Echolocating bats show species-specific variation in susceptibility to acoustic forward masking.

Echolocating bats rely on precise auditory temporal processing to detect echoes generated by calls that may be emitted at rates reaching 150-200 Hz. High call rates can introduce forward masking perceptual effects that interfere with echo detection; however, bats may have evolved specializations to prevent repetition suppression of auditory responses and facilitate detection of sounds separated by brief intervals. Recovery of the auditory brainstem response (ABR) was assessed in two species that differ in the temporal characteristics of their echolocation behaviors: Eptesicus fuscus, which uses high call rates to capture prey, and Carollia perspicillata, which uses lower call rates to avoid obstacles and forage for fruit. We observed significant species differences in the effects of forward masking on ABR wave 1, in which E. fuscus maintained comparable ABR wave 1 amplitudes when stimulated at intervals of <3 ms, whereas post-stimulus recovery in C. perspicillata required 12 ms. When the intensity of the second stimulus was reduced by 20-30 dB relative to the first, however, C. perspicillata showed greater recovery of wave 1 amplitudes. The results demonstrate that species differences in temporal resolution are established at early levels of the auditory pathway and that these differences reflect auditory processing requirements of species-specific echolocation behaviors.

Ventral wing hairs provide tactile feedback for aerial prey capture in the big brown bat, Eptesicus fuscus.

Bats rely on their hand-wings to execute agile flight maneuvers, to grasp objects, and cradle young. Embedded in the dorsal and ventral membranes of bat wings are microscopic hairs. Past research findings implicate dorsal wing hairs in airflow sensing for flight control, but the function of ventral wing hairs has not been previously investigated. Here, we test the hypothesis that ventral wing hairs carry mechanosensory signals for flight control, prey capture, and handling. To test this hypothesis, we used synchronized high-speed stereo video and audio recordings to quantify flight and echolocation behaviors of big brown bats (Eptesicus fuscus) engaged in an aerial insect capture task. We analyzed prey-capture strategy and performance, along with flight kinematics, before and after depilation of microscopic hairs from the bat's ventral wing and tail membranes. We found that ventral wing hair depilation significantly impaired the bat's prey-capture performance. Interestingly, ventral wing hair depilation also produced increases in the bat's flight speed, an effect previously attributed exclusively to airflow sensing along the dorsal wing surface. These findings demonstrate that microscopic hairs embedded in the ventral wing and tail membranes of insectivorous bats provide mechanosensory feedback for prey handling and flight control.

Deafness in an auditory specialist, the big brown bat (Eptesicus fuscus).

Bats are long-lived animals that show presumed resistance to noise-induced and age-related hearing loss, which has been attributed to their dependence on sound processing for survival. Echolocation and basic auditory functions have been studied extensively in the big brown bat (Eptesicus fuscus), an insectivorous microchiropteran species. We conducted hearing tests and analysis of cochlear sensory cells in a group of big brown bats that exhibited anomalies in behavioral sonar tracking experiments and/or lacked neural responses to acoustic stimulation in subcortical auditory nuclei. We show for the first time the presence of profound deafness and extensive cochlear damage in an echolocating bat species. Auditory brainstem responses were abnormal or absent in these bats, and histological analyses of their cochleae revealed extensive loss of hair cells, supporting cells, and spiral ganglion neurons. The underlying cause of deafness is unknown.

Spatial tuning to virtual sounds in the inferior colliculus of the guinea pig.

How do neurons in the inferior colliculus (IC) encode the spatial location of sound? We have addressed this question using a virtual auditory environment. For this purpose, the individual head-related transfer functions (HRTFs) of 18 guinea pigs were measured under free-field conditions for 122 locations covering the upper hemisphere. From 257 neurons, 94% responded to the short (50-ms) white noise stimulus at 70 dB sound pressure level (SPL). Out of these neurons, 80% were spatially tuned with a receptive field that is smaller than a hemifield (at 70 dB). The remainder responded omnidirectionally or showed fractured receptive fields. The majority of the neurons preferred directions in the contralateral hemisphere. However, preference for front or rear positions and high elevations occurred frequently. For stimulation at 70 dB SPL, the average diameter of the receptive fields, based on half-maximal response, was less than a quarter of the upper hemisphere. Neurons that preferred frontal directions responded weakly or showed no response to posterior directions and vice versa. Hence, front/back discrimination is present at the single-neuron level in the IC. When nonindividual HRTFs were used to create the stimuli, the spatial receptive fields of most neurons became larger, split into several parts, changed position, or the response became omnidirectional. Variation of absolute sound intensity had little effect on the preferred directions of the neurons over a range of 20 to 40 dB above threshold. With increasing intensity, most receptive fields remained constant or expanded. Furthermore, we tested the influence of binaural decorrelation and stimulus bandwidth on spatial tuning. The vast majority of neurons with a low characteristic frequency (<2.5 kHz) lost spatial tuning under stimulation with binaurally uncorrelated noise, whereas high-frequency units were mostly unaffected. Most neurons that showed spatial tuning under broadband stimulation (white noise and 1 octave wide noise) turned omnidirectional when stimulated with 1/3 octave wide noise.

Representation of sound source direction in the superior colliculus of the guinea pig in a virtual auditory environment.

The deep layers of the superior colliculus (SC) receive visual, auditory, and somatosensory input. A major function of the SC is the control of orientation movements of the eye, head, and pinna. While a topographical map for sound source direction remains elusive in primary auditory structures of mammals, such a map for azimuthal sound source directions has been reported in the deep layers of the SC. Moreover, a gradient of elevation tuning has been also seen in the SC of ferrets and cats. Here we demonstrate that a virtual auditory environment can be used to reveal azimuthal and elevational topography for auditory spatial receptive fields in neurons in the SC of guinea pigs. Individual, head-related transfer functions (HRTF) were measured in ten guinea pigs for 122 directions in the upper hemispheric field and convolved with white noise. Many neurons (39%) in the deep layers showed robust responses to these virtual sounds, and the majority of these neurons had small spatial receptive fields that were restricted to the contralateral hemifield. Best directions varied from 0 degree to 135 degree azimuth along the contralateral side and from --10 degree to 60 degree elevation. Like previous studies using free-field stimulation, a gradient of best azimuth direction was found along the rostral-caudal axis, with rear directions represented caudally and front directions rostrally. The topographical organization for best elevations had not been studied previously in the guinea pig. We found that it roughly followed the mediolateral axis, with preference for high elevations represented medially and low elevations laterally. A similar organization using free-field stimulation has been reported in the ferret.