Background: The mammalian auditory cortex can be subdivided into various fields characterized by neurophysiological and neuroarchitectural properties and by connections with different nuclei of the thalamus. Besides the primary auditory cortex, echolocating bats have cortical fields for the processing of temporal and spectral features of the echolocation pulses. This paper reports on location, neuroarchitecture and basic functional organization of the auditory cortex of the microchiropteran bat Phyllostomus discolor (family: Phyllostomidae).
Many organisms coordinate rhythmic motor actions with those of a partner to generate cooperative social behavior such as duet singing. The neural mechanisms that enable rhythmic interindividual coordination of motor actions are unknown. Here we investigate the neural basis of vocal duetting behavior by using an approach that enables simultaneous recordings of individual vocalizations and multiunit vocal premotor activity in songbird pairs ranging freely in their natural habitat. We find that in the duet-initiating bird, the onset of the partner’s contribution to the duet triggers a change in rhythm in the periodic neural discharges that are exclusively locked to the initiating bird’s own vocalizations. The resulting interindividually synchronized neural activity pattern elicits vocalizations that perfectly alternate between partners in the ongoing song. We suggest that rhythmic cooperative behavior requires exact interindividual coordination of premotor neural activity, which might be achieved by integration of sensory information originating from the interacting partner.
Bats quickly navigate through a highly structured environment relying on echolocation. Large natural objects in the environment, like bushes or trees, produce complex stochastic echoes, which can be characterized by the echo roughness. Previous work has shown that bats can use echo roughness to classify the stochastic properties of natural objects. This study provides both psychophysical and electrophysiological data to identify a neural correlate of statistical echo analysis in the bat Phyllostomus discolor. Psychophysical results show that the bats require a fixed minimum roughness of 2.5 (in units of base 10 logarithm of the stimulus fourth moment) for roughness discrimination. Electrophysiological results reveal a subpopulation of 15 of 94 recorded cortical units, located in an anterior region of auditory cortex, whose rate responses changed significantly with echo roughness. It is shown that the behavioral ability to discriminate differences in the statistics of complex echoes can be quantitatively predicted by the neural responses of this subpopulation of auditorycortical neurons.
Navigating on the wing in complete darkness is a challenging task for echolocating bats. It requires the detailed analysis of spatial and temporal information gained through echolocation. Thus neural encoding of spatiotemporal echo information is a major function in the bat auditory system. In this study we presented echoes in virtual acoustic space and used a reverse-correlation technique to investigate the spatiotemporal response characteristics of units in the inferior colliculus (IC) and the auditory cortex (AC) of the bat Phyllostomus discolor. Spatiotemporal response maps (STRMs) of IC units revealed an organization of suppressive and excitatory regions that provided pronounced contrast enhancement along both the time and azimuth axes. Most IC units showed either spatially centralized short-latency excitation spatiotemporally imbedded in strong suppression, or the opposite, i.e., central short-latency suppression imbedded in excitation. This complementary arrangement of excitation and suppression was very rarely seen in AC units. In contrast, STRMs in the AC revealed much less suppression, sharper spatiotemporal tuning, and often a special spatiotemporal arrangement of two excitatory regions. Temporal separation of excitatory regions ranged up to 25 ms and was thus in the range of temporal delays occurring in target ranging in bats in a natural situation. Our data indicate that spatiotemporal processing of echo information in the bat auditory midbrain and cortex serves very different purposes: Whereas the spatiotemporal contrast enhancement provided by the IC contributes to echo-feature extraction, the AC reflects the result of this processing in terms of a high selectivity and task-oriented recombination of the extracted features.
As opposed to visual imaging, biosonar imaging of spatial object properties represents a challenge for the auditory system because its sensory epithelium is not arranged along space axes. For echolocating bats, object width is encoded by the amplitude of its echo (echo intensity) but also by the naturally covarying spread of angles of incidence from which the echoes impinge on the bat's ears (sonar aperture). It is unclear whether bats use the echo intensity and/or the sonar aperture to estimate an object's width. We addressed this question in a combined psychophysical and electrophysiological approach. In three virtual-object playback experiments, bats of the species Phyllostomus discolor had to discriminate simple reflections of their own echolocation calls differing in echo intensity, sonar aperture, or both. Discrimination performance for objects with physically correct covariation of sonar aperture and echo intensity ("object width") did not differ from discrimination performances when only the sonar aperture was varied. Thus, the bats were able to detect changes in object width in the absence of intensity cues. The psychophysical results are reflected in the responses of a population of units in the auditory midbrain and cortex that responded strongest to echoes from objects with a specific sonar aperture, regardless of variations in echo intensity. Neurometric functions obtained from cortical units encoding the sonar aperture are sufficient to explain the behavioral performance of the bats. These current data show that the sonar aperture is a behaviorally relevant and reliably encoded cue for object size in bat sonar.
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