  potential  threats on the other has since been used to discern defensiveresponses to threat in terms of temporal proximity (Blanchard, Griebel, Pobbe, & Blanchard, 2011; Boyer & Lienard, 2006;Eilam,Izhar, &Mort, 2011;Woody& Szechtman,2011). A looselyconceptualised gradient has thereforebeen drawnbetweendefensive reactions to immediate threats (‘fear’) and defensive reactions to potential threats (‘anxiety’). In both cases, how-ever, an animal may use cues in the environment to assess the presence of threat, and to thereby launch the appropriateresponse(s). However, detection and preparation for potential threats can extend, at least in humans, beyond a responsetethered to perceptible cues in the environment. A capacity for internally generated thinking enables humans to representpotential future threats (prospectively) or reflect on those that they have already experienced (retrospectively), without hav-ing to rely on information available in their immediate surroundings (Pearson, Naselaris, Holmes, & Kosslyn, 2015; Schooleret al., 2011; Suddendorf & Corballis, 2007).In this paper, we present a taxonomy of threat-related internally generated cognition that comprises episodic and seman-tic formats of memory and prospection, based on an earlier taxonomy presented by Suddendorf and Corballis (2007). Foreach of the capacities in this taxonomy, we address both proximate mechanisms (in terms of content and phenomenology,cognitive characteristics, development and underlying neurobiology), as well as ultimate questions (in terms of evolutionaryheritage and function). As was recognised by early thinkers in ethology (Mayr, 1961; Tinbergen, 1963), there is utility inembedding mechanisticexplanations in their proper evolutionarycontext(Scott-Phillips, Dickins,& West, 2011). Thus, whileSeneca in the opening quote regards threat-related memory and prospection as a curse, we propose that despite their costsfor wellbeing, these capacities have characteristics that suggest they have been shaped by natural selection as tools in thestruggle for survival and reproduction. 2. What are threats? We here broadly define a threat in evolutionary terms, in line with previous accounts (Gray & McNaughton, 2003; Marks& Nesse, 1994), as any aspect of the environment that could be detrimental to the fitness of the organism. Humans haveevolved systems to detect and manage at least certain classes of these threats that have been encountered over many gen-erations in ancestral environments (Beck, Emery, & Greenberg, 1985; Blanchard et al., 2011; Neuberg, Kenrick, & Schaller,2011; Sherlock, Zietsch, Tybur, & Jern, 2016; Stein & Nesse, 2011; Tooby & Cosmides, 1990). Our forebears were no doubtregularly confronted with many types of potential threats, ranging from the quasi-universal risk of attacks by predators(Barrett, 2005; Hart & Sussman, 2005; Mobbs, Hagan, Dalgleish, Silston, & Prévost, 2015) to more subtle risks such as a lossof social status with potentially severe implications for access to cooperative partners, mates, or resources (Bulley, Miloyan,Brilot, Gullo, & Suddendorf, 2016; Gilbert, 2001; Trower, Gilbert, & Sherling, 1990).It has been suggested that different, albeit somewhat overlapping, processes have evolved in humans for the detectionand management of threats in different domains and under different circumstances (Blanchard, Hynd, Minke, Minemoto,& Blanchard, 2001; Harrison, Ahn, & Adolphs, 2015; Marks & Nesse, 1994; Stein & Bouwer, 1997). Detecting a cue of socialthreat (i.e. to one’s status), for example, entails a different set of processes than detecting a cue that a predator is lurkingnearby (Sterelny, 2003). For instance, a social threat to status may uniquely require the visual decoding of signs of disap-proval on another person’s face and interpretation of their intentions. However, there are also shared aspects of threat-detection and response to seemingly disparate threats, such as a state of enhanced vigilance that is useful for many kindof dangers (Brilot, Bateson, Nettle, Whittingham, & Read, 2012; Eilam et al., 2011; Mobbs et al., 2015). Different anxietyresponses may therefore represent partially segregated systems for the detection and subsequent management of differentclasses of threat encounteredin past environments, particularly in cases where a generalized response would not sufficientlymitigate the risk (Brilot et al., 2012; Cosmides & Tooby, 1994; McNaughton, 1989; Nesse, 1990; Tooby & Cosmides, 1990). 54  A. Bulley et al./Consciousness and Cognition 49 (2017) 53–69  These different detection and response processes manifest at extreme levels as the various subtypes of anxiety observed incontemporary humans. Social anxiety disorder, for instance, can be conceptualised as the pathological expression of theadaptive social anxiety trait that evolved because it facilitates the navigation of complex social hierarchies (Gilbert, 2001;Stein, 2015; Trower et al., 1990).A common distinction in the threat-management literature is between immediate or  manifest   threats on the one hand,and  potential  future threats on the other (Boyer & Lienard, 2006; Eilam et al., 2011). It is now widely agreed that animalsrespond to immediately perceptible manifest threats (i.e. the emergence of a predator from behind a bush) with ‘fear’and/or a ‘defensive’ response (see Adolphs, 2013; LeDoux, 1998). In contrast, when detecting and responding to cues of   potential  (future) threats (i.e. the sound of leaves rustling), an anxiety response is more typical. In both