Zoltan M. Fuzessery

Sound duration selectivity in the pallid bat inferior colliculus.

Neurons selective for sound duration have been reported in the auditory midbrain and cortex of several specialized vertebrate species that process behaviorally relevant signals of stereotypic duration. This study examines duration selectivity in the inferior colliculus (IC) of the pallid bat to determine if this selectivity is limited to regions that serve echolocation, or if it extends to low-frequency regions that serve passive listening. It also focuses on the temporal response properties of duration-selective neurons to elucidate mechanisms that may underlie the creation of this selectivity. Of 140 neurons tested, 36% were selective for short durations of </=7 ms, and acted as short-pass or bandpass duration filters. Sixteen percent, termed long duration neurons, differed in that they required minimum sound durations of 5-50 ms before responding, and all acted as long-pass duration filters. Short duration neurons were equally common in the high-frequency region serving echolocation and the lateral low-frequency region that serves passive listening, indicating that selectivity for short duration sounds was not associated only with the specialized function of echolocation. Long duration neurons were most common in the medial low-frequency region IC. Selectivity for short and long duration sounds was therefore not uniformly distributed across the IC. Analyses of the temporal response properties of short duration neurons, and the application of bicuculline to block gamma-aminobutyric acid-A receptors, were used to infer the synaptic interactions that underlie the creation of duration selectivity, the role of inhibition in its creation, and whether a coincidence mechanism proposed by Casseday et al. (Science 264 (1994) 847-850) is consistent with the behavior of the duration-selective neurons recorded in the pallid bat IC. Present results suggest that while some neurons do behave in a manner that is consistent with the coincidence mechanism, the behaviors of others suggest that more than one mechanism may create a selectivity for short duration sounds.

Passive sound localization of prey by the pallid bat (Antrozous p. pallidus)

SummaryThe pallid bat (Antrozous p. pallidus) uses passive sound localization to capture terrestrial prey. This study of captive pallid bats examined the roles of echolocation and passive sound localization in prey capture, and focused on their spectral requirements for accurate passive sound localization.Crickets were used as prey throughout these studies. All tests were conducted in dim, red light in an effort to preclude the use of vision. Hunting performance did not differ significantly in red light and total darkness, nor did it differ when visual contrast between the terrestrial prey and the substrate was varied, demonstrating that the bats did not use vision to locate prey.Our bats apparently used echolocation for general orientation, but not to locate prey. They did not increase their pulse emission rate prior to prey capture, suggesting that they were not actively scanning prey. Instead, they required prey-generated sounds for localization. The bats attended to the sound of walking crickets for localization, and also attacked small, inanimate objects dragged across the floor. Stationary and/or anesthetized crickets were ignored, as were crickets walking on substrates that greatly attenuated walking sounds. Cricket communication sounds were not used in prey localization; the bats never captured stationary, calling crickets.The accuracy of their passive sound localization was tested with an open-loop passive sound localization task that required them to land upon an anesthetized cricket tossed on the floor. The impact of a cricket produced a single 10–20 ms duration sound, yet with this information, the bats were able to land within 7.6 cm of the cricket from a maximum distance of 4.9 m. This performance suggests a sound localization accuracy of approximately ±1° in the horizontal and vertical dimensions of auditory space. The lower frequency limit for accurate sound localization was between 3–8 kHz. A physiological survey of frequency representation in the pallid bat inferior colliculus suggests that this lower frequency limit is around 5 kHz.

Monaural and binaural spectral cues created by the external ears of the pallid bat

The acoustic properties of external ears transform the spectra of incident sound in a location-dependent manner, and provide monaural and binaural spectral information used in 2-dimensional localization. Human studies suggest that binaural spectral differences, and spectral peaks and notches in monaural transfer functions, may all provide spatial information. This study examined the acoustic properties of the pallid bat ear to determine directionality, interaural intensity differences spectral peaks and notches in transfer functions, as well as acoustic gain. The pallid bat is a gleaning bat that uses passive sound localization to find prey, and echolocation for general orientation. It is capable of very accurate passive sound localization, and the primary focus of this study was to determine the spectral cues that might support this localization acuity. Results show that the external ears of this bat create spectral maxima and minima that vary systematically with azimuth and elevation. The monaural spectral cues resemble those reported in humans and cats and suggest that similar spectral cues are used across taxa. The ears also create robust interaural spectral differences that vary systematically with both sound azimuth and elevation. These monaural and binaural spectral cues may provide the basis for the 1 degrees angular resolution apparent in it this bats passive sound localization performance.

