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PubMed2006

Sensory acquisition in active sensing systems.

A defining feature of active sensing is the use of self-generated energy to probe the environment. Familiar biological examples include echolocation in bats and dolphins and active electrolocation in weakly electric fish. Organisms that utilize active sensing systems can potentially exert control over the characteristics of the probe energy, such as its intensity, direction, timing, and spectral characteristics. This is in contrast to passive sensing systems, which rely on extrinsic energy sources that are not directly controllable by the organism. The ability to control the probe energy adds a new dimension to the task of acquiring relevant information about the environment. Physical and ecological constraints confronted by active sensing systems include issues of signal propagation, attenuation, speed, energetics, and conspicuousness. These constraints influence the type of energy that organisms use to probe the environment, the amount of energy devoted to the process, and the way in which the nervous system integrates sensory and motor functions for optimizing sensory acquisition performance.

Animals↗
PubMed2006

Temperature affects interaction of visual and vibrational cues in parasitoid host location.

Parasitoid host location in nature is facilitated by simultaneously using different information sources. How multisensory orientation on the same spatial scale is influenced by environmental conditions is however poorly understood. Here we test whether changes in reliability of cues can cause parasitoids to alter multisensory orientation and to switch to cues that are more reliable under extreme temperatures. In the ichneumonid wasp Pimpla turionellae, multisensory use of thermally insensitive vision and thermally sensitive mechanosensory host location by vibrational sounding (echolocation on solid substrate) was investigated with choice experiments on plant-stem models under optimum temperature (18 degrees C), at high- (28 degrees C) and low-temperature limits (8 degrees C) of vibrational sounding. Temperature affected relative importance of vibrational sounding whereas visual orientation did not vary. At 18 degrees C, parasitoids used visual and vibrational cues with comparable relative importance. At 8 and 28 degrees C, the role of vibrational sounding in multisensory orientation was significantly reduced in line with decreased reliability. Wasps nearly exclusively chose visual cues at 8 degrees C. The parasitoids switch between cues and sensory systems depending on temperature. As overall precision of ovipositor insertions was not affected by temperature, the parasitoids fully compensate the loss of one cue provided another reliable cue is available on the same spatial scale.

Animals↗
PubMed2001

The effect of sound intensity on duration-tuning characteristics of bat inferior collicular neurons.

Previous studies have shown that inferior collicular neurons of the big brown bat, Eptesicus fuscus, serve as short-, band-, long- and all-pass filters for sound durations. Neurons with band-, short- and long-pass filtering characteristics discharged maximally to a specific sound duration or a range of sound durations. In contrast, neurons with all-pass filtering characteristics do not have duration selectivity. To determine if duration-tuning characteristics of collicular neurons were tolerant to changes in sound intensity, we examined the duration-tuning characteristics of collicular neurons using a wide range of sound intensities. Duration-tuning characteristics examined included the type, bandwidth and slope of duration-tuning curves. Sound intensity delivered within 20 dB of minimum threshold did not affect duration-tuning characteristics of all collicular neurons studied. Sound intensities at still higher levels did not affect the tuning characteristics of two-thirds of collicular neurons but decreased the duration selectivity and changed the duration-tuning curves of the remaining one-third of neurons from one type to another. However, these two groups of duration-tuning collicular neurons were not separately organized inside the inferior colliculus. The biological relevance of these findings to bat echolocation is discussed.

Acoustic Stimulation↗
PubMed1998

Bat sonar: an alternative interpretation of the 10-ns jitter result.

In 1990 Simmons et al. reported evidence of a time resolution hitherto unknown in any animal, namely a 10-ns jitter detection threshold in echolocating bats. This result is discussed. The calibration data from the original papers are examined. Observations indicating other cues than delay being presented to the bats are given. We offer an alternative explanation for the psychometric jitter function, based on the assumption of a subtle distortion due to impedance mismatch in the delay-producing apparatus. We also report that effects of impedance mismatch are detectable by a human subject in a model experiment.

Acoustic Stimulation↗
PubMed1999

Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons.

