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A Review of the Diversity in Motor Control, Kinematics and Behaviour Paolo Domenici1,* and Melina E

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A Review of the Diversity in Motor Control, Kinematics and Behaviour Paolo Domenici1,* and Melina E © 2019. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2019) 222, jeb166009. doi:10.1242/jeb.166009 REVIEW Escape responses of fish: a review of the diversity in motor control, kinematics and behaviour Paolo Domenici1,* and Melina E. Hale2 ABSTRACT 1978a; Weihs, 1973) and neural control (Eaton et al., 1977; Eaton and The study of fish escape responses has provided important insights Hackett, 1984), and it focused on a small number of species (mainly into the accelerative motions and fast response times of these animals. goldfish, trout and pike). As a result, fish escapes were seen as In addition, the accessibility of the underlying neural circuits has made stereotyped responses (Webb, 1984a). This basic high-acceleration the escape response a fundamental model in neurobiology. Fish escape response was described as occurring in three stages: stage 1 ‘ ’ escape responses were originally viewed as highly stereotypic all-or- (see Glossary), the preparatory stage, in which the body bends none behaviours. However, research on a wide variety of species has rapidly with minimal translation of the centre of mass; stage 2 (see ‘ ’ shown considerable taxon-specific and context-dependent variability Glossary), the propulsive stroke, when the fish accelerates away from in the kinematics and neural control of escape. In addition, escape-like its initial position; and stage 3, in which the fish either continues motions have been reported: these resemble escape responses swimming or starts gliding (Weihs, 1973). The first two stages have kinematically, but occur in situations that do not involve a response to a been the focus of most literature on escape response kinematics threatening stimulus. This Review focuses on the diversity of escape (Webb, 1976, 1978a, 1982, 1986; Weihs and Webb, 1984), although responses in fish by discussing recent work on: (1) the types of escape later work showed that escape responses can consist of stage 1 only responses as defined by kinematic analysis (these include C- and (i.e. single-bend responses as opposed to double-bend responses; S-starts, and single- versus double-bend responses); (2) the diversity Domenici and Blake, 1997). Stage 1 involves one of two distinct of neuromuscular control; (3) the variability of escape responses in motor patterns: during the C-start, the body takes on the shape of a ‘ ’ ‘ ’ terms of behaviour and kinematics within the context of predator−prey C , and in the S-start, the body bends into an S shape. interactions; and (4) the main escape-like motions observed in various Subsequent work on fish escape responses has addressed a broad species. Here, we aim to integrate recent knowledge on escape range of species, and has demonstrated wide kinematic variability responses and highlight rich areas for research. Rapidly developing across species. More recent work has also revealed the use of escape- approaches for studying the kinematics of swimming motion both in the like motions (see Glossary) that resemble escape responses but that lab and within the natural environment provide new avenues for occur in the absence of a frightening stimulus (Canfield and Rose, research on these critical and common behaviours. 1993; Domenici et al., 2015; Wohl and Schuster, 2007). Escape response studies have developed to include a number of variables that KEY WORDS: Escape response, Fish, Kinematics, Mauthner cells, add to the traditional ‘locomotor-type’ variables (e.g. speed and Swimming acceleration) to assess escape performance and its relevance in terms of vulnerability to predators (Domenici, 2010a; Walker et al., 2005). Introduction Escape traits that are relevant for successfully avoiding predation The past two decades have seen rapid developments in the ability to include the escape latency (see Glossary), the distance at which the explore behaviour and its neural basis in a wide range of species, prey react to the approaching predator and the directionality (see thanks to automated approaches to recording the movement of Glossary), in addition to locomotor traits. All of these traits may be individual animals and groups (Dell et al., 2014; Neuswanger et al., affected by the behavioural context, such as whether the prey is: (i) 2016; Olsen and Westneat, 2015; Shamur et al., 2016). Accordingly, part of a school, (ii) engaged in feeding or (iii) near a refuge the analysis of animal movement and behaviour has become less (Domenici, 2010a,b). In addition, dissection of the neural circuits labour intensive and more sophisticated, making use of machine driving escape has provided detailed understanding of the escape learning and ‘big data’ (Hong et al., 2015; Valletta et al., 2017). By circuit and variations in its structure and use; although Mauthner (M) taking advantage of these techniques we can hope to achieve an cells are the primary reticulospinal neuron responsible for triggering integrative view of behaviour – one that links kinematics to motor fast escape