Evolutionary aspects of bat echolocation.

This review is yet another attempt to explain how echolocation in bats or bat-like mammals came into existence. Attention is focused on neuronal specializations in the ascending auditory pathway of echolocating bats. Three different mechanisms are considered that may create a specific auditory sensitivity to echos: (1). time-windows of enhanced echo-processing opened by a corollary discharge of neuronal vocalization commands; (2). differentiation and expansion of ensembles of combination-sensitive neurons in the midbrain; and (3). corticofugal top-down modulations. The second part of the review interprets three different types of echolocation as adaptations to ecological niches, and presents the sophisticated cochlear specializations in constant-frequency/frequency-modulated bats as a case study of finely tuned differentiation. It is briefly discussed how a resonant mechanism in the inner ear of constant-frequency/frequency-modulated bats may have evolved in common mammalian cochlea.

The function of the medial superior olive in small mammals: temporal receptive fields in auditory analysis.

Traditionally, the medial superior olive, a mammalian auditory brainstem structure, is considered to encode interaural time differences, the main cue for localizing low-frequency sounds. Detection of binaural excitatory and inhibitory inputs are considered as an underlying mechanism. Most small mammals, however, hear high frequencies well beyond 50 kHz and have small interaural distances. Therefore, they can not use interaural time differences for sound localization and yet possess a medial superior olive. Physiological studies in bats revealed that medial superior olive cells show similar interaural time difference coding as in larger mammals tuned to low-frequency hearing. Their interaural time difference sensitivity, however, is far too coarse to serve in sound localization. Thus, interaural time difference sensitivity in medial superior olive of small mammals is an epiphenomenon. We propose that the original function of the medial superior olive is a binaural cooperation causing facilitation due to binaural excitation. Lagging inhibitory inputs, however, suppress reverberations and echoes from the acoustic background. Thereby, generation of antagonistically organized temporal fields is the basic and original function of the mammalian medial superior olive. Only later in evolution with the advent of larger mammals did interaural distances, and hence interaural time differences, became large enough to be used as cues for sound localization of low-frequency stimuli.

Discrimination of wingbeat motion by bats, correlated with echolocation sound pattern.

Bats of the species Rhinolophus rouxi, Hipposideros lankadiva and Eptesicus fuscus were trained to discriminate between two simultaneously presented artificial insect wingbeat targets moving at different wingbeat rates. During the discrimination trials, R. rouxi, H. lankadiva and E. fuscus emitted long-CF/FM, short-CF/FM and FM echolocation sounds respectively. R. rouxi, H. lankadiva and E. fuscus were able to discriminate a difference in wingbeat rate of 2.7 Hz, 9.2 Hz and 15.8 Hz, respectively, between two simultaneously presented targets at an absolute wingbeat rate of 60 Hz, using a criterion of 75% correct responses. The performance of the different bat species is correlated with the echolocation signal design used by each species, particularly with the presence and relative duration of a narrowband component preceding a broadband FM component. These results provide behavioral evidence supporting the hypothesis that bats that use CF/FM echolocation sounds have adaptations for the perception of insect wingbeat motion and that long-CF/FM species are more specialized for this task than short CF/FM species.

Ontogenesis of tonotopy in inferior colliculus of a hipposiderid bat reveals postnatal shift in frequency-place code.

The postnatal development of midbrain tonotopy was investigated in the inferior colliculus (IC) of the south Indian CF-FM bat Hipposideros speoris. The developmental progress of the three-dimensional frequency representation was determined by systematic stereotaxic recordings of multiunit clusters from the 1st up to the 7th postnatal week. Additional developmental measures included the tuning characteristics of single units (Figs. 3f; 4f; 5f), the analysis of the vocalised pulse repertoire (Figs. 3e, 4e, 5e), and morphometric reconstructions of the brains of all experimental animals (Fig. 1). The maturation of auditory processing could be divided into two distinct, possibly overlapping developmental periods: First, up to the 5th week, the orderly tonotopy in the IC developed, beginning with the low frequency representation and progressively adding the high frequency representation. With regard to the topology of isofrequency sheets within the IC, maturation progresses from dorsolateral to ventromedial (Figs. 3c, 4c). At the end of this phase the entire IC becomes specialised for narrowly tuned and sensitive frequency processing. This includes the establishment of the 'auditory fovea', i.e. the extensive spatial representation of a narrow band of behaviorally relevant frequencies in the ventromedial part of the IC. In the 5th postnatal week the auditory fovea is concerned with frequencies from 100-118 kHz (Fig. 4c, d). During subsequent development, the frequency tuning of the auditory fovea increases by 20-25 kHz and finally attains the adult range of ca. 125-140 kHz. During this process, neither the bandwidth of the auditory fovea (15-20 kHz) nor the absolute sensitivity of its units (ca. 50 dB SPL) were changed. Further maturation occurred at the single unit level: the sharpness of frequency tuning increased from the 5th to the 7th postnatal weeks (Q-10-dB-values up to 30-60), and upper thresholds emerged (Figs. 4f, 5f). Although in the adult the frequency of the auditory fovea matches that of the vocalised pulses, none of the juvenile bats tested from the 5th to the 7th weeks showed such a frequency match between vocalisation and audition (Figs. 4e, 5e). The results show that postnatal maturation of audition in hipposiderid bats cannot be described by a model based on a single developmental parameter.

