Perception and steering control in paired bat flight

Animals within groups need to coordinate their reactions to perceived environmental features and to each other in order to safely move from one point to another. This paper extends our previously published work on the flight patterns of Myotis velifer that have been observed in a habitat near Johnson City, Texas. Each evening, these bats emerge from a cave in sequences of small groups that typically contain no more than three or four individuals, and they thus provide ideal subjects for studying leader-follower behaviors. By analyzing the flight paths of a group of M. velifer, the data show that the flight behavior of a follower bat is influenced by the flight behavior of a leader bat in a way that is not well explained by existing pursuit laws, such as classical pursuit, constant bearing and motion camouflage. Thus we propose an alternative steering law based on virtual loom, a concept we introduce to capture the geometrical configuration of the leader-follower pair. It is shown that this law may be integrated with our previously proposed vision-enabled steering laws to synthesize trajectories, the statistics of which fit with those of the bats in our data set. The results suggest that bats use perceived information of both the environment and their neighbors for navigation.2018-08-0

Optical flow sensing and the inverse perception problem for flying bats

The movements of birds, bats, and other flying species are governed by complex sensorimotor systems that allow the animals to react to stationary environmental features as well as to wind disturbances, other animals in nearby airspace, and a wide variety of unexpected challenges. The paper and talk will describe research that analyzes the three-dimensional trajectories of bats flying in a habitat in Texas. The trajectories are computed with stereoscopic methods using data from synchronous thermal videos that were recorded with high temporal and spatial resolution from three viewpoints. Following our previously reported work, we examine the possibility that bat trajectories in this habitat are governed by optical flow sensing that interpolates periodic distance measurements from echolocation. Using an idealized geometry of bat eyes, we introduce the concept of time-to-transit, and recall some research that suggests that this quantity is computed by the animals' visual cortex. Several steering control laws based on time-to-transit are proposed for an idealized flight model, and it is shown that these can be used to replicate the observed flight of what we identify as typical bats. Although the vision-based motion control laws we propose and the protocols for switching between them are quite simple, some of the trajectories that have been synthesized are qualitatively bat-like. Examination of the control protocols that generate these trajectories suggests that bat motions are governed both by their reactions to a subset of key feature points as well by their memories of where these feature points are located

Perceptual modalities guiding bat flight in a native habitat

Flying animals accomplish high-speed navigation through fields of obstacles using a suite of sensory modalities that blend spatial memory with input from vision, tactile sensing, and, in the case of most bats and some other animals, echolocation. Although a good deal of previous research has been focused on the role of individual modes of sensing in animal locomotion, our understanding of sensory integration and the interplay among modalities is still meager. To understand how bats integrate sensory input from echolocation, vision, and spatial memory, we conducted an experiment in which bats flying in their natural habitat were challenged over the course of several evening emergences with a novel obstacle placed in their flight path. Our analysis of reconstructed flight data suggests that vision, echolocation, and spatial memory together with the possible exercise of an ability in using predictive navigation are mutually reinforcing aspects of a composite perceptual system that guides flight. Together with the recent development in robotics, our paper points to the possible interpretation that while each stream of sensory information plays an important role in bat navigation, it is the emergent effects of combining modalities that enable bats to fly through complex spaces

Communicating through motion in dance and animal groups

This study explores principles of motion based communication in animal and human group behavior. It develops models of cooperative control that involve communication through actions aimed at a shared objective. Moreover, it aims at understanding the collective motion in multi-agent models towards a desired objective which requires interaction with the environment. In conducting a formal study of these problems, first we investigate the leader-follower interaction in a dance performance. Here, the prototype model is salsa. Salsa is of interest because it is a structured interaction between a leader (usually a male dancer) and a follower (usually a female dancer). Success in a salsa performance depends on how effectively the dance partners communicate with each other using hand, arm and body motion. We construct a mathematical framework in terms of a Dance Motion Description Language (DMDL). This provides a way to specify control protocols for dance moves and to represent every performance as sequences of letters and corresponding motion signals. An enhanced form of salsa (intermediate level) is discussed in which the constraints on the motion transitions are described by simple rules suggested by topological knot theory. It is shown that the proficiency hierarchy in dance is effectively captured by proposed complexity metrics. In order to investigate the group behavior of animals that are reacting to environmental features, we have analyzed a large data set derived from 3-d video recordings of groups of Myotis velifer emerging from a cave. A detailed statistical analysis of large numbers of trajectories indicates that within certain bounds of animal diversity, there appear to be common characteristics of the animals' reactions to features in a clearly defined flight corridor near the mouth of the cave. A set of vision-based motion control primitives is proposed and shown to be effective in synthesizing bat-like flight paths near groups of obstacles. A comparison of synthesized paths and actual bat motions culled from our data set suggests that motions are not based purely on reactions to environmental features. Spatial memory and reactions to the movement of other bats may also play a role. It is argued that most bats employ a hybrid navigation strategy that combines reactions to nearby obstacles and other visual features with some combination of spatial memory and reactions to the motions of other bats

