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1. Sensory error drives fine motor adjustment

   https://doi.org/10.1073/pnas.2201275119  

   Wang, H. (June 2022, Proceedings of the National Academy of Sciences of the United States of America)

   Fine audiovocal control is a hallmark of human speech production and depends on precisely coordinated muscle activity guided by sensory feedback. Little is known about shared audiovocal mechanisms between humans and other mammals. We hypothesized that real-time audiovocal control in bat echolocation uses the same computational principles as human speech. To test the prediction of this hypothesis, we applied state feedback control (SFC) theory to the analysis of call frequency adjustments in the echolocating bat, Hipposideros armiger. This model organism exhibits well-developed audiovocal control to sense its surroundings via echolocation. Our experimental paradigm was analogous to one implemented in human subjects. We measured the bats’ vocal responses to spectrally altered echolocation calls. Individual bats exhibited highly distinct patterns of vocal compensation to these altered calls. Our findings mirror typical observations of speech control in humans listening to spectrally altered speech. Using mathematical modeling, we determined that the same computational principles of SFC apply to bat echolocation and human speech, confirming the prediction of our hypothesis. 

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2. Echolocating bats accumulate information from acoustic snapshots to predict auditory object motion

   https://doi.org/10.1073/pnas.2011719117  

   Salles, Angeles; Diebold, Clarice Anna; Moss, Cynthia F. (November 2020, Proceedings of the National Academy of Sciences)

   Unlike other predators that use vision as their primary sensory system, bats compute the three-dimensional (3D) position of flying insects from discrete echo snapshots, which raises questions about the strategies they employ to track and intercept erratically moving prey from interrupted sensory information. Here, we devised an ethologically inspired behavioral paradigm to directly test the hypothesis that echolocating bats build internal prediction models from dynamic acoustic stimuli to anticipate the future location of moving auditory targets. We quantified the direction of the bat’s head/sonar beam aim and echolocation call rate as it tracked a target that moved across its sonar field and applied mathematical models to differentiate between nonpredictive and predictive tracking behaviors. We discovered that big brown bats accumulate information across echo sequences to anticipate an auditory target’s future position. Further, when a moving target is hidden from view by an occluder during a portion of its trajectory, the bat continues to track its position using an internal model of the target’s motion path. Our findings also reveal that the bat increases sonar call rate when its prediction of target trajectory is violated by a sudden change in target velocity. This shows that the bat rapidly adapts its sonar behavior to update internal models of auditory target trajectories, which would enable tracking of evasive prey. Collectively, these results demonstrate that the echolocating big brown bat integrates acoustic snapshots over time to build prediction models of a moving auditory target’s trajectory and enable prey capture under conditions of uncertainty. 

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3. Auditory Communication Processing in Bats: What We Know and Where to Go

   https://doi.org/http://dx.doi.org/10.1037/bne0000308  

   Salles, A.; Bohn, K.; Moss, C.F. (June 2019, Behavioral neuroscience)

   Bats are the second largest mammalian order, with over 1,300 species. These animals show diverse behaviors, diets, and habitats. Most bats produce ultrasonic vocalizations and perceive their environment by processing information carried by returning echoes of their calls. Echolocation is achieved through a sophisticated audio-vocal system that allows bats to emit and detect frequencies that can range from ten to hundreds of kilohertz. In addition, most bat species are gregarious, and produce social communication calls that vary in complexity, form, and function across species. In this article, we (a) highlight the value of bats as model species for research on social communication, (b) review behavioral and neurophysiological studies of bat acoustic communication signal production and processing, and (c) discuss important directions for future research in this field. We propose that comparative studies of bat acoustic communication can provide new insights into sound processing and vocal learning across the animal kingdom. 

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4. Echo interval and not echo intensity drives bat flight behavior in structured corridors

   https://doi.org/doi:10.1242/jeb.191155  

   Warnecke, M.; Macias, S.; Falk, B.; Moss, C.F. (October 2018, Journal of experimental biology)

   To navigate in the natural environment, animals must adapt their locomotion in response to environmental stimuli. The echolocating bat relies on auditory processing of echo returns to represent its surroundings. Recent studies have shown that echo flow patterns influence bat navigation, but the acoustic basis for flight path selection remains unknown. To investigate this problem, we released bats in a flight corridor with walls constructed of adjacent individual wooden poles, which returned cascades of echoes to the flying bat. We manipulated the spacing and echo strength of the poles comprising each corridor side, and predicted that bats would adapt their flight paths to deviate toward the corridor side returning weaker echo cascades. Our results show that the bat’s trajectory through the corridor was not affected by the intensity of echo cascades. Instead, bats deviated toward the corridor wall with more sparsely spaced, highly reflective poles, suggesting that pole spacing, rather than echo intensity, influenced bat flight path selection. This result motivated investigation of the neural processing of echo cascades. We measured local evoked auditory responses in the bat inferior colliculus to echo playback recordings from corridor walls constructed of sparsely and densely spaced poles. We predicted that evoked neural responses would be discretely modulated by temporally distinct echoes recorded from the sparsely spaced pole corridor wall, but not by echoes from the more densely spaced corridor wall. The data confirm this prediction and suggest that the bat’s temporal resolution of echo cascades may drive its flight behavior in the corridor. 

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5. Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat

   https://doi.org/DOI: https://doi.org/10.7554/eLife.29053  

   Kothari, N.B.; Wohlgemuth, M.J.; Moss, C.F. (April 2018, eLife)

   Essential to spatial orientation in the natural environment is a dynamic representation of direction and distance to objects. Despite the importance of 3D spatial localization to parse objects in the environment and to guide movement, most neurophysiological investigations of sensory mapping have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here, we show for the first time that sensory neurons in the midbrain superior colliculus (SC) of the free-flying echolocating bat encode 3D egocentric space, and that the bat’s inspection of objects in the physical environment sharpens tuning of single neurons, and shifts peak responses to represent closer distances. These findings emerged from wireless neural recordings in free-flying bats, in combination with an echo model that computes the animal’s instantaneous stimulus space. Our research reveals dynamic 3D space coding in a freely moving mammal engaged in a real-world navigation task. 

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