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Using conventional electrophysiological techniques, we demonstrate that neurons in the superior colliculus of the big brown bat (Eptesicus fuscus) respond to ultrasonic signals. Most response properties of these neurons are very similar to neurons of the inferior colliculus in the same bat.
Using free-field acoustic stimulation conditions, we studied the auditory spatial response areas of 242 cerebellar neurons of Eptesicus fuscus. A best frequency stimulus was delivered from a loudspeaker which was moved across the frontal auditory space in order to determine the response center of each cerebellar neuron. At the response center, the neuron had its lowest minimum threshold. The stimulus was then raised 5-15 dB above the lowest minimum threshold of each neuron and the spatial response area for each stimulus intensity was measured. The spatial response area of each neuron expanded asymmetrically with the stimulus intensity. The size of the spatial response area was not correlated with the minimum threshold, best frequency or recording depth of the neuron. The distribution of the best frequencies of single neurons was not correlated with their recording depths or minimum thresholds. The response centers of all cerebellar neurons were located within a small area of the central portion of the frontal auditory space suggesting that the cerebellum could play an effective role in orienting the bat toward the echo source within the frontal gaze during insect capture.
The auditory spatial response areas of 333 inferior collicular (IC) neurons of Eptesicus fuscus were studied under free-field acoustic stimulus conditions. A stimulus was delivered from a loudspeaker placed 14 cm in front of a bat and the best frequency of an encountered neuron was determined. Then a best frequency (BF) stimulus was delivered as the loudspeaker was moved across the frontal auditory space to determine the response center of the neuron. At the response center, the neuron had the lowest minimum threshold. The stimulus was then raised 3-15 dB above the lowest minimum threshold of the neuron and the spatial response area for each stimulus intensity was measured. The response center and spatial response area of a neuron measured with a one-octave downward-sweep FM stimulus were similar to those measured with the pure tone pulse. The spatial response area of a neuron expanded asymmetrically with the stimulus intensity. High BF neurons generally had smaller spatial response areas than low BF neurons had. All 333 response centers were located in the contralateral auditory space. Response centers of low BF neurons tended to be located laterally while those of high BF neurons were located medially. Although each neuron had a point of lowest minimum threshold in the contralateral auditory space, the point-to-point representation of the auditory space was not systematically organized. This representation was not correlated with the recording sites of the neurons in the mediolateral, posteroanterior and dorsoventral axes of the IC.
Single-neuron responses to pulse repetition rate in the inferior colliculus, auditory cortex and pontine nuclei of the FM bat, Eptesicus fuscus were studied under free-field stimulation conditions. The best frequency (BF) and minimum threshold (MT) of each neuron were first determined with a 4 ms pulse broadcast from a specific point (response center) of the bat's frontal auditory space at which the neuron had maximal spatial sensitivity. The neuron's intensity-rate function was then studied with a 4 ms BF pulse delivered at 10 dB increments above its MT in order to determine the best intensity to which the neuron discharged maximally. The neuron's discharge pattern and number of impulses to 32 trials of 300 ms train stimuli, which consisted of different number of 4 ms BF and best intensity pulses (1, 2, 3, 8, 12, 19, 24, 29 pulses/train) and delivered at an interpulse interval of 1000, 250, 170, 100, 40, 25, 15, 12 and 10 ms (i.e. at a pulse repetition rate of 1, 4, 6, 10, 25, 40, 67, 83, 100 pulses/s), were sequentially recorded. All neurons recorded from the inferior colliculus, auditory cortex and pontine nuclei discharged phasically (1-3 impulses) but they responded to the pulse repetition rate in different manners. More than 63% of 38 inferior collicular and 65 pontine neurons studied discharged impulses to each pulse within a train stimulus when the pulse repetition rate was up to 40 pulses/s.(ABSTRACT TRUNCATED AT 250 WORDS)
A speculative neuronal model for vowel normalization and representation is offered. The neurophysiological basis for the premise is the "combination-sensitive" neuron recently documented in the auditory cortex of the mustached bat (N. Suga, W. E. O'Neill, K. Kujirai, and T. Manabe, 1983, Journal of Neurophysiology, 49, 1573-1627). These neurons are specialized to respond to either precise frequency, amplitude, or time differentials between specific harmonic components of the pulse-echo pair comprising the biosonar signal of the bat. Such multiple frequency comparisons lie at the heart of human vowel perception and categorization. A representative vowel normalization algorithm is used to illustrate the operational principles of the neuronal model in accomplishing both normalization and categorization in early infancy. The neurological precursors to a phonemic vocalic system is described based on the neurobiological events characterizing regressive neurogenesis.