cases, however, cuesin the perceptual environment form the basis of these responses.Humans are additionally capable of representing threats even in the absence of any relevant sensory cues through themental simulation of past and future scenarios (Boyer & Bergstrom, 2011; Miloyan, Bulley, & Suddendorf, 2016; Mobbset al., 2015; Perkins, Arnone, Smallwood, & Mobbs, 2015; Suddendorf & Corballis, 2007). Humans are also capable of theabstract, general representation of threat by drawing on semantic knowledge about how the environment used to be, orhow it might be in the future (Wu, Szpunar, Godovich, Schacter, & Hofmann, 2015). Together, these capacities afford enor-mous flexibility in how an individual can respond behaviourally to a variety of potential dangers without being limited tocurrently incoming perceptual cues. We now turn to a discussion of future-oriented threat-detection and response inhumans, by considering the contribution of both episodic and semantic processes. 3. Semantic and episodic processes in internally generated thinking  Traditionally, declarative memory refers to the capacity to process information that can be explicitly recalled, and thusconsists of both facts or knowledge about the world – semantic memory – as well as autobiographical details about one’sexperiences – episodic memory (Martin-Ordas, Atance, & Caza, 2014; Raby & Clayton, 2009; Squire, 1992; Tulving, 1972;Tulving, 1985a; Tulving, 1985b). Semantic memory is therefore generally conceptualised as being ‘knowledge-based’ andepisodic memory as ‘event-based’. Tulving (1985b) suggested that while episodic memory was hallmarked by a kind of ‘au-tonoetic’ (‘self-knowing’) consciousness that involved the first-person subjective experience of previously lived events,semantic memory instead was a form of ‘noetic’ (knowing) consciousness that did not require such mental simulation(see also Szpunar & Tulving, 2011; Wheeler, Stuss, & Tulving, 1997). These memory processes are now considered integralto thinking about or imagining the future (  prospection ), and while they rely on partly dissociable neural systems, their inter-dependence is essential for episodic ‘mental time travel’ in both temporal directions (Irish, Addis, Hodges, & Piguet, 2012;Irish & Piguet, 2013; Klooster & Duff, 2015; Martin-Ordas, Atance, & Louw, 2012; Suddendorf & Corballis, 1997;Suddendorf & Corballis, 2007; Szpunar, 2010; Szpunar, Spreng, & Schacter, 2014). However, the contributions of thesesub-systems to threat management processes have not, to our knowledge, been discussed.The distinction between episodic and semantic processes coincides with research on ‘representational formats’ or ‘modes’of thinkingthatemphasizeverbalversus imagerycodingschemes (Paivio,1986; see also Stawarczyk,Cassol,& D’Argembeau, 2013). In memory and prospection, semantic knowledge is usually conceptualised as abstracted and primarily verbal-linguistic, whilst episodic knowledge is more commonly conceptualised as an imagery-based thought process involvingthe projection of the self into mentally constructed scenarios of another time or place (Buckner & Carroll, 2007; Klein,Loftus, & Kihlstrom, 2002; Kosslyn, 1980; Suddendorf & Corballis, 2007). Note, however, that this does not rule outimagery-based representations of semantic facts, or verbal-linguistic representation of episodic events. Some authors haveargued that episodic processes should be regarded as a general mental scenario building capacity that encompasses theinternal generation of mental imagery relating not only to past and future events, but also fictitious scenarios, theory of mind, dreaming, and more generally creative thought (Addis, Wong, & Schacter, 2007; Domhoff & Fox, 2015; Dong,Collier-Baker, & Suddendorf, 2015; Hassabis & Maguire, 2009; Mullally & Maguire, 2013; Suddendorf, 2013).From a neural perspective, a number of authors have proposed that these varied imagery-based activities are the productof the  default mode network  of brain regions that includes the medial temporal lobe, midline prefrontal cortex, and cingulatecortex (Buckner, Andrews-Hanna, & Schacter, 2008; Konishi, Mclaren, Engen, & Smallwood, 2015; Raichle et al., 2001;Smallwood et al., 2013; Spreng & Grady, 2010). Recent studies also demonstrate a large overlap between the default modenetwork and the ‘semantic knowledge network’ (Binder, Desai, Graves, & Conant, 2009), and the results of lesion studies sug-gest that semanticknowledge plays a critical – if not pivotal – role in episodic cognition (Binder & Desai, 2011; Irish & Piguet,2013; Irish et al., 2012).In sum, semantic and episodic processes collectively comprise dissociable but interacting forms of ‘internally generatedthinking’ (Smallwood & Schooler, 2015; Suddendorf & Corballis, 2007; Szpunar et al., 2014). In both cases, these processesentail ‘detached’ representations that are not entirely contingent upon cues drawn from the immediate perceptual environ-ment, despite the influence these cues might have on resulting content and phenomenology (Craik, 1943; Gärdenfors, 1996).Together, episodic and semantic processes enable the spatiotemporally detached representation of threats in different ways– both in retrospective memory and in prospective cognition (see MacLeod, Tata, Kentish, & Jacobsen, 1997). We will explorehow these processes provide diverse mechanistic inroads to the same adaptive challenge of detecting and managing threats  A. Bulley et al./Consciousness and Cognition 49 (2017) 53–69  55
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