Foraging ecology and audition in echolocating bats.

The types of echolocation signal and the auditory capacities of echolocating bats are adapted to specific acoustical constraints of the foraging areas. Bats hunting insects above the canopy use low frequencies for echolocation; this is an adaptation to prey detection over long distances. Bats foraging close to and within foliage avoid masking of insect echoes by specializing on 'fluttering target' detection. 'Gleaning' bats are adapted to the auditory detection of very faint noises generated by ground-dwelling prey, and are capable of analysing fine changes in the echo spectrum, which may indicate a stationary prey changing its posture on a substrate. This review of recent research demonstrates that, in bats, foraging ecology and audition are intricately interrelated and interdependent.

Interaural time and intensity coding in superior olivary complex and inferior colliculus of the echolocating bat Molossus ater.

Single-unit responses to tonal stimulation with interaural disparities were recorded in the nuclei of the superior olivary complex (SOC) and the central nucleus of the inferior colliculus (ICC) of the echolocating bat, Molossus ater. Seventy-six units were recorded from the ICC and 74 from the SOC; of the SOC units, 31 were histologically verified in the medial superior olive (MSO), 10 in the lateral superior olive (LSO), and 33 in unidentified areas of the SOC. Best frequencies (BFs) of the units ranged from 10.3 to 89.6 kHz, and Q10 dB values ranged from 2 to 70 dB. Most ICC neurons responded phasically to stimulus onset and were either inhibitory/excitatory [I/E; (53)] or excitatory/excitatory [E/E; (21)] units. In the MSO, 23 units responded tonically and 7 phasically on, 18 were E/E or E/OF (facilitatory for other input) units, and 11 were I/E neurons. All LSO neurons responded in a "chopper" fashion, and the binaural neurons were E/I units. In E/E units the excitatory response to binaural stimulation was frequently larger than the sum of the monaurally evoked responses. Many neurons with E/I or I/E inputs had very steep binaural impulse-count functions and were sensitive to small interaural intensity differences. Twenty-eight units (24%) responded with a change in firing rate of at least 20% to interaural time differences of +/- 500 microseconds. Within this sample, 11 units (8 from ICC, 2 from MSO, and 1 from SOC) were sensitive to interaural time differences of only +/- 50 microseconds. Of these 11 units, 10 were I/E units responding phasically only to stimulus onset and were also sensitive to intensity differences (delta I), being suppressed completely by the inhibitory input over a delta I range of 20 dB or less. Of 117 units tested in the ICC and SOC nuclei, 86 units (76%) were not sensitive to interaural time disparities within +/- 500 microseconds. Because the BFs of these units sensitive to interaural transient time differences (delta t) ranged between 18 and 90 kHz, responses were elicited by pure tones, and responses did not change periodically with the period equal to that of the stimulus frequency, we conclude that the neurons reacted to interaural differences of stimulus-onset time (transient time difference) but not to phase differences (ongoing time difference). Sensitivity to interaural time differences was also correlated with interaural intensity differences.(ABSTRACT TRUNCATED AT 400 WORDS)

Processing of noise by single units of the inferior colliculus of the bar Rhinolophus ferrumequinum.

For inferior colliculus units the response patterns and the thresholds for pure tones and noise of variable bandwidth were determined. In a threshold-bandwidth plot the noise thresholds usually fell along two regression lines whose point of intersection established the size of the neuronal critical bandwidth (nCB). The relevance of the small nCBs (0.2-0.4 kHz) obtained for the frequency range of the constant frequency part of the orientation call is discussed. No fixed relation was found either between the nCBs and the neuronal critical ratios or between the size of nCB and the width of the tuning curve 3 dB above threshold of the best frequency.