Neural mechanisms underlying catastrophic failure in human-machine interaction during aerial navigation

Objective. We investigated the neural correlates of workload buildup in a fine visuomotor task called the boundary avoidance task (BAT). The BAT has been known to induce naturally occurring failures of human-machine coupling in high performance aircraft that can potentially lead to a crash; these failures are termed pilot induced oscillations (PIOs). Approach. We recorded EEG and pupillometry data from human subjects engaged in a flight BAT simulated within a virtual 3D environment. Main results. We find that workload buildup in a BAT can be successfully decoded from oscillatory features in the electroencephalogram (EEG). Information in delta, theta, alpha, beta, and gamma spectral bands of the EEG all contribute to successful decoding, however gamma band activity with a lateralized somatosensory topography has the highest contribution, while theta band activity with a frontocentral topography has the most robust contribution in terms of real world usability. We show that the output of the spectral decoder can be used to predict PIO susceptibility. We also find that workload buildup in the task induces pupil dilation, the magnitude of which is significantly correlated with the magnitude of the decoded EEG signals. These results suggest that PIOs may result from the dysregulation of cortical networks such as the locus coeruleus (LC) anterior cingulate cortex (ACC) circuit. Significance. Our findings may generalize to similar control failures in other cases of tight man machine coupling where gains and latencies in the control system must be inferred and compensated for by the human operators. A closed-loop intervention using neurophysiological decoding of workload buildup that targets the LC ACC circuit may positively impact operator performance in such situations.Comment: Manuscript as initially submitted to Journal of Neural Engineering in March, 201

Adaptive echolocation and flight behaviors in free-flying bats, Eptesicus fuscus

Echolocating bats emit ultrasonic sonar pulses and listen to returning echoes, which are reflected from targets or obstacles, to probe their surroundings. Their biological sonar system is well-developed and highly adaptive to the dynamic acoustic environment. Bats are also agile flyers and they can modify their flight behavior in order to capture insects efficiently. Adaptable echolocation and flight behaviors evolved in bats in response to environmental demands. This study employed changes in the external ear of bats and in the acoustic environment to examine how the big brown bat, Eptesicus fuscus, modifies its echolocation call design and flight patterns to cope with these new experimental conditions. Study one investigated the influences of changes in sound localization cues on prey capture behavior. The tragus, which is part of the external ear, is believed to contribute to sound localization in the vertical plane. Deflecting the tragus affected prey capture performance of the bat, but it adapted to this manipulation by adjusting its flight behavior. The tragus-deflected bat tended to attack the prey item from above and show lower tangential velocity and larger bearing from the side, compared with its flight pattern in the tragus intact conditions. The bat did not change its echolocation call design in the tragus-deflected condition. Study two paired two bats together and allowed them to perform a prey capture task in a large flight room. Echolocating bats showed two adaptive strategies in their echolocation behavior when flying with another conspecific. The bat either stopped vocalizing or increased its difference in call design from the other bat. In addition, one bat tended to follow another bat when flying together and antagonistic behavior was found in male-male and female-male pairs. The pursuit strategy the bat uses to track another bat is different from the strategy it uses to capture flying insects. This thesis confirms that the big brown bat's echolocation and flight behaviors are highly adaptable and describes several strategies the bat employs to cope with changes in sound localization cues and conspecific interference

