Order in Spontaneous Behavior

Maÿe, Alexander; Hsieh, Chih‐hao; Sugihara, George; Brembs, Björn

doi:10.1371/journal.pone.0000443

Cited by 210 publications

(219 citation statements)

References 92 publications

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“…(similar to our shorter experiments here) has shown that, during extended flights, the occurrence of turning maneuvers can be described by a Lévi distribution (Maye et al, 2007). Such distributions of behavioral output, seen in foraging behavior in many animals, are characteristically long-tailed.…”

Section: Discussionsupporting

confidence: 85%

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Attention-Like Deficit and Hyperactivity in aDrosophilaMemory Mutant

Swinderen¹,

Brembs²

2010

J. Neurosci.

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The primary function of a brain is to produce adaptive behavioral choices by selecting the right action at the right time. In humans, attention determines action selection as well as memory formation, whereas memories also guide which external stimuli should be attended to (Chun and Turk-Browne, 2007). The complex codependence of attention, memory, and action selection makes approaching the neurobiological basis of these interactions difficult in higher animals. Therefore, a successful reductionist approach is to turn to simpler systems for unraveling such complex biological problems. In a constantly changing environment, even simple animals have evolved attention-like processes to effectively filter incoming sensory stimuli. These processes can be studied in the fruit fly, Drosophila melanogaster, by a variety of behavioral and electrophysiological techniques. Recent work has shown that mutations affecting olfactory memory formation in Drosophila also produce distinct defects in visual attention-like behavior (van Swinderen, 2007; van Swinderen et al., 2009). In this study, we extend those results to describe visual attention-like defects in the Drosophila memory consolidation mutant radish 1 . In both behavioral and brain-recording assays, radish mutant flies consistently displayed responses characteristic of a reduced attention span, with more frequent perceptual alternations and more random behavior compared with wild-type flies. Some attentionlike defects were successfully rescued by administering a drug commonly used to treat attention-deficit hyperactivity disorder in humans, methylphenidate. Our results suggest that a balance between persistence and flexibility is crucial for adaptive action selection in flies and that this balance requires radish gene function.

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Section: Discussionsupporting

confidence: 85%

“…Flies were tethered as described previously (Maye et al, 2007) and tested the following day for flight behavior (for a video of the procedure, see Brembs, 2008). The duration of the experiments had to be confined to 6 min because radish mutants were reluctant to fly continuously in the arena.…”

Section: Methodsmentioning

confidence: 99%

Attention-Like Deficit and Hyperactivity in aDrosophilaMemory Mutant

Swinderen¹,

Brembs²

2010

J. Neurosci.

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“…Under such conditions, an innate movement process could account for the movement patterns we observed in albatrosses, and could apply more generally. Although there is no clear evidence of an innate Lévy process driving movements of vertebrates, experimental studies have shown that in featureless environments Drosophila activity patterns are well approximated by a Lévy flight (8,27). Furthermore, Drosophila with silenced parts of the brain's mushroom body, or modified dopaminergic signaling-circuitry linked to decision-making-show disrupted activity patterning and behavioral burstiness, where burstiness is described as heavy-tailed distributions of move or pause times (28).…”

Section: Resultsmentioning

confidence: 99%

Foraging success of biological Lévy flights recorded in situ

Humphries

Weimerskirch

Queiroz

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

316

357

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It is an open question how animals find food in dynamic natural environments where they possess little or no knowledge of where resources are located. Foraging theory predicts that in environments with sparsely distributed target resources, where forager knowledge about resources' locations is incomplete, Lévy flight movements optimize the success of random searches. However, the putative success of Lévy foraging has been demonstrated only in model simulations. Here, we use high-temporal-resolution Global Positioning System (GPS) tracking of wandering (Diomedea exulans) and black-browed albatrosses (Thalassarche melanophrys) with simultaneous recording of prey captures, to show that both species exhibit Lévy and Brownian movement patterns. We find that total prey masses captured by wandering albatrosses during Lévy movements exceed daily energy requirements by nearly fourfold, and approached yields by Brownian movements in other habitats. These results, together with our reanalysis of previously published albatross data, overturn the notion that albatrosses do not exhibit Lévy patterns during foraging, and demonstrate that Lévy flights of predators in dynamic natural environments present a beneficial alternative strategy to simple, spatially intensive behaviors. Our findings add support to the possibility that biological Lévy flight may have naturally evolved as a search strategy in response to sparse resources and scant information.optimal foraging | organism | predator-prey | telemetry | evolution T heoretically, in situations where animals possess limited or no information on the whereabouts of resources, a specialized random walk known as a Lévy flight can yield encounters with sparsely and randomly distributed targets (e.g., prey) more efficiently than random walks such as Brownian motion (1, 2), which are efficient where prey is abundant (3) and probably more predictable (4, 5). Lévy flight, in which movement displacements (steps) are drawn from a probability distribution with a powerlaw tail (a Pareto-Lévy distribution), describes a search pattern composed of many small-step 'walk clusters' interspersed by longer relocations. This pattern is repeated across all scales, such that PðlÞ ∼ l −μ , with 1 < μ ≤ 3 where l is the flight length (move-steplength), and μ the power-law exponent. Simple model simulations of Lévy search generally describe a forager moving along consecutive step lengths drawn from a power law distribution, such that when randomly and sparsely distributed prey is detected within a "sensory" field, the current step length is terminated, the prey is consumed and then a new random direction and step length are selected (3). These Lévy search-model simulations indicate an optimal exponent of μ ≈ 2 for the power-law move-step frequency distribution, leading to searches that increase the probability of a forager encountering new prey patches (1-3). In recent years, Lévy flight or Lévy walk patterns approaching the theoretically optimal value of μ ≈ 2 have been identified in movements of divers...

