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.
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Neural Response Selectivity to Natural Sounds in the Bat Midbrain
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.
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- Award ID(s):
- 1734744
- NSF-PAR ID:
- 10172430
- Date Published:
- Journal Name:
- Neuroscience
- Volume:
- 434
- Issue:
- May
- ISSN:
- 0735-2743
- Page Range / eLocation ID:
- 200-211
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Most bat species have highly developed audio-vocal systems, which allow them to adjust the features of echolocation calls that are optimized for different sonar tasks, such as detecting, localizing, discriminating and tracking targets. Furthermore, bats can also produce a wide array of social calls to communicate with conspecifics. The acoustic properties of some social calls differ only subtly from echolocation calls, yet bats have the ability to distinguish them and reliably produce appropriate behavioral responses. Little is known about the underlying neural processes that enable the correct classification of bat social communication sounds. One approach to this question is to identify the brain regions that are involved in the processing of sounds that carry behavioral relevance. Here, we present preliminary data on neuronal activation, as measured by c-fos expression, in big brown bats (Eptesicus fuscus) exposed to either social calls, echolocation calls or kept in silence. We focused our investigation on five relevant brain areas; three within the canonical auditory pathway (auditory cortex, inferior colliculus and medial geniculate body) and two that are involved in the processing of emotive stimulus content (amygdala and nucleus accumbens). In this manuscript we report c-fos staining of the areas of interest after exposure to conspecific calls. We discuss future work designed to overcome experimental limitations and explore whether c-fos staining reveals anatomical segregation of neurons activated by echolocation and social call call categories.more » « less
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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.more » « less
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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.more » « less
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Abstract Sensory systems perform fitness‐relevant functions, and specialized sensory structures allow organisms to accomplish challenging tasks. However, broad comparative analyses of sensory morphologies and their performance are lacking for diverse mammalian radiations.
Neotropical leaf‐nosed bats (Phyllostomidae) are one of the most ecologically diverse mammal groups; including a wide range of diets and foraging behaviours, and extreme morphological variation in external sensory structures used in echolocation (nose leaf and pinnae).
We coupled 3D geometric morphometrics and acoustic field recordings under a phylogenetic framework to investigate the mechanisms underlying the diversification of external sensory morphologies in phyllostomids, and explored the potential implications of sensory morphological diversity to functional outputs and dietary ecology.
We found that the nose leaf consists of two evolutionary modules—spear and horseshoe—suggesting that modularity enabled morphological and functional diversification of this structure.
We found a significant association between some aspects of nose leaf shape and maximum frequency and bandwidth of echolocation calls, but not between pinnae shape and echolocation call parameters. This may be explained by the use of multiple sensory modes across phyllostomids and plasticity of some echolocation call parameters.
Species with different diets significantly differed in nose leaf shape, specifically in spear breadth, presence of a midrib, and cupping and anterior rotation of the horseshoe. This may relate to different levels of prey type specificity within each diet. Pinnae shape significantly differed between species that consume non‐mobile, non‐evasive prey (broad rounded, cupped pinnae) and mobile, evasive prey (flattened pinnae with a sharp tapering apex). This may reflect the use of different sound cues to detect prey.
Our results give insight into the morphological evolution of external sensory structures in bats, and highlight new links between morphological diversity and ecology.
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1016/j.neuroscience.2019.11.047