This study examines the contribution of GABAergic inhibition to the discharge pattern and pulse duration tuning characteristics of 101 bat inferior collicular neurons by means of bicuculline application to their recording sites. When stimulated with single pulses 56 (55%) neurons discharged 1 or 2 impulses (phasic responders), 42 (42%) discharged 3-10 impulses (phasic bursters) and 3 (3%) discharged impulses throughout the stimulus duration (tonic responders). Bicuculline application increased the number of impulses and changed the discharge patterns of 66 neurons. Using 50% difference between maximal and minimal responses as a criterion, the duration tuning characteristics of these neurons can be described as band-pass (20, 20%), long-pass (17, 17%), short-pass (33, 32%), and all-pass (31, 31%). Each band-pass neuron discharged maximally to a specific duration (the best duration) which was at least 50% larger than the neuron's responses to a long-duration pulse and a short-duration pulse. In contrast, each long- or short-pass neuron discharged maximally to a range of long or short duration pulses. Bicuculline application changed the duration tuning characteristics of 65 neurons. Possible mechanisms underlying duration tuning characteristics and the behavioral relevance to bat echolocation are discussed.

Acoustic Stimulation↗
PubMed1999

Frequency discrimination of brief tonal steps as a function of frequency in the lesser bulldog bat.

In a two-alternative, forced-choice task lesser bulldog bats were trained to distinguish between a pure tone pulse and a pulse composed of a series of brief tonal steps oscillating between two different frequencies. The tone-step pulse gradually approximates the pure tone pulse as the frequency difference between the steps becomes progressively smaller. Frequency difference limens for the brief tonal frequency steps were determined for a broad range of ultrasonic frequencies. The variation in tone-step difference limens with frequency appears to be correlated to the frequency structure of the bat's short-constant-frequency/frequency-modulated echolocation sound. There was a marked decline in the value of the relative frequency difference limens (Weber ratio) over a fairly narrow range of frequencies above the constant frequency and a sharp increase in threshold above this range. The relative thresholds for frequency discrimination were small and uniform over the frequency range of the frequency-modulated sweep and increased for frequencies below the frequency-modulated sweep. Thus, the most accurate frequency-discrimination abilities occur over a narrow frequency range around the frequency of the constant-frequency component of returning echoes. Frequency discrimination over the range of frequencies of the frequency-modulated component is relatively good.

Acoustic Stimulation↗
PubMed1999

Binaural influences on Doppler shift compensation of the horseshoe bat Rhinolophus rouxi.

The flying horseshoe bat Rhinolophus rouxi compensates for Doppler shifts in echoes of their orientation pulses. By lowering the frequency of subsequent calls the echo's constant frequency is stabilized at the so-called reference frequency centered in a narrow and sensitive cochlear filter. This audio-vocal behaviour is known as Doppler shift compensation. To investigate whether the bats depend on binaural cues when compensating, three animals were tested for compensation on a swing before and after unilateral deafening. In each case compensation was severely impaired by unilateral deafening. Individual animals' compensation amplitude was reduced to 28-48% of the preoperational compensation of a +1.8 kHz shift. Doppler shift compensation performance did not recover to control levels during the observed period of 24 h after surgery. In contrast, unilateral middle ear removal which induces a unilateral auditory threshold increase of 9-14 dB does not impair compensation performance on the swing. To mimick Doppler shifts in a fixed setup, the frequencies of recorded echolocation calls were experimentally shifted between 0 and +2 kHz and played back via earphones to six animals. The bats completely compensated the experimental shifts only as long as the interaural intensity difference of the playback did not exceed 20 dB. No animal compensated with monaural playback.

Adaptation, Physiological↗
PubMed2001

Temporally patterned sound pulse trains affect intensity and frequency sensitivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus.

This study examined the effect of temporally patterned pulse trains on intensity and frequency sensitivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus. Intensity sensitivity of inferior collicular neurons was expressed by the dynamic range and slope of rate-intensity functions. Inferior collicular neurons with non-monotonic rate-intensity functions have smaller dynamic ranges and larger slopes than neurons with monotonic or saturated rate-intensity functions. Intensity sensitivity of all inferior collicular neurons improved by increasing the number of non-monotonic rate-intensity functions when the pulse repetition rate of pulse trains increased from 10 to 30 pulses per second. Intensity sensitivity of 43% inferior collicular neurons further improved when the pulse repetition rate of pulse trains increased still from 30 to 90 pulses per second. Frequency sensitivity of inferior collicular neurons was expressed by the Q10, Q20, and Q30 values of threshold frequency tuning curves and bandwidths of isointensity frequency tuning curves. Threshold frequency tuning curves of all inferior collicular neurons were V-shape and mirror-images of their counterpart isointensity frequency tuning curves. The Q10, Q20, and Q30 values of threshold frequency tuning curves of all inferior collicular neurons progressively increased and bandwidths of isointensity frequency tuning curves decreased with increasing pulse repetition rate in temporally patterned pulse trains. Biological relevance of these findings to bat echolocation is discussed.

