Cognitive Control of Escape Behaviour
Authors: Dominic A. Evans, A. Vanessa Stempel, Ruben Vale, Tiago Branco
Journal: Trends in Cognitive Sciences (2019)

Escape behaviours are not only simple stimulus-reactions but are under cognitive control, allowing the study of processes such as decision-making and action selection in tractable organisms in ethological settings. Successful escape relies on integrating multiple external and internal variables, such as for computing flight trajectories towards shelter, and implementing trade-offs by choosing between actions that satisfy competing motivations. Some neural mechanisms of escape are innate and conserved across species, but are subject to control and modification by multiple systems, including the neocortex, which allow experience to be flexibly incorporated into escape behaviour. New tools to quantify behaviour while recording neural activity enable analysis of ethologically-relevant behaviours in complex environments, and will advance our understanding of the neural basis of natural behaviours. When faced with potential predators, animals instinctively decide whether there is a threat they should escape from, and also when, how, and where to take evasive action. While escape is often viewed in classical ethology as an action that is released upon presentation of specific stimuli, successful and adaptive escape behaviour relies on integrating information from sensory systems, stored knowledge, and internal states. From a neuroscience perspective, escape is an incredibly rich model that provides opportunities for investigating processes such as perceptual and value-based decision-making, or action selection, in an ethological setting. We review recent research from laboratory and field studies that explore, at the behavioural and mechanistic levels, how elements from multiple information streams are integrated to generate flexible escape behaviour. When faced with potential predators, animals instinctively decide whether there is a threat they should escape from, and also when, how, and where to take evasive action. While escape is often viewed in classical ethology as an action that is released upon presentation of specific stimuli, successful and adaptive escape behaviour relies on integrating information from sensory systems, stored knowledge, and internal states. From a neuroscience perspective, escape is an incredibly rich model that provides opportunities for investigating processes such as perceptual and value-based decision-making, or action selection, in an ethological setting. We review recent research from laboratory and field studies that explore, at the behavioural and mechanistic levels, how elements from multiple information streams are integrated to generate flexible escape behaviour. Escape (see Glossary) is an instinctive defensive behaviour that has evolved to avoid harm from predators and other threats in the environment. Animals that fail to escape from imminent threats will suffer reduced fitness, catastrophically in the case of death, but also in the case of injury, for example owing to reduced ability to forage for food or weakening in social status [1Lima S.L. Dill L.M. Behavioral decisions made under the risk of predation: a review and prospectus.Can. J. Zool. 1990; 68: 619-640Crossref Google Scholar]. Evolution has produced many different expressions of escape behaviour that reflect aspects such as biomechanics, the nature of the threat, local ecology or individual history, and which range from simple to extraordinarily complex [2Wilson A.M. et al.Biomechanics of predator–prey arms race in lion, zebra, cheetah and impala.Nature. 2018; 554: 183-188Crossref PubMed Scopus (12) Google Scholar]. At one end of the spectrum, animals might escape a fast-approaching predator by moving away with reflex-like actions, such as the 'jack-knife' tail flip in crayfish and the C-start escape in fish [3Zottoli S.J. Faber D.S. The Mauthner cell: what has it taught us?.Neuroscientist. 2000; 6: 26-38Crossref Google Scholar, 4Herberholz J. Marquart G.D. Decision making and behavioral choice during predator avoidance.Front. Neurosci. 2012; 6: 125Crossref PubMed Scopus (34) Google Scholar]. At the other end, successfully escaping from threats can require cognitive processes, including using memory and deciding between alternative options. For example, animals escaping in complex environments need to use knowledge of refuge locations and escape routes, and prey escaping from a pursuing pack of predators must dynamically compute escape strategies and trajectories [5Cooper W.E.J. Blumstein D.T. Escaping from Predators: An Integrative View of Escape Decisions. 