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Little is known about the neural mechanisms that mediate differential action–selection responses to communication and echolocation calls in bats. For example, in the big brown bat, frequency modulated (FM) food-claiming communication calls closely resemble FM echolocation calls, which guide social and orienting behaviors, respectively. Using advanced signal processing methods, we identified fine differences in temporal structure of these natural sounds that appear key to auditory discrimination and behavioral decisions. We recorded extracellular potentials from single neurons in the midbrain inferior colliculus (IC) of passively listening animals, and compared responses to playbacks of acoustic signals used by bats for social communication and echolocation. We combined information obtained from spike number and spike triggered averages (STA) to reveal a robust classification of neuron selectivity for communication or echolocation calls. These data highlight the importance of temporal acoustic structure for differentiating echolocation and food-claiming social calls and point to general mechanisms of natural sound processing across species. 

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. 

Echolocating bats must process temporal streams of sonar sounds to represent objects along the range axis. Neuronal echo-delay tuning, the putative mechanism of sonar ranging, has been characterized in the inferior colliculus (IC) of the mustached bat, an insectivorous species that produces echolocation calls consisting of constant frequency and frequency modulated (FM) components, but not in species that use FM signals alone. This raises questions about the mechanisms that give rise to echo-delay tuning in insectivorous bats that use different signal designs. To investigate whether stimulus context may account for species differences in echo-delay selectivity, we characterized single-unit responses in the IC of awake passively listening FM bats, Eptesicus fuscus, to broadcasts of natural sonar call-echo sequences, which contained dynamic changes in signal duration, interval, spectrotemporal structure, and echo-delay. In E. fuscus, neural selectivity to call-echo delay emerges in a population of IC neurons when stimulated with call-echo pairs presented at intervals mimicking those in a natural sonar sequence. To determine whether echo-delay selectivity also depends on the spectrotemporal features of individual sounds within natural sonar sequences, we studied responses to computer-generated echolocation signals that controlled for call interval, duration, bandwidth, sweep rate, and echo-delay. A subpopulation of IC neurons responded selectively to the combination of the spectrotemporal structure of natural call-echo pairs and their temporal patterning within a dynamic sonar sequence. These new findings suggest that the FM bat’s fine control over biosonar signal parameters may modulate IC neuronal selectivity to the dimension of echo-delay. 

Temporal analysis of sound is fundamental to auditory processing throughout the animal kingdom. Echolocating bats are powerful models for investigating the underlying mechanisms of auditory temporal processing, as they show microsecond precision in discriminating the timing of acoustic events. However, the neural basis for microsecond auditory discrimination in bats has eluded researchers for decades. Combining extracellular recordings in the midbrain inferior colliculus (IC) and mathematical modeling, we show that microsecond precision in registering stimulus events emerges from synchronous neural firing, revealed through low-latency variability of stimulus-evoked extracellular field potentials (EFPs, 200–600 Hz). The temporal precision of the EFP increases with the number of neurons firing in synchrony. Moreover, there is a functional relationship between the temporal precision of the EFP and the spectrotemporal features of the echolocation calls. In addition, EFP can measure the time difference of simulated echolocation call–echo pairs with microsecond precision. We propose that synchronous firing of populations of neurons operates in diverse species to support temporal analysis for auditory localization and complex sound processing.