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“…In saltatory searches, where scanning is discontinuous, reorientation behavior might be linked to decision-making mechanisms capable of stopping and/or starting relocation moves in different directions. In both cases, the mechanisms themselves could consist of simple internal biological programs (6,43) or could emerge as interactive processes with other individuals (i.e., collective mechanisms of intermittence) or the environment (i.e., relocation displacements). As occurs in dispersal processes, for example, many animals could actively take benefit of external transportation devices (e.g., winds, ocean currents, other animals) as part of a search strategy.…”

Section: Discussionmentioning

confidence: 99%

“…There are some examples in the literature showing that at least for ''simple'' organisms (e.g., bacteria, flagellates, fruit flies) motor-related neuronal configurations (43,44) and biochemical paths (45) could be responsible for a Lévy timing of reorientations (12,13,44,46). Empirical evidence of such fractal reorientation clocks at different levels of biological organization (e.g., neuronal, biochemical, physiological, behavioral) could explain, to some extent, the presence of Lévy flights and scale-free (i.e., fractal) properties in the movement patterns of some animals (e.g., refs.…”

Section: Discussionmentioning

confidence: 99%

Fractal reorientation clocks: Linking animal behavior to statistical patterns of search

Bartumeus

Levin

2008

Proc. Natl. Acad. Sci. U.S.A.

176

231

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The movement ecology framework depicts animal movement as the result of the combined effects of internal and external constraints on animal navigation and motion capacities. Nevertheless, there are still fundamental problems to understand how these modulations take place and how they might be translated into observed statistical properties of animal trajectories. Of particular interest, here, is the general idea of intermittence in animal movement. Intermittent locomotion assumes that animal movement is, in essence, discrete. The existence of abrupt interruptions in an otherwise continuous flow of movement allows for the possibility of reorientations, that is, to break down previous directional memories of the trajectory. In this study, we explore the potential links between intermittent locomotion, reorientation behavior, and search efficiency. By means of simulations we show that the incorporation of Lé vy intermittence in an otherwise nonintermittent search strongly modifies encounter rates. The result is robust to different types of landscapes (i.e., target density and spatial distribution), and spatial dimensions (i.e., 2D, 3D). We propose that Lé vy intermittence may come from reorientation mechanisms capable of organizing directional persistence on time (i.e., fractal reorientation clocks), and we rationalize that the explicit distinction between scanning and reorientation mechanisms is essential to make accurate statistical inferences from animal search behavior. Finally, we provide a statistical tool to judge the existence of episodic and strong reorientation behaviors capable of modifying relevant properties of stochastic searches, ultimately controlling the chances of finding unknown located items.animal movement ͉ intermittent locomotion ͉ Lé vy walks ͉ random walks ͉ search strategies T he movement ecology framework explicitly recognizes animal movement as the result of a constant ''dialogue'' between environment (external factors) and animal internal states. This dialogue affects organisms' motion and/or navigation capacities to finally produce the actual movement (1). Beyond phenomenological descriptions of movement, the random paradigm (1) should seek to understand how interactions between the four components of the movement ecology framework (i.e., internal states, external forces, motion, and navigation capacities) might be translated into observed statistical patterns of movement (2, 3). In the present work, we suggest that a major advance in bridging the gap between animal behavior (mechanistic approach) and the statistical properties of search strategies involves a statistical reinterpretation of the idea of intermittent locomotion (4-6).The biological principle of intermittent locomotion assumes that animal behavior unavoidably produces observable punctuations in the movement (e.g., stops, strong changes in speed). Thus, the forces generating movement operate discontinuously, producing pauses and speeding patterns on the move. Intermittent locomotion (also known as stop-and-go movement, pau...

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Order in Spontaneous Behavior

Cited by 210 publications

References 92 publications

Attention-Like Deficit and Hyperactivity in aDrosophilaMemory Mutant

Attention-Like Deficit and Hyperactivity in aDrosophilaMemory Mutant

Foraging success of biological Lévy flights recorded in situ

Fractal reorientation clocks: Linking animal behavior to statistical patterns of search

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