Spatially clustered neurons encode vocalization categories in the bat midbrain.

Rapid categorization of vocalizations enables adaptive behavior across species. While categorical perception is thought to arise in the neocortex, humans and other animals could benefit from functional organization of ethologically-relevant sounds at earlier stages in the auditory hierarchy. Here, we developed two-photon calcium imaging in the awake echolocating bat () to study encoding of sound meaning in the Inferior Colliculus, which is as few as two synapses from the inner ear.

Neural coding of 3D spatial location, orientation, and action selection in echolocating bats.

Echolocating bats are among the only mammals capable of powered flight, and they rely on active sensing to find food and steer around obstacles in 3D environments. These natural behaviors depend on neural circuits that support 3D auditory localization, audio-motor integration, navigation, and flight control, which are modulated by spatial attention and action selection.

Spatial attention in natural tasks [version 1; peer review: 2 approved with reservations].

Little is known about fine scale neural dynamics that accompany rapid shifts in spatial attention in freely behaving animals, primarily because reliable indicators of attention are lacking in standard model organisms engaged in natural tasks. The echolocating bat can serve to bridge this gap, as it exhibits robust dynamic behavioral indicators of overt spatial attention as it explores its environment. In particular, the bat actively shifts the aim of its sonar beam to inspect objects in different directions, akin to eye movements and foveation in humans and other visually dominant animals.

Active head rolls enhance sonar-based auditory localization performance.

Animals utilize a variety of active sensing mechanisms to perceive the world around them. Echolocating bats are an excellent model for the study of active auditory localization. The big brown bat (Eptesicus fuscus), for instance, employs active head roll movements during sonar prey tracking.

Echolocating bats inspect and discriminate landmark features to guide navigation.

Landmark-guided navigation is a common behavioral strategy for way-finding, yet prior studies have not examined how animals collect sensory information to discriminate landmark features. We investigated this question in animals that rely on active sensing to guide navigation. Four echolocating bats () were trained to use an acoustic landmark to find and navigate through a net opening for a food reward.

3D Hippocampal Place Field Dynamics in Free-Flying Echolocating Bats.

A large body of laboratory research has investigated the process by which environmental cues are acquired and used for spatial navigation in rodents; however, the key to differentiating between species specializations and general principles lies in comparative research. Rodent research has focused on a class of neurons in the hippocampus implicated in the representation of space - termed place cells - and the process by which these representations form. One class of models of hippocampal place field formation depends on continuous theta, a low frequency brain oscillation that is prevalent in crawling rodents.

Adaptive sonar call timing supports target tracking in echolocating bats.

Echolocating bats dynamically adapt the features of their sonar calls as they approach obstacles and track targets. As insectivorous bats forage, they increase sonar call rate with decreasing prey distance, and often embedded in bat insect approach sequences are clusters of sonar sounds, termed sonar sound groups (SSGs). The bat's production of SSGs has been observed in both field and laboratory conditions, and is hypothesized to sharpen spatiotemporal sonar resolution.

Active acoustic interference elicits echolocation changes in heterospecific bats.

Echolocating bats often forage in the presence of both conspecific and heterospecific individuals, which have the potential to produce acoustic interference. Recent studies have shown that at least one bat species, the Brazilian free-tailed bat (), produces specialized social signals that disrupt the sonar of conspecific competitors. We herein discuss the differences between passive and active jamming signals and test whether heterospecific jamming occurs in species overlapping spatiotemporally, as well as whether such interference elicits a jamming avoidance response.

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

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.

Functional Organization and Dynamic Activity in the Superior Colliculus of the Echolocating Bat, .

Sensory-guided behaviors require the transformation of sensory information into task-specific motor commands. Prior research on sensorimotor integration has emphasized visuomotor processes in the context of simplified orienting movements in controlled laboratory tasks rather than an animal's more complete, natural behavioral repertoire. Here, we conducted a series of neural recording experiments in the midbrain superior colliculus (SC) of echolocating bats engaged in a sonar target-tracking task that invoked dynamic active sensing behaviors.

Action Enhances Acoustic Cues for 3-D Target Localization by Echolocating Bats.

Under natural conditions, animals encounter a barrage of sensory information from which they must select and interpret biologically relevant signals. Active sensing can facilitate this process by engaging motor systems in the sampling of sensory information. The echolocating bat serves as an excellent model to investigate the coupling between action and sensing because it adaptively controls both the acoustic signals used to probe the environment and movements to receive echoes at the auditory periphery.

Three-dimensional auditory localization in the echolocating bat.

Echolocating bats exhibit accurate three-dimensional (3D) auditory localization to avoid obstacles and intercept prey. The bat achieves high spatial resolution through a biological sonar system. Key features of the bat's sonar system are (1) high frequency, directional echolocation signals; (2) high frequency hearing; (3) mobile ears; and (4) measurement of distance from the time delay between sonar emission and echo reception.

Midbrain auditory selectivity to natural sounds.

This study investigated auditory stimulus selectivity in the midbrain superior colliculus (SC) of the echolocating bat, an animal that relies on hearing to guide its orienting behaviors. Multichannel, single-unit recordings were taken across laminae of the midbrain SC of the awake, passively listening big brown bat, Eptesicus fuscus. Species-specific frequency-modulated (FM) echolocation sound sequences with dynamic spectrotemporal features served as acoustic stimuli along with artificial sound sequences matched in bandwidth, amplitude, and duration but differing in spectrotemporal structure.

Timing matters: sonar call groups facilitate target localization in bats.

To successfully negotiate a cluttered environment, an echolocating bat must control the timing of motor behaviors in response to dynamic sensory information. Here we detail the big brown bat's adaptive temporal control over sonar call production for tracking prey, moving predictably or unpredictably, under different experimental conditions. We studied the adaptive control of vocal-motor behaviors in free-flying big brown bats, Eptesicus fuscus, as they captured tethered and free-flying insects, in open and cluttered environments.

Linked control of syllable sequence and phonology in birdsong.

The control of sequenced behaviors, including human speech, requires that the brain coordinate the production of discrete motor elements with their concatenation into complex patterns. In birdsong, another sequential vocal behavior, the acoustic structure (phonology) of individual song elements, or "syllables," must be coordinated with the sequencing of syllables into a song. However, it is unknown whether syllable phonology is independent of the sequence in which a syllable is produced.

Central contributions to acoustic variation in birdsong.

Birdsong is a learned behavior remarkable for its high degree of stereotypy. Nevertheless, adult birds display substantial rendition-by-rendition variation in the structure of individual song elements or "syllables." Previous work suggests that some of this variation is actively generated by the avian basal ganglia circuitry for purposes of motor exploration.

Bypassing V1: a direct geniculate input to area MT.

Thalamic nuclei are thought to funnel sensory information to the brain's primary cortical areas, which in turn transmit signals afresh to higher cortical areas. Here we describe a direct projection in the macaque monkey from the lateral geniculate nucleus (LGN) to the motion-selective middle temporal area (MTor V5), a cortical area not previously considered 'primary'. The constituent neurons are mostly koniocellular, send virtually no collateral axons to primary visual cortex (V1) and equal about 10% of the V1 population innervating MT.