With only a little knowledge of programming IBM compatible computers in Basic, it is possible to create a digital software oscilloscope with sampling rates up to 17 kHz (depending on the CPU- and bus-speed). The only additional hardware requirement is a common sound card compatible with the Soundblaster. The system presented in this paper is built to analyse the direction a flying bat is facing during sound emission. For this reason the system works with some additional hardware devices, in order to monitor video sequences at the computer screen, overlaid by an online oscillogram. Using an RS232-interface for a Panasonic video tape recorder both the oscillogram and the video tape recorder can be controlled simultaneously and moreover be analysed frame by frame. Not only acoustical events, but also APs, myograms, EEGs and other physiological data can be digitized and analysed in combination with the behavioural data of an experimental subject.
Cochlear microphonic (CM) potentials were recorded from the bat, Pteronotus p. parnellii during tethered flight and during simulated flight on a pendulum. For each emitted signal the frequency of the ca. 61 kHz constant frequency (CF) component was compared with the frequency response characteristics of the animals's ear. The majority of "resting pulses' had CF components with the maximum frequency approximately 200 Hz below the best frequency (BF) of the CM audiogram. Doppler shift compensation occurred only during forward swings of the pendulum and in such a way that the echo CF components were always maintained near the BF, but on the low frequency slope of the CM audiogram. CM responses to emitted pulses were usually small in amplitude and in some animals no responses were seen. Echoes Doppler shifted upward, however, evoked high amplitude potentials. Echo CF components estimated to be at least 43 dB fainter than the emitted pulses evoked higher amplitude CM potentials than the loud emitted pulses. Echoes from large surfaces up to 4.5-5.0 meters away evoked CM potentials as high in amplitude as those elicited by emitted pulses, even when there was no Doppler shift. Beats in the CM were observed on many occasions and occurred as a result of pulse-echo and echo-echo interactions.
The acoustic vibrations of the eardrum at the umbo and of the stapes have been measured in the greater horseshoe bat. The displacement amplitude response of the eardrum shows a second-order low-pass characteristic, typical of a lumped mass and stiffness system with a resonance frequency of about 55 kHz. The effective mass was calculated to be about 8 micrograms, and the specific stiffness 40 X 10(6) dyne/cm3, which is one hundred times greater than guinea pig. The measured level ratio appears to be greater (3X - 5X) than the geometric ratio (2X) probably due to flexing of the manubrium. The umbo-stapes phase lag exceeds 1 cycle at high frequencies, suggesting a system of at least four reactances. This is not consistent with the relatively slight change in lever ratio with frequency. One possibility for reconciling the two results is that the distributed mass and stiffness of the ossicles act as a transmission line for transverse vibrations. There is no evidence for a sharply peaked middle-ear response (although it is more sharply tuned than some species), nor for resonant absorption by the cochlea in the region of 83 kHz - the 'constant' frequency of this bat. The eardrum shows theoretically optimal matching to the air at 55 kHz and is reasonably efficient from 15 kHz to at least 110 kHz.
