Evoked potential study of the inferior collicular response to constant frequency-frequency modulation (CF-FM) sounds in FM and CF-FM bats.

The auditory system of echolocating bats is adapted for processing species-specific ultrasonic signals. While FM (frequency modulation) bats are strictly sensitive to the frequency ranges of their orientation signals or prey-generated noise, CF-FM (constant frequency-FM) bats have a disproportionate number of neurons tuned to frequencies near the CF component of their orientation sounds, and most of them are on-off responders. Furthermore, the inferior collicular neurons of the CF-FM bats discharged as single-on or double-on responders to CF-FM stimuli. To further study the differences in auditory signal processing of these two types of bats, as the first step we conducted an evoked potential response study in the inferior colliculus of the CF-FM bat, Hipposideros pratti and the FM bat, Pipistrellus abramus using CF, FM and CF-FM stimuli. The results showed that the CF sounds always evoked collicular on- and off-responses in CF-FM bats, but the FM bats only had on-responses to both CF and FM sounds, indicting species-specific neural circuits. However, when stimulated with CF-FM sounds, collicular responses were evoked by both the CF and FM components from both FM and CF-FM bats, suggesting they have some generic neural circuit.

Comparisons of MRI images, and auditory-related and vocal-related protein expressions in the brain of echolocation bats and rodents.

Although echolocating bats and other mammals share the basic design of laryngeal apparatus for sound production and auditory system for sound reception, they have a specialized laryngeal mechanism for ultrasonic sound emissions as well as a highly developed auditory system for processing species-specific sounds. Because the sounds used by bats for echolocation and rodents for communication are quite different, there must be differences in the central nervous system devoted to producing and processing species-specific sounds between them. The present study examines the difference in the relative size of several brain structures and expression of auditory-related and vocal-related proteins in the central nervous system of echolocation bats and rodents. Here, we report that bats using constant frequency-frequency-modulated sounds (CF-FM bats) and FM bats for echolocation have a larger volume of midbrain nuclei (inferior and superior colliculi) and cerebellum relative to the size of the brain than rodents (mice and rats). However, the former have a smaller volume of the cerebrum and olfactory bulb, but greater expression of otoferlin and forkhead box protein P2 than the latter. Although the size of both midbrain colliculi is comparable in both CF-FM and FM bats, CF-FM bats have a larger cerebrum and greater expression of otoferlin and forkhead box protein P2 than FM bats. These differences in brain structure and protein expression are discussed in relation to their biologically relevant sounds and foraging behavior.

The cochlear size of bats and rodents derived from MRI images and histology.

From the evolutionary perspective, the ear of each animal species is built for effective processing of the biologically relevant signals used for communication and acoustically guided orientation. Because the sound pulses used by echolocating bats for orientation and rodents for communication are quite different, the basic design of the mammalian auditory system commonly shared by echolocating bats must be specialized in some manner to effectively process their species-specific sounds. The present study examines the difference in the cochlea of these animal species using MRI images and histological techniques. We report here that, although all these animal species share a similar cochlear structure, they vary in their cochlear size and turns. Bats using constant frequency-frequency-modulated pulses (CF-FM bats) and frequency-modulated pulses (FM bats) for echolocation have a larger cochlear size and more cochlear turns than rodents (mice and rats). However, CF-FM bats have the largest cochlear size and most cochlear turns. This difference in cochlear size and turns of these animal species is discussed in relation to their biologically relevant sounds and acoustic behavior.

Sexual dimorphism in echolocation pulse parameters of the CF-FM bat, Hipposideros pratti.

BACKGROUND: Previousstudies of sexual dimorphism in the echolocation pulses of the constant frequency-frequency modulating (CF-FM) bat have been mainly concentrated on the difference in the frequency of the CF component of the predominant second harmonic while neglected other pulse parameters. However, recent studies have shown that other pulse parameters of the predominant second harmonic are also biologically significant to the bat hunting. To complement and advance these studies, we have examined sexual dimorphism of multiple parameters (e.g., duration, frequency, bandwidth of the FM component, and repetition rate of emitted pulses) of the echolocation pulses of the CF-FM bat, Hipposideros pratti. RESULTS: Our studies of the predominant second harmonic show that on average the male bat has higher frequency of the CF component, wider FM bandwidth, and higher pulse repetition rate while the female bat has longer duration of the CF and FM components. CONCLUSIONS: Theseobservations suggest that bats may potentially use this sexual dimorphism in echolocation pulse parameters for social communication and species and sex identification.

The role of the FM component in shaping the number of impulses and response latency of inferior collicular neurons of Hipposideros armiger elicited by CF-FM sounds.