Can two streams of auditory information be processed simultaneously? Evidence from the gleaning bat Antrozous pallidus.

A tenet of auditory scene analysis is that we can fully process only one stream of auditory information at a time. We tested this assumption in a gleaning bat, the pallid bat (Antrozous pallidus) because this bat uses echolocation for general orientation, and relies heavily on prey-generated sounds to detect and locate its prey. It may therefore encounter situations in which the echolocation and passive listening streams temporally overlap. Pallid bats were trained to a dual task in which they had to negotiate a wire array, using echolocation, and land on one of 15 speakers emitting a brief noise burst in order to obtain a food reward. They were forced to process both streams within a narrow 300 to 500 ms time window by having the noise burst triggered by the bats’ initial echolocation pulses as it approached the wire array. Relative to single task controls, echolocation and passive sound localization performance was slightly, but significantly, degraded. The bats also increased echolocation interpulse intervals during the dual task, as though attempting to reduce temporal overlap between the signals. These results suggest that the bats, like humans, have difficulty in processing more than one stream of information at a time.

GABA Shapes Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Auditory Cortex

In the pallid bat auditory cortex and inferior colliculus (IC), the majority of neurons tuned in the echolocation range is selective for the direction and rate of frequency-modulated (FM) sweeps used in echolocation. Such selectivity is shaped mainly by spectrotemporal asymmetries in sideband inhibition. An early-arriving, low-frequency inhibition (LFI) shapes direction selectivity. A delayed, high-frequency inhibition (HFI) shapes rate selectivity for downward sweeps. Using iontophoretic blockade of GABAa receptors, we show that cortical FM sweep selectivity is at least partially shaped locally. GABAa receptor antagonists, bicuculline or gabazine, reduced or eliminated direction and rate selectivity in approximately 50% of neurons. Intracortical GABA shapes FM sweep selectivity by either creating the underlying sideband inhibition or by advancing the arrival time of inhibition relative to excitation. Given that FM sweep selectivity and asymmetries in sideband inhibition are already present in the IC, these data suggest a refinement or recreation of similar response properties at the cortical level.

Facilitatory Mechanisms Underlying Selectivity for the Direction and Rate of Frequency Modulated Sweeps in the Auditory Cortex

Neurons selective for frequency modulated (FM) sweeps are common in auditory systems across different vertebrate groups and may underlie representation of species-specific vocalizations. Studies on mechanisms of FM sweep selectivity have primarily focused on sideband inhibition. Here, we present the first evidence for facilitatory mechanisms of FM sweep selectivity. Facilitatory interactions were found in 46 of 264 (17%) neurons tuned in the echolocation range (25–60 kHz) in the auditory cortex of the pallid bat. These neurons respond poorly to individual tones but are facilitated by combinations of tones with specific spectral and temporal intervals. Facilitation neurons show remarkable sensitivity to sub-millisecond differences in time delays between the two tones. Interestingly, the range of delays eliciting facilitation is not fixed but varies systematically with frequency difference between the two tones. Properties of facilitation strongly predict selectivity for the direction and rate of FM sweeps. Together with previous studies, there appear to be at least three mechanisms underlying FM rate and direction selectivity: sideband inhibition, duration tuning, and facilitation. Interestingly, similar mechanisms underlie direction and velocity tuning in the visual system, suggesting the evolution of similar computations across sensory systems to process dynamic sensory stimuli.

Experience is required for the maintenance and refinement of FM sweep selectivity in the developing auditory cortex

Frequency modulated (FM) sweeps are common components of vocalizations, including human speech. How developmental experience shapes neuronal selectivity for these important signals is not well understood. Here, we show that altered developmental experience with FM sweeps used in echolocation by the pallid bat leads to either a loss of sideband inhibition or millisecond delays in the timing of inhibitory inputs, both of which lead to a reduction in rate and direction selectivity in auditory cortex. FM rate selectivity develops in an experience-independent manner, but requires experience for subsequent maintenance. Direction selectivity depends on experience for both development and maintenance. Rate and direction selectivity are affected by experience over different time periods during development. Altered inhibition may be a general mechanism of experience-dependent plasticity of selectivity for vocalizations.