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The computation of escape behaviour therefore integrates information from various streams, which creates the flexibility necessary for animals to survive in dynamic environments, and produce escapes that minimize reaction time in response to imminent threats, or that maximize success by considering as much information as possible. This information can be extracted at the time of the encounter (e.g., the nature of the threat and the current state of the environment), derive from prior experience (e.g., expectation about the outcome of the escape action), and also arise from internal signals of the state of the animal, such as hunger or anxiety. The ability to robustly trigger escape in a stimulus-dependent manner, together with the potential for investigating it in conditions that require different levels of cognitive complexity, make escape behaviour a powerful ethological model for systems neuroscience and mechanistic studies of cognition. Classic ethological field work has revealed many principles of escape at the behavioural level [5Cooper W.E.J. Blumstein D.T. Escaping from Predators: An Integrative View of Escape Decisions. Cambridge University Press, 2015Crossref Google Scholar], whereas laboratory studies aiming to understand the neurophysiology of escape have traditionally focused on fast stimulus-escape reactions, such as jumping escapes in locusts and flies [9Card G.M. Escape behaviors in insects.Curr. Opin. Neurobiol. 2012; 22: 180-186Crossref PubMed Scopus (39) Google Scholar, 10Fotowat H. Gabbiani F. Collision detection as a model for sensory-motor integration.Annu. Rev. Neurosci. 2011; 34: 1-19Crossref PubMed Scopus (68) Google Scholar]. There is thus a gap between our understanding of the biological mechanisms of escape and the complex behaviours displayed by animals escaping in natural environments. However, recent advances in behaviour monitoring and recording techniques in freely moving animals promise to bridge this gap, and open the way for understanding how neural circuits implement the cognitive processes that control escape behaviour. Here we review evidence that escape is a flexible behaviour under cognitive control, as well as some of the currently known underlying neural mechanisms (see further references in the supplemental information online). We consider three time points: threat detection, escape initiation, and escape execution (Figure 1). In addition to structuring escape into separate control points, this division generalizes to classes of problems that the brain must solve when computing any behaviour, namely classifying sensory information, selecting, and then executing flexible actions (Figure 2), and further underscores the power of using escape behaviour as a model for systems neuroscience.Figure 2Flexibility of Escape Execution in Different Species. Escape directionality depends on the presence and location of shelter (left panels). (Top) When an animal has knowledge that a refuge is inaccessible, absent, or too far away, the predominant response to threat switches from escape to freezing behaviour. (Bottom) The presence of a suitable refuge in the environment guides precise escape trajectories to its location. If a refuge becomes unavailable and the animal finds a new one, flight paths are modified accordingly very rapidly. Escape trajectories are threat-dependent (middle panels). (Top) The type and location of a predator influences escape trajectory. A frog directs its escape away from a terrestrial predator such as a snake, but flees towards an aerial predator such as a bat to undercut their flight path [117Bulbert M.W. et al.Danger comes from all fronts: predator-dependent escape tactics of túngara frogs.PLoS One. 2015; 10e0120546Crossref PubMed Scopus (8) Google Scholar]. (Bottom) Animals including birds, deer, fish, and frogs flee directly away from threatening stimuli, which may function to maximize the distance between predator and prey. The same animals can also escape at a 130–90° angle, for example, to facilitate visual monitoring of predators during escape in response to less threatening stimuli, or as a less predictable, evasive manoeuvre in response to a fast predatory strike [118Lind J. et al.Split-second escape decisions in blue tits (Parus caeruleus).Naturwissenschaften. 2002; 89: 420-423Crossref PubMed Scopus (25) Google Scholar]. The physical and social environment modulates escape (right panels). (Top) Flight trajectories take into account the presence of obstacles in the environment. For example, fish that usually flee away from an approaching predator may escape towards it if an obstacle occludes the optimal escape path. (Bottom) Solitary fish can initiate escapes at various onset angles, whereas schooling fish escape in straight and uniform trajectories owing to the spatial constraints imposed by the shoal.View Large Image Figure ViewerDownload Hi-res image Download (PPT) The first step in the computation of escape behaviour is to evaluate sensory information to identify whether a threat is present. This is a classification operation where sensory stimuli are sorted into threatening or not-threatening, and includes a perceptual component (is the stimulus there?) and a value component (is it threatening or not?). Animals must detect, identify, and evaluate threats based on sensory features such as shape, size, speed, or smell. For most animal species there are stimuli that innately carry negative valence, which is essential for surviving and escaping from predators without needing to rely on prior exposure to learn that they are threatening. 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