The greater horseshoe bat has greatly expanded frequency mapping, and morphological specialisations, in the first half turn of its cochlea and a sudden transition to normal mapping. Amplitude and phase of vibration have been measured on various structures in the expanded and normal regions and have not revealed any sharply tuned responses. Amplitudes are much lower than those found in other species and frequently show a deep notch in the 77-84 kHz region. The high-frequency cut-off frequencies are tonotopically organised but deviate from the Bruns map, so that hair-cell tuning appears to occur at a frequency at which basilar membrane vibration is small. In the basal region, phase differences were frequently found between the inner and outer parts of the basilar membrane. These appear to be due to interaction between two components of motion and are probably not indicative of a further filtering mechanism. There is no evidence for reflection of the travelling wave at the transition.
Binaurally sensitive E-I neurons in the inferior colliculus are topographically organized with respect to their sensitivity to interaural intensity disparities (IIDs). IID sensitivity dictates the azimuthal position of the medial border of a neuron's spatial receptive field. A sound moving along the azimuth will result in a change in the percentage of excited neurons as receptive field borders are crossed. Percent excitation within this population may provide a neural code for horizontal sound location.
Mustached bats, Pteronotus p. parnellii, use complex, multiharmonic biosonar signals with prominent approx. 60 kHz (CF) components. The sense of hearing is especially acute to sounds near 60 kHz and the cochlea shows a number of specializations in the 60 kHz region. Foremost is a remarkable degree of cochlear resonance. In this study it is shown that: 1) any sounds near the resonance frequency elicit a pronounced resonance that continues after the stimulus terminates; 2) Doppler-shifted echoes of the bat's own cries may cause resonance; 3) continuous resonance can be produced by stimulating the ear with broadband noise but such resonance does not interfere with the bat's ability to Doppler-shift compensate during simulated flight; 4) significant changes in the resonance frequency of the cochlea occur during and after flight; 5) the changes in resonance can be dependent or independent of body temperature changes; and 6) mustached bats continuously adjust the CF component of their pulses to keep the second harmonic echoes in a constant frequency band near the resonance frequency. Thus, mustached bats not only compensate for Doppler-shifts imposed by their movements relative to that of a target, but they cochlear resonance compensate to deal with small changes in the micromechanical properties of the cochlea.
The sense of hearing in the mustached bat, Pteronotus parnellii, is specialized for fine frequency analysis in three narrow bands that correspond to approx 30, 60 and 90 kHz constant frequency harmonics in the biosonar signals used for Doppler-shift compensation and acoustic imaging of the environment. Previous studies have identified anatomical specializations in and around the area of the cochlea that processes the dominant second harmonic component, but similar features have not been found in areas related to sharp tuning and high sensitivity for the first or third harmonics. In this report we call attention to the large size of the tectorial membrane and spiral limbus in all three areas that appear to process the harmonically related constant frequency components. These structures are especially pronounced in the regions of the cochlea that respond to the approx 61 kHz, second harmonic and 91.5 kHz, third harmonic bands; they correspond specifically to areas where the density of afferent nerve fibers is high and where very sharply tuned neurons occur. These data for cochleae with multiple specializations lend strong support to the idea that the mass of the tectorial membrane can be an important factor in establishing the response properties of the cochlea.
Tadarida brasiliensis mexicana employs a broad-band sonar system at frequencies between 80 and 20 kHz and is characterized by non-specialized hearing capabilities. The cochlear frequency map was determined with extracellular horseradish peroxidase tracing in relation to quantitative morphological data obtained with light, scanning and transmission electron microscopy. These data reveal distinct species characteristic specializations clearly separate from the patterns observed in other bats with either broad-band or narrow-band sonar systems. The basilar membrane (BM) is coiled to 2.5 turns and about 12 mm long. Its thickness and width only change within the extreme basal and apical ends. The frequency range from about 30 to 80 kHz is represented in the lower basal turn with a typically mammalian mapping coefficient of about 3 mm/octave. This region exhibits morphological features correlated with non-specialized processing of high frequencies. (1) The BM is radially segmented by thickenings of pars tecta and pars pectinata. (2) The 3 rows of outer hair cells (OHCs) have similar morphology. Between 35 and 86% distance from base, frequencies between 30 and 12 kHz are represented with a slightly expanded mapping coefficient of about 6 mm/octave. In analogy to previous work, this cochlea region is termed acoustic fovea. It includes the frequency range of maximum sensitivity and sharpest tuning (21-27 kHz) but also frequencies below the sonar signals. The fovea is characterized by several morphological specializations. (1) The BM features a continuous radial thickening mainly composed of hyaline substance. (2) There is an increased number of layers of tension fibroblasts in the spiral ligament. (3) There are morphological differences in the arrangements of stereocilia bundles among the 3 rows of OHCs. The transitions between non-specialized and specialized cochlear regions occur gradually within a distance of about 600 microns. The gradients in stereocilia length of both receptor cell types and the gradations in length of the OHC bodies match specialized aspects of the frequency map.