Animals↗
PubMed2004

Cytoarchitecture of the medial geniculate body and thalamic projections to the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi). I. Temporal fields.

The auditory cortex in echolocating bats is one of the best studied in mammals, yet the projections of the thalamus to the different auditory cortical fields have not been systematically analyzed in any bat species. The data of the present study were collected as part of a combined investigation of physiological properties, neuroarchitecture, and chemoarchitecture as well as connectivity of cortical fields in Rhinolophus in order to establish a neuroanatomically and functionally coherent view of the auditory cortex in the horseshoe bat. This paper first describes the neuroanatomic parcellation of the medial geniculate body and then concentrates on the afferent thalamic connections with auditory cortical fields of the temporal region. Deposits of horseradish peroxidase and wheatgerm-agglutinated horseradish peroxidase were made into neurophysiologically characterized locations of temporal auditory cortical fields; i.e., the tonotopically organized primary auditory cortex, a ventral field, and a temporal subdivision of a posterior dorsal field. A clear topographic relationship between thalamic subdivisions and specific cortical areas is demonstrated. The primary auditory cortex receives topographically organized input from the central ventral medial geniculate body. The projection patterns to the temporal subdivision of the posterior dorsal field suggest that it is a "core" field, similar to the posterior fields in the cat. Projections to the ventral field arise primarily from border regions of the ventral medial geniculate body. On the whole, the organization of the medial geniculate body projections to the temporal auditory cortex is quite similar to that described in other mammals, including cat and monkey.

Animals↗
PubMed1982

Responses of cerebellar neurons of the CF-FM bat, Pteronotus parnellii to acoustic stimuli.

Single units (125) which faithfully discharged action potentials to acoustic stimuli (35 ms in duration with 0.5 ms rise and decay times) were recorded in the cerebellar vermis and hemispheres of the CF-FM bat, Pteronotus parnellii. These units had response latencies between 1.5 and 27 ms and minimum thresholds between 2 and 83.5 dB SPL. Best frequencies (BFs) of these units ranged from 30.32 to 79.28 kHz, but more than half (64 units, 51.2%) were between 59.73 and 63.32 kHz. While most tuning curves of these units were either broad or irregular, those curves with BFs tuned at around 61 kHz which is the frequency of the predominant CF component of the bat's echolocation signals were extremely narrow with Q10-dB values as high as 153. Those units (29) with BFs tuned near the 61 kHz also showed off-responses. These data indicate that auditory specialization for processing of species-specific orientation signals also exists in the cerebellum of this bat.

Animals↗
PubMed1984

Pinna orientation determines the maximal directional sensitivity of bat auditory neurons.

The auditory response areas of 192 inferior collicular neurons (IC) of Eptesicus fuscus were studied under free field acoustic stimulation. The boundary of the auditory response area of a neuron expands with stimulus intensity (Fig. 1). However, there is a response center within each neuron's response area at which the neuron has the maximal sensitivity. All response centers of the 192 neurons are located within a limited space of the bat's contralateral auditory space. The position of the response center of a neuron changes with different pinna orientations (Figs. 2 and 3) providing a bat with versatility in maximizing the sensitivity of its echolocation system.

Acoustic Stimulation↗
PubMed1994

Connectionist networks in auditory system modeling.

Understanding how complex sounds, such as speech, are processed and eventually perceived in the brain is essential for building more effective speech processors. The echolocating bat provides an animal model for complex-sound processing of identified stimulus features at higher levels of the auditory pathway. In this paper, we present the use of connectionist models for modeling cortical neurons that play a key role in our auditory system model of a species of FM bat, Myotis lucifugus. The influence of network related parameters on modeling accuracy is presented, and the response of these models is explained in a behavioral context.