Development of Inhibitory Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Auditory Cortex

Although it is known that neural selectivity for species-specific vocalizations changes during development, the mechanisms underlying such changes are not known. This study followed the development of mechanisms underlying selectivity for the direction and rate of frequency-modulated (FM) sweeps in the auditory cortex of the pallid bat, a species that uses downward FM sweeps to echolocate. In the adult cortex, direction and rate selectivity arise as a result of different spectral and temporal properties of low-frequency inhibition (LFI) and high-frequency inhibition (HFI). A narrow band of delayed HFI shapes rate selectivity for downward FM sweeps. A broader band of early LFI shapes direction selectivity. Here we asked whether these differences in LFI and HFI are present at the onset of hearing in the echolocation range or whether the differences develop slowly. We also studied how the development of properties of inhibitory frequencies influences FM rate and direction selectivity. We found that adult-like FM rate selectivity is present at 2 weeks after birth, whereas direction selectivity matures 12 weeks after birth. The different developmental time course for direction and rate selectivity is attributable to the differences in the development of LFI and HFI. Arrival time and bandwidth of HFI are adult-like at 2 weeks. Average arrival time of LFI gradually becomes faster and bandwidth becomes broader between 2 and 12 weeks. Thus, two properties of FM sweeps that are important for vocalization selectivity follow different developmental time courses attributable to the differences in the development of underlying inhibitory mechanisms.

Acute sensitivity to interaural time differences in the inferior colliculus of a bat that relies on passive sound localization

Gleaning bats rely on passive hearing to detect and localize terrestrial prey, and display remarkable accuracy in their passive sound localization. This study examines binaural processing in the inferior colliculus (IC) of the pallid bat (Antrozous pallidus), a gleaner that attends to prey-generated noise transients to locate prey. The primary focus is to determine whether neurons in its lateral IC, a region that appears dedicated to passive localization, possess a level of sensitivity to interaural time difference (ITD) sensitivity sufficient to indicate the use of ITDs in sound localization. Such a sensitivity was suspected because the pallid bat is capable of very accurate passive sound localization at the lower end of its audible range, where interaural intensity differences (IIDs) are small and may not provide sufficient spatial information. Because the pallid bats audible range is too high for neurons to phase-lock to carrier frequencies, neurons were tested with square-wave, amplitude-modulated tones and noise to determine their sensitivity to ITDs in the sound envelope. Their sensitivity to the bats behaviorally relevant ITD range of +/- 70 micros, and their low average interaural time/ intensity trading ratios (18 micros/dB) suggest that the pallid bat IC may have the greatest ITD sensitivity reported in a high-frequency mammalian auditory system.

Parallel thalamocortical pathways for echolocation and passive sound localization in a gleaning bat, Antrozous pallidus

We present evidence for parallel auditory thalamocortical pathways that serve two different behaviors. The pallid bat listens for prey‐generated noise (5–35 kHz) to localize prey, while reserving echolocation [downward frequency‐modulated (FM) sweeps, 60–30 kHz] for obstacle avoidance. Its auditory cortex contains a tonotopic map representing frequencies from 6 to 70 kHz. The high‐frequency (BF > 30 kHz) representation is dominated by FM sweep‐selective neurons, whereas most neurons tuned to lower frequencies prefer noise. Retrograde tracer injections into these physiologically distinct cortical regions revealed that the high‐frequency region receives input from the suprageniculate (SG) nucleus, but not the ventral division of the medial geniculate body (MGBv), in all experiments (n = 9). In contrast, the low‐frequency region receives tonotopically organized input from the MGBv in all experiments (n = 16). Labeling in the SG was observed in only two of these experiments. Both cortical regions also receive sparse inputs from medial (MGBm) and parts of the dorsal division (MGBd) outside the SG. These results show that the low‐ and high‐frequency regions of a single tonotopic map receive dominant inputs from different thalamic divisions. Within the low‐frequency region, most neurons are binaurally inhibited, and an orderly map of interaural intensity difference (IID) sensitivity is present. We show that the input to the IID map arises from topographically organized projections from the MGBv. As observed in other species, a frequency‐dependent organization is observed in the lateromedial direction in the MGBv. These data demonstrate that MGBv‐to‐auditory cortex connections are organized with respect to both frequency and binaural selectivity. J. Comp. Neurol. 500:322–338, 2007.