In this study, we present a methodology that identifies acoustic units in Gunnison's prairie dog alarm calls and then uses those units to classify the alarm calls and bouts according to the species of predator that was present when the calls were vocalized. While traditional methods measure specific acoustic parameters in order to describe a vocalization, our method uses the variation in the internal structure of a vocalization to define possible information structures. Using a simple representation similar to that used in human speech to identify vowel sounds, a software system was developed that uses this representation to recognize acoustic units in prairie dog alarm calls. These acoustic units are then used to classify alarm calls and their associated bouts according to the species of predator that was present when the alarm calls were vocalized. Identification of bouts with up to 100% accuracy was obtained. This work represents a first step toward revealing the details of how information is encoded in a complex nonhuman communication system. Furthermore, the techniques discussed in this paper are not restricted to a database of prairie dog alarm calls. They could be applied to any animal whose vocalizations include multiple simultaneous frequencies.
The mechanism of sound reception and the hearing abilities of the prawn (Palaemon serratus) have been studied using a combination of anatomical, electron microscopic and electrophysiological approaches, revealing that P. serratus is responsive to sounds ranging in frequency from 100 to 3000 Hz. It is the first time that the Auditory Brainstem Response (ABR) recording technique has been used on invertebrates, and the acquisition of hearing ability data from the present study adds valuable information to the inclusion of an entire sub-phylum of animals when assessing the potential impact of anthropogenic underwater sounds on marine organisms. Auditory evoked potentials were acquired from P. serratus, using two subcutaneous electrodes positioned in the carapace close to the supraesophageal ganglion and the statocyst (a small gravistatic organ located below the eyestalk on the peduncle of the bilateral antennules). The morphology of the statocyst receptors and the otic nerve pathways to the brain have also been studied, and reveal that P. serratus possesses an array of sensory hairs projecting from the floor of the statocyst into a mass of sand granules embedded in a gelatinous substance. It is the purpose of this work to show that the statocyst is responsive to sounds propagated through water from an air mounted transducer. The fundamental measure of the hearing ability of any organism possessing the appropriate receptor mechanism is its audiogram, which presents the lowest level of sound that the species can hear as a function of frequency. The statocyst of P. serratus is shown here to be sensitive to the motion of water particles displaced by low-frequency sounds ranging from 100 Hz up to 3000 Hz, with a hearing acuity similar to that of a generalist fish. Also, recorded neural waveforms were found to be similar in both amplitude and shape to those acquired from fish and higher vertebrates, when stimulated with low-frequency sound, and complete ablation of the electrophysiological response was achieved by removal of the statocyst.
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Theories of brain function abound, and they range from Aristotle's idea that it cools the blood to the most recent conclusions deduced from fMRI scans. Today, such ideas, theories and constructs are often called models, the best of which blend the writer's laboratory data with what he or she has culled from the experiments others report. A model can therefore be viewed as the product of a unique collection of intellectual encounters with teachers-some living, some dead-at lectures and in libraries to which have been added countless unique personal experiences during experiments performed in laboratories. This essay describes some of the models I have published, naming the places where the experiments were done and some of the teachers from whom I learned what I know.