Acoustic Stimulation↗
PubMed1987

Pinna position affects the auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus.

Using free-field acoustic stimulus conditions, we studied the auditory space representation in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, under different pinna positions. Stimuli were delivered from a loudspeaker placed 14 cm in front of the bat to determine the best frequency (BF) of an isolated neuron. A BF stimulus was then delivered as the loudspeaker was moved across the frontal auditory space of the bat to locate the response center of the neuron. At the response center, the neuron has its lowest minimum threshold (MT). The stimulus was then raised 5-dB above the lowest MT to measure the spatial response area. Both response center and spatial response area of each neuron were measured under different pinna positions. Variations in the response center and MT of each neuron under different pinna positions was determined and a possible reason for this variation was discussed. The variation in auditory space representation in the IC due to variation in pinna position is presented. We suggest that during echolocation a bat could make changes in its pinna position to create additional binaural disparity for accurate target localization.

Animals↗
PubMed1989

Neural mechanisms of ranging are different in two species of bats.

The primary cue for ranging by echolocation is the delay between an emitted pulse and its echo. The abilities of several species of bats to discriminate target ranges have been accounted for by a theory which assumes that bats perform cross-correlation analysis of the FM components of pulse and echo. In this study, the neural mechanisms performing the cross-correlation are shown to differ in two species. The mustached bat emits CF-FM pulses with four harmonics (CF1-4 and FM1-4) while the little brown bat emits FM pulses with only one harmonic (FM1). In the auditory cortex of both species, there is a cluster or clusters of delay-tuned neurons. Delay-tuned neurons in the mustached bat utilize delay lines created by neurons which respond to the FM1 component of the pulse and extract range information from the combination of the pulse FM1 and the echo FMn (n = 2, 3, or 4). In contrast, delay-tuned neurons in the little brown bat utilize delay lines evoked by the pulse FM1, which is stronger than the echo FM1, and extract range information from the combination of the pulse FM1 and the echo FM1. Inhibition is involved in creating the delay lines in both species.

Acoustics↗
PubMed1992

High frequency distortion products from the ears of two bat species, Megaderma lyra and Carollia perspicillata.

In two echolocating bat species, Megaderma lyra and Carollia perspicillata 2f1-f2 distortion products were measured acoustically in the outer ear canal for f1 frequencies between 5 and 95 kHz in an attempt to study nonlinear cochlear processes at high frequencies. Similar to other mammals, the input/output (I/O) functions of 2f1-f2 show non-monotonicities and notches at f1 levels between 40-70 dB SPL. The slope of the initial rise of the 2f1-f2 I/O functions increased with f1 frequency from 0.73 (5 kHz) to 1.41 (95 kHz) in Megaderma and from 0.66 (7.5 kHz) to 1.47 (95 kHz) in Carollia. With increasing f1 frequency the optimum frequency ratio f2/f1 in order to evoke maximum distortion level decreases from 1.18 (5 kHz) to 1.09 (95 kHz) in Megaderma and from 1.21 (7.5 kHz) to 1.11 (95 kHz) in Carollia. This is taken as indication of a general increase of the quality of tuning of the distortion generating mechanism with frequency. The f1 levels that were sufficient to elicit distortion levels of -10 dB SPL were used to construct iso-distortion threshold curves which lay on average 37.2 dB (Megaderma) and 33.9 dB (Carollia) above the neuronal threshold curves [Rübsamen et al., J. Comp. Physiol. A 163 (1988); Sterbing et al., Proc. 18th Göttingen Neurobiol. Conf. Thieme Verlag, Stuttgart (1990)] and roughly paralleled these. Highest distortion levels (40-50 dB SPL with f1 levels of 80 dB SPL) and lowest distortion thresholds were measured in the f1 frequency range of 10-30 kHz (Megaderma) and 15-30 kHz (Carollia).(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗
PubMed1993

The influence of temporal pattern of stimulation on delay tuning of neurons in the auditory cortex of the FM bat, Myotis lucifugus.