responses, escapes controlled by other reticulospinal control in multiple species – by deriving basic principles through neurons can also occur (Korn and Faber, 2005; Liu and Fetcho, 1999). species comparison. The escape response of fish has provided not only a prime example of One rich system for exploring behavioural diversity is the fish simple sensorimotor circuits and their evolutionary diversity, but escape response (see Glossary) and related accelerative behaviours also allows us to begin to understand a broad repertoire of high- (collectively termed ‘fast starts’; see Glossary). Early work on fish acceleration behaviours performed by a large number of fish species. escape responses was based on kinematics (Webb, 1975, 1976; Webb, Here, we review the diversity of escape and related behaviours and their neural underpinnings. We aim to synthesize current findings and provide a foundation for future work on accelerative behaviours in 1Organismal Biology Laboratory, IAS-CNR LocalitàSa Mardini, Torregrande, Oristano 09170, Italy. 2Department of Organismal Biology and Anatomy, University fish. Understanding the diversity in the motor control and kinematic of Chicago, Chicago, IL 60637, USA. output of high-acceleration movements is fundamental for furthering our knowledge of how fish swim. Even more broadly, it can provide a *Author for correspondence ([email protected]) window into how organisms evolve and coordinate suites of P.D., 0000-0003-3182-2579; M.E.H., 0000-0001-5194-1220 responses in a number of behavioural contexts. Journal of Experimental Biology 1 REVIEW Journal of Experimental Biology (2019) 222, jeb166009. doi:10.1242/jeb.166009 Escape kinematics: diversity of escape responses In the past couple of decades, multiple types of escape response (e.g. C-start, S-start, single bend, double bend) have been examined in Glossary depth (Domenici and Batty, 1997; Fleuren et al., 2018; Hale, 2002; Directionality Lefrançois et al., 2005; Spierts and Leeuwen, 1999; Tytell and Lauder, Escape responses can be divided into away and towards responses, 2002). Consequently, the fast-start nomenclature has proliferated. In when the head of the fish moves away from or towards the position of the order to clarify the nomenclature, we propose a simple Venn diagram threat, respectively. Directionality can be measured as the percentage of illustrating the current definitions of the fast-start behaviours discussed away responses out of the total number of trials. below (Fig. 1). As a response to a threat, fish typically show a startle Escape angle The angle between (a) the line corresponding to the fish’s orientation at response (see Glossary), which can consist of an escape response (a the time of the stimulation and (b) the line corresponding to the fish sudden acceleration), a head retraction or a freezing response (see swimming trajectory at the end of the escape response. Glossary). Of these, only escape responses involve locomotion and are Escape latency considered fast starts; head retraction and freezing are startle responses The time interval between the onset of the threatening stimulus and the but not fast starts. While escape responses can be considered a type of first visible reaction by the fish. fast start, not all fast starts are escape responses: fast starts can also be Escape response predator strikes (see Glossary) or other accelerative motions. Finally, An accelerative motion performed as a response to a sudden threat. All escape responses are fast-starts, although not all fast starts are escape predators not only use strikes to capture their prey, prey capture can responses. also be aided by suction feeding (Fig. 1; Norton and Brainerd, 1993). Escape trajectory The kinematics of the main escape response variants and other The angular sum of the stimulus angle and the escape angle. accelerative behaviours, along with the behavioural contexts within Escape-like motion which they are used and what is known about their neural control, are Any accelerative motion that resembles an escape response from a outlined below and illustrated in Fig. 2. kinematic perspective, but that is not triggered by a frightening, predator- like stimulus. Fast start Stage 1 kinematics: C-starts and S-starts An accelerative motion from resting or swimming, that can be observed The two most common stage 1 kinematic patterns are the C-start and during various behavioural contexts, including predator−prey encounters S-start. These are different behaviours with distinct motor programs (i.e. predator strikes, escape responses) and social interactions. (e.g. Hale, 2002; Liu and Hale, 2017). To discern a true S-start from a Freezing C-start it is critical to use electromyography or other physiological A startle response involving cessation of any pre-startle movement and a period when the fish is alert but unmoving. approaches to determine whether the pattern of bending in stage 1 is Mauthner cells (M-cells) actively generated, as water resistance can cause passive caudal Two giant neurons in the hindbrain of most fish species. They are known bending and result in an S-like bend from a C-start motor to control stage 1 of the escape response (although non-M-cell-mediated pattern.
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