Steering by Hearing: A Bat’s Acoustic Gaze Is Linked to Its Flight Motor Output by a Delayed, Adaptive Linear Law

Ghose, Kaushik; Moss, Cynthia F.

doi:10.1523/jneurosci.4315-05.2006

Cited by 111 publications

(112 citation statements)

References 37 publications

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“…Previous studies have intensively examined spatial attention to a particular target (7)(8)(9)(10)(11)(12)(13)(14). However, in fact, predators usually capture successive prey items (e.g., aerial-feeding bats) (21).…”

Section: Discussionmentioning

confidence: 99%

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Echolocating bats use future-target information for optimal foraging

Fujioka

Aihara

Sumiya

et al. 2016

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

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When seeing or listening to an object, we aim our attention toward it. While capturing prey, many animal species focus their visual or acoustic attention toward the prey. However, for multiple prey items, the direction and timing of attention for effective foraging remain unknown. In this study, we adopted both experimental and mathematical methodology with microphone-array measurements and mathematical modeling analysis to quantify the attention of echolocating bats that were repeatedly capturing airborne insects in the field. Here we show that bats select rational flight paths to consecutively capture multiple prey items. Microphone-array measurements showed that bats direct their sonar attention not only to the immediate prey but also to the next prey. In addition, we found that a bat's attention in terms of its flight also aims toward the next prey even when approaching the immediate prey. Numerical simulations revealed a possibility that bats shift their flight attention to control suitable flight paths for consecutive capture. When a bat only aims its flight attention toward its immediate prey, it rarely succeeds in capturing the next prey. These findings indicate that bats gain increased benefit by distributing their attention among multiple targets and planning the future flight path based on additional information of the next prey. These experimental and mathematical studies allowed us to observe the process of decision making by bats during their natural flight dynamics.bat sonar | aerial capture | microphone array | mathematical modeling | flight dynamics S electively focusing attention on a particular target allows us to effectively extract information (1-4). Animals spatially focus their attention toward prey for suitable foraging (5, 6). During prey pursuit, most animals direct their visual attention toward it [e.g., tiger beetle (7), dragonfly (8), and falcon (9)]. Specifically, for example, dragonflies maintain a prey item at a constant retinal position during approaching it so that they steer an interception flight path (interception strategy) (10). However, for multiple prey items, the direction and timing of attention for effective foraging remain unknown.Echolocating bats actively emit sonar signals to obtain surrounding information and adaptively change the characteristics of the emissions depending on the situation (11). Therefore, their attention in terms of the sonar (sonar attention) is characterized as the direction to which bats emit their sonar beams (12-14). When echolocating bats approach an airborne insect, the sonar attention directs toward the prey (12, 13). During natural foraging, the sonar attention of bats alternately shifts from their flying direction to the side (15). Additionally the wild bats are capable of capturing two prey items within the short interval of 1 s (16).We predicted that bats localize multiple prey items by distributing their attention between them and then select an efficient flight path to successively capture the multiple prey. To test this prediction, ...

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Section: Discussionmentioning

confidence: 99%

“…Therefore, their attention in terms of the sonar (sonar attention) is characterized as the direction to which bats emit their sonar beams (12)(13)(14). When echolocating bats approach an airborne insect, the sonar attention directs toward the prey (12,13).…”

mentioning

confidence: 99%

Echolocating bats use future-target information for optimal foraging

Fujioka

Aihara

Sumiya

et al. 2016

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

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“…2 A), requires that the neural controller generate a velocity command to the motor plant. The power of these kinematic approaches, which are commonly used in the description of sensory-mediated locomotion (Collett et al, 1998;Srinivasan et al, 2000;Barron and Srinivasan, 2006;Ghose and Moss, 2006), is that they reduce task-level control of locomotion to simple kinematic movement, enabling one to find direct correlations between salient sensor readings and animal motion.…”

Section: B Models Of the C(s) Filter; Magnitude (In Decibels) Againsmentioning

confidence: 99%

The Critical Role of Locomotion Mechanics in Decoding Sensory Systems

2007

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How do neural systems process sensory information to control locomotion? The weakly electric knifefish Eigenmannia, an ideal model for studying sensorimotor control, swims to stabilize the sensory image of a sinusoidally moving refuge. Tracking performance is best at stimulus frequencies less than ϳ1 Hz. Kinematic analysis, which is widely used in the study of neural control of movement, predicts commensurately low-pass sensory processing for control. The inclusion of Newtonian mechanics in the analysis of the behavior, however, categorically shifts the prediction: this analysis predicts that sensory processing is high pass. The counterintuitive prediction that a low-pass behavior is controlled by a high-pass neural filter nevertheless matches previously reported but poorly understood high-pass filtering seen in electrosensory afferents and downstream neurons. Furthermore, a model incorporating the high-pass controller matches animal behavior, whereas the model with the low-pass controller does not and is unstable. Because locomotor mechanics are similar in a wide array of animals, these data suggest that such high-pass sensory filters may be a general mechanism used for task-level locomotion control. Furthermore, these data highlight the critical role of mechanical analyses in addition to widely used kinematic analyses in the study of neural control systems.

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“…The equation (1) showing the basic control law of the gaze and moving direction was suggested in some previous studies for bats while flying towards a given goal (tracking and attacking prey task) (Ghose and Moss, 2006) and human drivers during car racing (eye gaze and turn rate) (Land and Tatler, 2001). In the present study, we verified that the acoustic gaze and flight direction of the bats during free U-turn flights in the chamber basically followed this law.…”

Section: Discussionmentioning

confidence: 99%