During hunting, duration selectivity and recovery cycle underlie a bat's ability to determine echo duration and target distance (echo ranging). This study shows that the recovery cycle of most duration-selective neurons in the bat central nucleus of the inferior colliculus neurons varies with biologically relevant pulse-echo (P-E) duration and amplitude. As such, neurons with short best duration recover rapidly when stimulated with P-E pairs with short duration and small P-E amplitude difference, whereas neurons with long best duration recover rapidly when stimulated with P-E pairs with long duration and large P-E amplitude difference. These data indicate that different groups of duration-selective neurons underlie the bat's ability to effectively perform echo recognition and ranging during different phases of hunting.
The present study examines duration-sensitive neurons in the inferior colliculus (IC) of the least horseshoe bat, Rhinolophus pusillus, from China. In contrast to other bat species tested for duration selectivity so far, echolocation pulses emitted by horseshoe bats are generally longer and composed of a long constant-frequency (CF) component followed by a short downward frequency-modulated (FM) sweep (CF-FM pulse). We used combined CF-FM pulses to analyze the differential effects that these two pulse components had on the duration tuning in neurons of the horseshoe bat's IC. Consistent with results from other mammals, duration-sensitive neurons found in the least horseshoe bat fall into three main classes: short-pass, band-pass, and long-pass. Using a CF stimulus alone, 54% (51/95) of all IC neurons showed at least one form of duration selectivity at one or more stimulus intensities. In 65 of the 95 IC neurons tested with CF pulses, we were also able to test their duration selectivity for a combined CF-FM pulse, which increased the ratio of duration-sensitive neurons to 66% (43/65). Seven to 15 neurons that failed to show duration tuning for CF bursts became duration sensitive for CF-FM pulses, with most of them exhibiting short-pass (depending on stimulus intensity, between 4 and 8 neurons) or band-pass tuning (1-3 neurons). Increasing stimulus intensities did not affect the duration tuning in 53% (23/43) of duration-sensitive neurons for CF bursts and in about 26% (7/27) for CF-FM stimuli. In the remaining neurons, increasing sound levels generally reduced the ratio of duration-sensitive neurons to 33% for CF and 37% for CF-FM stimulation. In those that remained duration sensitive, louder CF bursts shortened best durations in band-pass neurons and cutoff durations in short- and long-pass neurons, whereas louder CF-FM stimuli reduced the cutoff durations only in short-pass neurons. Bandwidths of band-pass neurons were not significantly affected by any stimulus configuration, with only a slight trend for increasing bandwidths for louder CF bursts (but not CF-FM stimuli). Best durations and cutoff durations reached higher values than those in the other bat species examined so far and roughly match the longer durations of echolocation pulses emitted by horseshoe bats. Therefore presentation of a CF-FM stimulus improved the duration sensitivity in IC neurons by increasing the ratio of duration-tuned neurons and making them less susceptible to changes in signal intensity.
In central auditory signal processing, neural inhibition plays an important role in sharpening the selectivity of auditory neurons. The present study examines the involvement of GABA-mediated inhibition in shaping the frequency selectivity of neurons in the bat inferior colliculus (IC) using forward masking paradigm and bicuculline application. At each study session, we recorded two IC neurons with a pair of electrodes and reciprocally studied whether a sound that served as a probe to elicit response of one neuron might serve as a masker to affect the frequency tuning curve (FTC) of the other paired neuron. Among the 33 pairs of IC neurons recorded, this forward masking paradigm produces sharpening of the FTC in 29 (88%) pairs of IC neurons and broadening of the FTC in 4 (12%) pairs of IC neurons. The degree of sharpening of FTC decreases with recording depth as well as with the difference in the best frequency and recording depth between each pair of IC neurons. Although bicuculline application broadens the FTC of all IC neurons, forward masking still produces sharpening of the FTC in most IC neurons. These data suggest that population of IC neurons are highly correlated during frequency analysis such that frequency selectivity of some groups of IC neurons is improved through inhibition while the spectrum of frequency sensitivity of other groups of IC neurons is enhanced through excitation. Biological significance of these data relevant to acoustic signal processing is discussed.
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