In echolocating bats, delay-sensitive neurons show facilitative responses to simulated pulse-echo pairs at particular echo delays. Three experiments examined how the temporal pattern of stimulation affected the delay tuning of neurons in the auditory cortex of the awake FM bat, Myotis lucifugus. First, delay tuning was compared using a series of pulse-echo pairs fixed in echo delay ('standard' stimuli), and a series of pulse-echo pairs in which successive sound pairs decreased by a fixed echo-delay step ('approach' stimuli). Similar best delays were measured with both stimulation patterns presented at repetition rates in which the neuron was delay-sensitive. At the higher delay-sensitive pulse repetition rates, approach stimuli evoked larger delay-dependent responses. Second, approach stimuli were fixed at different intertrial intervals. The best delay was unaffected by intertrial interval, although some neurons showed larger responses for longer intertrial intervals (0.5, 1.0 s), especially at the higher delay-sensitive pulse repetition rates. Third, approach stimuli were fixed at different echo-delay steps to simulate target velocity. The majority of neurons showed some sensitivity to echo-delay step, with clear preference for target velocity mainly between 1.8-7.0 m/s. This suggests that delay-sensitive neurons compute target velocity by rate of change of echo delay over successive echoes. Thus, response properties of cortical neurons are influenced by dynamic acoustic conditions found in target-directed flight.

Acoustic Stimulation↗
PubMed1996

The midbrain creates and the thalamus sharpens echo-delay tuning for the cortical representation of target-distance information in the mustached bat.

Mustached bats emit complex biosonar 'pulses' for echolocation. A delay of an echo from the emitted pulse carries target-distance information. At the auditory periphery, distance information is expressed by a time interval between the responses of neurons to the emitted pulse and its echo. In the auditory cortex (AC), however, it is mapped by 'FM-FM' neurons which are tuned to particular echo delays. FM-FM neurons have been found not only in the AC but also in the inferior colliculus (IC) of the midbrain and the medial geniculate body (MGB) of the thalamus. In the present study, we found that the IC has a precursor of the cortical echo-delay axis for the systematic representation of target-distance information and that the MGB shows the improved neural representation of target-distance information.

Animals↗
PubMed1996

Further studies on the mechanics of the cochlear partition in the mustached bat. I. Ultrastructural observations on the tectorial membrane and its attachments.

From semithin and ultrathin sections of the mustached bat cochlea, baso-apical gradients in ultrastructural composition, shape and attachment site of the tectorial membrane (TM) were determined in relation to gradients in hair cell size and stereocilia size. These provide a data base for estimates of the mechanical properties of the organ of Corti as they relate to specialized aspects of the cochlear frequency map (Kössl and Vater, 1996). As in other mammals, the TM is composed to type A and type B protofibrils. Measurements of the packing density of type A protofibrils reveal gradients in both the radial and longitudinal direction. Distinct variations in packing density of type A protofibrils across the radial extent of the TM allow the definition of more subregions than in other mammals. Throughout the cochlea, packing density is highest in the 'stripe' region located close to the spiral limbus. The centrally located 'core' region of the middle zone contains distinctly fewer type A protofibrils than the laterally located 'mantle' region of the middle zone. The TM in the specialized basal turn (first and second half-turns) features a higher packing density of type A protofibrils in the 'mantle' than the TM in the apical cochlea (upper third to fifth half-turns), and in incorporation of longitudinally directed type A protofibrils in the marginal zone. Among cochlear turns, there are pronounced changes in cross-sectional area of the TM and the extent of its limbal attachment site. Within the densely innervated second half-turn that contains an expanded representation of the 60 kHz constant frequency (CF) component of the echolocation signal, both the cross-sectional area (see also Henson and Henson, 1991) and the attachment site of the TM are enlarged. An extended limbal attachment site is also observed in the densely innervated region of the lower first half-turn that represents the upper harmonics of the call. Within the sparsely innervated region of the upper first half-turn, the limbal attachment site of the TM is significantly diminished. Size of outer hair cells (OHC) ranges between 12 and 13 microns throughout the basal 80% of cochlear length and reaches maximal values of 20 microns in the apex. Size of OHC stereocilia ranges between 0.7 and 0.8 microns throughout the basal 60% of cochlear length and reaches a maximal size of 2.2 microns in the apex. These data corroborate and extend previous notions that morphological specializations of the TM in concert with specializations of the basilar membrane and perilymphatic spaces play an integral role in creating specialized cochlear tuning in the mustached bat.

Animals↗