Previous studies show that when stimulated with constant frequency-frequency modulated (CF-FM) sounds, the inferior collicular neurons of the leaf-nosed bat, Hipposideros armiger, either discharge impulses only to the CF component (single-on, SO neurons) or to both CF and FM components (double-on, DO neurons). In this study, we specifically determine the role of the FM component in shaping the number of impulses and response latency of these two types of neurons in response to CF-FM sounds. Adding the FM component to the CF sounds significantly decreases the number of impulses of both SO and DO neurons but shortens the response latency of DO neurons in response to the CF component of the CF-FM sounds. The possible neural mechanisms underlying these seemingly paradoxical observations are briefly discussed based on our preliminary intracellular recording studies. Biological relevance of these findings in relation to different phases of bats' hunting is also discussed.

Local neuronal circuits that may shape the discharge patterns of inferior collicular neurons.

The discharge patterns of neurons in auditory centers encode information about sounds. However, few studies have focused on the synaptic mechanisms underlying the shaping of discharge patterns using intracellular recording techniques. Here, we investigated the discharge patterns of inferior collicular (IC) neurons using intracellular recordings to further elucidate the mechanisms underlying the shaping of discharge patterns. Under in vivo intracellular recording conditions, recordings were obtained from 66 IC neurons in 18 healthy adult mice (Mus musculus, Km) under free field-stimulation. Fifty-eight of these neurons fi red bursts of action potentials (APs) to auditory stimuli and the remaining eight just generated local responses such as excitatory (n = 4) or inhibitory (n = 4) postsynaptic potentials. Based on the APs and subthreshold responses, the discharge patterns were classified into seven types: phasic (24/58, 41.4%), phasic burst (8/58,13.8%), pauser (4/58, 6.9%), phasic-pauser (1/58, 1.7%), chopper (2/58, 3.4%), primary-like tonic (14/58, 24.1%) and sound-induced inhibitory (5/58,8.6%). We concluded that (1) IC neurons exhibit at least seven distinct discharge patterns; (2) inhibition participates in shaping the discharge pattern of most IC neurons and plays a role in sculpting the pattern, except for the primary-like tonic pattern which was not shaped by inhibition; and (3) local neural circuits are the likely structural basis that shapes the discharge patterns of IC neurons and can be formed either in the IC or in lower-level auditory structures.

Recovery cycles of single-on and double-on neurons in the inferior colliculus of the leaf-nosed bat, Hipposideros armiger.

Our previous study showed that when stimulated with constant frequency-frequency modulation (CF-FM) sounds, neurons in the central nucleus of the inferior colliculus of the CF-FM bat, Hipposideros armiger, either only discharged impulses to the onset of CF-FM sounds (76%, single-on neurons) or to the onset of both CF and FM components of CF-FM sounds (24%, double-on neuron) (Fu et al., 2010). The present paper reports the recovery cycles of these two types of neurons using paired CF, FM and CF-FM sounds as stimuli. Both types of neurons had similar recovery cycle for CF sounds but had the shortest recovery cycle for FM sounds. Whereas single-on neurons had similar recovery cycle for CF and CF-FM sounds, double-on neurons had longer recovery cycle for CF sounds than for CF-FM sounds. In addition, double-on neurons had significantly shorter recovery cycles than single-on neurons for FM and CF-FM sounds. Most neurons did not respond to the second sound when each pair of sounds overlapped. However, when stimulated with paired CF-FM sounds, 3 single-on and 7 double-on neurons discharged to the second sound even when both sounds overlapped. As such, they had "cyclic" recovery cycles that varied between maximum and minimum with inter-pulse intervals. Possible mechanisms underlying the different recovery cycles of these neurons are proposed. Possible biological significance of these neurons in relation to responding to varied pulse repetition rate during hunting is discussed.

The auditory response properties of single-on and double-on responders in the inferior colliculus of the leaf-nosed bat, Hipposideros armiger.

The present study examines the response properties of neurons in the central nucleus of the inferior colliculus (IC) of the CF-FM (constant frequency-frequency-modulated) bat, Hipposideros armiger using CF, FM and CF-FM sounds as stimuli. All 169 IC neurons recorded are tonotopically organized along the dorsoventral axis of the IC. Collicular neurons have V-shaped or upper-threshold frequency tuning curves. Those neurons tuned at the predominant second harmonic have extremely sharp frequency tuning curves and low minimum thresholds. Collicular neurons typically discharge impulses to both CF and FM sounds. However, when stimulated with CF-FM sounds, most (76%) neurons only discharge impulses to the onset of CF-FM sounds (single-on responders). The remaining neurons (24%) discharge impulses to both CF and FM components (double-on responders) of CF-FM sounds. The double-on responders have higher minimum threshold and longer latency to the FM component than to the CF component of CF-FM sounds. Our data show that the FM component of the CF-FM sounds contributes significantly in shaping the discharge pattern, latency and number of impulses of IC neurons. The present study suggests that using CF-FM sounds to study auditory response properties of the CF-FM bat may be essential for a better understanding of echo analysis by the CF-FM in the real world. Because the double-on responders have shorter response latency than single-on responders, we speculate that these two types of responders may be best suited for echo analysis during different phases of hunting.