Temporal coding and auditory processing in the prothoracic ganglion of crickets

We used the auditory system of crickets as a model system to examine the importance of temporal coding in sensory processing. The bilaterally paired Ascending Neurons 1 and 2 (AN1 and AN2) of crickets receive inputs from the auditory receptors on one side and carry the information to the brain. We used stimuli with either conspecific-like or predator-like (i.e. bats) carrier frequency to quantify the accuracy with which the interneurons code the information contained within the amplitude modulation (AM) envelope of the stimulus. AN1, which is tuned to the dominant carrier frequency of cricket songs, selectively codes the limited range of amplitude-modulation frequencies that occur in these signals. AN2, which is most sensitive to ultrasound, serves as a "bat-detector" and codes a broader range of AM frequencies, as occur in bat calls.A striking characteristic in AN2's responses to ultrasound is the presence of bursts of high-frequency spiking separated by relatively sparse spikes. We examined the relative importance of isolated spikes and bursts in the processing of ultrasound. We showed that bursts reliably signal the occurrence of salient amplitude increases. Furthermore, we showed that burst, but not isolated spikes, reliably predict behavioural responses. We suggest AN2 encodes behaviourally important information with bursts.The Omega Neuron 1 (ON1) responds to conspecific signals and to the ultrasonic echolocation sounds. ON1's temporal coding properties vary with carrier frequency, allowing it to encode both of these behaviourally important signals. Furthermore, the temporal coding properties of ON1 in response to cricket-like sound and bat-like sound match those of AN1 and AN2 respectively.ON1 is a source of contralateral inhibition to AN1 and AN2, enhancing binaural contrast and facilitating sound localization. We used dichotic stimulation to examine the importance of the temporal structure of contralateral inhibition for enhancing binaural contrast. Contralateral inhibition degrades the accuracy with which amplitude modulation is encoded by AN 1 and AN2, but only if the temporal pattern of inhibitory input matches that of excitation. Our results show that the CF-specific coding properties of ON1 allow this single neuron to enhance localization cues most effectively for both cricket-like and bat-like acoustic signals

Responses of a Locust Looming Sensitive Neuron, Flight Muscle Activity and Body Orientation to Changes in Object Trajectory, Background Complexity, and Flight Condition

Survival is one of the highest priorities of any animal. Interaction in the environment with conspecifics, predators, or objects, is driven by evolution of systems that can efficiently and rapidly respond to potential collision with these stimuli. Flight introduces further complexity for a collision avoidance system, requiring an animal to compute air speed, wind speed, ground speed, as well as transverse and longitudinal image flow, all within the context of detecting an approaching object. Understanding the mechanisms underlying neural control and coordination of motor systems to produce behaviours in response to the natural environment is a main goal of neuroethology. Locusts have a tractable nervous system, and a robust, reproducible collision avoidance response to looming stimuli. This tractable system allows recording from the nerve cord and flight muscles with precision and reliability, allowing us to answer important questions regarding the neuronal control of muscle coordination and, in turn, collision avoidance behaviour during flight. In flight, a collision avoidance behaviour will most often be a turn away from the approaching stimulus. I tested the hypothesis that during loosely tethered flight, synchrony between flight muscles increases just prior to the initiation of a turn and that muscle synchronization would correlate with body orientation changes during flight steering. I found that hind and forewing flight muscle synchronization events correlated strongly with forewing flight muscle latency changes, and to pitch and roll body orientation changes in response to a lateral looming visual stimulus. These findings led me to investigate further the role of the looming-sensitive descending contralateral movement detector (DCMD) neuron in flight muscle coordination and the initiation of forewing asymmetry in rigidly tethered locusts that generate a flight-like rhythm. By conducting simultaneous recordings from the nerve cord, forewing flight muscles, and visually recording the wing positions within the same flying animal, I hypothesized that DCMD burst properties would correlate with flight muscle activity changes and the initiation of wing asymmetry associated with turning behaviour. Furthermore, I accessed the effect of manipulating background complexity of the locust’s visual environment, looming object trajectory, and the putative effect of mechanosensory feedback during flight, on DCMD burst firing rate properties. DCMD burst properties were affected by changes in background complexity and object trajectory, and most interestingly during flight. This suggests that reafferent feedback from the flight motor system modulates the DCMD signal, and therefore represents a more naturalistic representation of collision avoidance behaviour. A pivotal discovery in my study was the temporal role of bursting in collision avoidance behaviour. I found that the first burst in a DCMD spike train represents the earliest detectable neuronal event correlated with muscle activity changes and the creation of wing asymmetry. I found strong correlations across all object trajectories and background complexities, between the timing of the first bursts, flight muscle activity changes and the initiation of wing asymmetry. These findings reinforce the importance of the temporal properties of DCMD bursting in collision avoidance behaviour