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Surviving Threats: Neural Circuit and Computational Implications of a New Taxonomy of Defensive Behaviour

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Surviving Threats: Neural Circuit and Computational Implications of a New Taxonomy of Defensive Behaviour REVIEWS Surviving threats: neural circuit and computational implications of a new taxonomy of defensive behaviour Joseph LeDoux1,2,3* and Nathaniel D. Daw4 Abstract | Research on defensive behaviour in mammals has in recent years focused on elicited reactions; however, organisms also make active choices when responding to danger. We propose a hierarchical taxonomy of defensive behaviour on the basis of known psychological processes. Included are three categories of reactions (reflexes, fixed reactions and habits) and three categories of goal-directed actions (direct action–outcome behaviours and actions based on implicit or explicit forecasting of outcomes). We then use this taxonomy to guide a summary of findings regarding the underlying neural circuits. Innate behaviours As soon as there is life, there is danger. distinctions have been studied mainly in appetitive 1 Behaviours, such as reflexes Ralph Waldo Emerson behaviour, it is similarly necessary to go beyond super‑ and fixed responses, that all ficial similarities and differences in order to understand members of a species share as As the eminent comparative psychologist T. C. Schneirla the psychological processes, computations and neural part of their heritage and that 2 make minimal demands on noted, behaviour is a decisive factor in natural selection : mechanisms underlying defensive responses. In light of learning. life is a dangerous undertaking, and those organisms this, we here propose a hierarchical taxonomy of defen‑ that are adept at surviving live to pass their genes on to sive behaviours on the basis of their known psychological their offspring. Predators are pervasive sources of harm processes. We use this framework to organize a review of to animals, and most predators are themselves prey to the neural circuit and, where possible, the computational other animals. As a result, nervous systems are typi‑ basis of specific behavioural examples of each of the var‑ cally equipped with predatory defence systems. This is ious response modes in the defensive hierarchy and to true of invertebrate and vertebrate species, and within identify gaps and hypotheses for future work. mammals, defence circuits are highly conserved3–5. Although humans are only minimally affected by A defensive taxonomy predatory attacks from other animals, our predatory Our taxonomy partly overlaps with and extends the defence systems have been co‑opted to cope with social tripartite division between Pavlovian, habitual and 1Center for Neural Science threats arising from members of our own species6,7. goal‑ directed responses proposed in the context of and Department of Thus, understanding how the human brain responds appetitive behaviour by Dickinson and Balleine10,13,14. In Psychology, New York innate University, New York, NY, USA to threats is important for both well‑being and men‑ their scheme, Pavlovian responses are defined as 2Department of Psychiatry tal health because psychological disorders centred on behaviours that come under the control of novel stimuli and Department of Child and pathological threat processing are common8,9. Because through associative learning and arbitrary learnedin- Adolescent Psychiatry, of the limitations of studies of the human brain, inves‑ strumental responses (such as lever‑pressing) are divided New York University Langone tigations of conserved defensive networks in other into habits and goal‑directed actions. Whereas goal-­ Medical School, New York, NY, USA. mammals have provided a viable approach for acquir‑ directed actions depend on their association with out‑ 3Nathan Kline Institute ing information relevant to human defensive circuitry. comes, habits are typically instrumental responses that for Psychiatry Research, However, our ability to understand the neural circuits have lost their relationship to the outcome over time. Orangeburg, NY, USA. underlying any class of behaviour is only as good as our These psychological categories have also been linked 4Princeton Neuroscience Institute and Department of understanding of the behaviour itself. to distinct approaches to the computational problem 12 Psychology, Princeton Organisms can respond to danger in a number of of evaluating and selecting favourable actions : specifi‑ University, Princeton, NJ, ways. In recent years, it has become apparent that sim‑ cally, goal‑directed actions are thought to correspond to USA. ilar behaviours can arise from distinct psychological ‘model‑ based’ algorithms for evaluating actions on the *e‑mail: [email protected] processes that depend on different neural circuits10 and basis of their outcomes, whereas habits are ‘model‑free’ doi:10.1038/nrn.2018.22 embody distinct computational approaches to the prob‑ without such computations. Although this taxonomy Published online 29 Mar 2018 lem of controlling action11,12. Although many of these has been both influential and useful, we recommend NATURE REVIEWS | NEUROSCIENCE ADVANCE ONLINE PUBLICATION | 1 ©2018 Mac millan Publishers Li mited, part of Spri nger Nature. All ri ghts reserved. REVIEWS Instrumental responses that its focus be modified and extended to broaden the Innate responses Responses that are learned scope of responses covered in both the appetitive and Defensive reflexes. If you step on a sharp object bare‑ because of their relationship aversive domains. footed, your leg reflexively withdraws. If an insect flies with some consequent Rather than focusing on learned associations, our close to your eye, you reflexively blink to protect the outcome (such as safety or food) and include both actions taxonomy treats unlearned or innate responses as foun‑ underlying tissues. Reflexes such as these are more or and habits. dational. In particular, we distinguish between two cat‑ less hardwired stimulus–response connections that egories of innate reactions: reflexes and fixed reaction are automatically and rapidly triggered by an innately Habits patterns. These responses are automatically elicited programmed stimulus (known as an unconditioned Learned behaviours that are by external stimuli. Both of these types of reaction stimulus (US)). They are part of an organism’s species acquired as a result of their initial relation to an outcome can also come under the control of Pavlovian stimuli; heritage and are common to all members of the spe‑ but do not depend on the thus, together they subsume Dickinson and Balleine’s cies. Reflexes are typically graded (that is, the more value of the outcome. Pavlovian category. We also adopt and extend their intense the stimulus, the stronger the response (up to instrumental categories: alongside habits, we thus sub‑ a limit)) and usually involve one muscle or a limited Actions Behaviours that result in an divide goal‑directed behaviours into three categories set of muscles. From a computational perspective, expected outcome as a of actions (behaviours that result in some expected reflexes (and the fixed reaction patterns described consequence of a previously outcome) according to how their outcome is forecast. below) constitute largely preprogrammed responses learned contingency between Specifically, in addition to those actions that use learned, to different types of event11. They are adapted to the the behaviour and its outcome direct action–outcome associations, we also consider organism’s ethological niche and, within the organism, (action–outcome behaviours) 5,15 or of deliberative cognitive those in which goals are forecast indirectly through to the particular context . Reflexes occur throughout forecasting (implicit or explicit) deliberative cognitive processes. Computationally, this invertebrate and vertebrate phyla as part of their innate of a possible outcome. corresponds to the recognition that there are multiple survival repertoire. types of model‑based controllers, using different types A defensive behavioural reflex that has been studied Reactions startle16,17 Behaviours — such as reflexes, of model. We include both implicit (nonconscious) and extensively in mammals is . This flinch‑like fixed responses and habits — explicit (conscious) forecasts, which helps to account response involves muscles up and down the body. The that are directly elicited by for dissociations in neural mechanisms and provides neck and back of mammals are outside of their visual innate or learned stimuli. a basis for considering the role of states such as fear field, and startle reflexes protect the organism in the case in these behaviours. The result is a hierarchical taxon‑ of a predatory attack to these areas by shortening and Startle A flinch-like behavioural reflex omy consisting of six categories of behaviours: innate stiffening muscles, thus reducing exposure and making often studied in the laboratory species‑typical reflexes and fixed reactions, learned penetration more difficult. The reflex can be elicited by by using sudden, loud acoustic instrumental responses and actions based on noncon‑ touch, acoustic stimuli or vestibular stimuli, and combi‑ stimuli. scious or conscious deliberation (TABLE 1). Importantly, nations of these produce more robust responses. In lab‑ although we use this taxonomy to discuss defensive oratory settings, startle is often studied by using sudden, behaviours, it may apply equally well to the appetitive loud acoustic stimuli. domain. The defensive behaviours in these six catego‑ Defensive reflexes such as startle, although innate, ries occur to differing degrees in different organisms in can be modulated by learning. For example, an innoc‑ the animal
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