Orientation Sounds Research Articles

Selective laryngeal neurotomy and the control of phonation by the echolocating bat,Eptesicus

1. The effect, on the subglottic pressure and on the emitted orientation sounds, of selectively cutting nerves to various laryngeal muscles of the Big Brown Bat,Eptesicus fuscus, was studied. 2. Bilateral inferior laryngeal neurotomy caused no change in the repetition rate, duration, initial frequency or bandwidth of downward sweeping frequency modulated (FM) pulses, but after this treatment mean subglottic pressure at pulse onset was lowered 8 to 16 cm H2O and the mean peak pulse intensity was reduced 4 to 5 dB. The relationship of subglottic pressure to the bandwidth of the FM sweep was also altered (Table 1, Figs. 1, 2, 3). 3. Inferior laryngeal neurotomy also caused the bat to produce atypical rising FM pulses which began at about 20 kHz and swept upward almost one octave (Table 1, Fig. 2). 4. Total bilateral superior laryngeal neurotomy eliminated most of the FM and reduced the fundamental frequency to 7.9 kHz with multiple harmonics (Fig. 4). Pulse duration became highly variable and the peak sound pressure level (SPL) dropped 7 to 13 dB (Table 2). The correlation between subglottic pressure and pulse SPL was also eliminated. 5. Bilateral section of only the caudal branch of the superior laryngeal nerve reduced the fundamental frequency of the pulses to 10 kHz and eliminated most of the frequency modulation. Pulse SPL was reduced about 10 dB, but pulse onset subglottic pressure remained correlated with the maximum SPL (Table 2). 6. Paralysis of the tongue by bilateral section of the hypoglossal nerves distal to the thyrohyoid twigs had no detectable effect on the downward sweeping FM pulses, but caused the bats to also emit long duration pulses whose frequency rose and fell in a sinusoidal fashion (Figs. 5, 6). 7. The muscular control of pulse frequency and intensity is discussed in the light of these data. The aberrant rising FM after section of the inferior laryngeal nerves and sigmoid pulses after hypoglossal neurotomy can be understood as the result of timing errors in the opening and/or closing of the glottis relative to the contraction-relaxation cycle of the cricothyroid muscles.

Echolocation calls produced by Trachops cirrhosus (Chiroptera: Phyllostomatidae) while hunting for frogs

The echolocation calls produced by Trachops cirrhosus in the field and in a flight cage were recorded as they hunted for frogs. The calls were of low intensity (< 70 dB sound pressure level (SPL) at 10 cm), short (less than 1 ms), multiharmonic frequency modulated sweeps with energy from over 100 to around 50 kHz. During most successful attacks of frogs in the cage, these orientation sounds were produced by the bats which are also known to rely on frog calls to locate prey.

Echolocation and hearing in the mouse-tailed bat (Rhinopoma hardwickei)

Rhinopoma produces four-harmonic, constant frequency orientation sounds. The 7- to 8-ms-long search and 2- to 4-ms-long approach signals rise to full amplitude in two to three waves of the fundamental (18 kHz), producing an onset transient. This click-CF signal appears unique to Rhinopoma and may link the complex orientation sounds of the Microchiroptera with the sonar clicks of shrews. The N4 audiogram shows sensitivity peaks corresponding to the harmonic peaks of the signal spectrum. Sensitivity is particularly great for the second harmonic, the strongest component of the signal. This sharp tuning around the second harmonic suggests that primary auditory neurons may have Q-10 dB values as high as 20 to 50. The sharp roll-off on the low frequency side of this sensitivity peak further suggests Rhinopoma may perform the Doppler-compensation response.

The development of flight, foraging, and echolocation in the little brown bat (Myotis lucifugus)

1. Two colonies of little brown bats,Myotis lucifugus (Vespertilionidae), were studied for two summers. The young could not perform practice flights within the buildings where they roosted. Young of estimated relative ages and adults were light-tagged, released, and tracked to determine the development of flying skills and foraging behavior. Orientation sounds were observed and tape-recorded. 2. The earliest flights at ca. 19–20 days of age were usually relatively brief (a few tens of seconds or less) but still remarkable considering the absence of practice. The young at first emerged after adults had left to forage, avoided entering acoustically complex habitats, flew slowly within about 50 m of the roost, and made frequent, awkward landings. They avoided other flying bats and did not pursue insects. More time was spent in rest than flight. 3. Slightly older young, beginning at ca. 22–23 days, gradually increased their flight distance and duration (Table 1) and began to hunt insects in clearings or at the forest edge. Some adopted a ‘flycatcher’ hunting style at this time. They still avoided flying conspecifics. 4. The final phase of development began at about days 24–27 and may last 2 weeks or more. It involved virtually continual flight, insect pursuits, and maneuvers that became indistinguishable from those of adults, and also gradual integration with the adults during emergence, flight along traditional routes, and foraging. 5. The echolocation sounds of young of known and estimated relative ages were recorded in the field, a flight cage, or large room. Again, development was rapid. Landing buzzes always occurred, even in the first flight, although the progressive changes in frequency were sometimes not as uniform as in adults. 6. The pulses during all phases of early flight were of lower frequency than in adults. Those emitted during cruise and approach phases were frequently paired. There is possible ontogenetic and phylogenetic significance to this pairing. Within a few days, the pairing disappeared and within ca. 1 week all echolocation parameters became similar to those of adults (Fig. 1; Table 2).

Neural axis representing target range in the auditory cortex of the mustache bat.

In echolocating bats, the primary cue for determining distance to a target is the interval between an emitted orientation sound and its echo. Whereas frequency is represented by place in the bat cochlea, no anatomical location represents of primary range. Target range is coded by the time interval between grouped discharges of primary auditory neurons in response to both the emitted sound and its echo. In the frequency-modulated-signal processing area of the auditory cortex of the mustache bat (Pteronotus parnellii rubiginosus), neurons respond poorly or not at all to synthesized orientation sounds or echoes alone but respond vigorously to echoes following the emitted sound with a specific delay from targets at a specific range. These range-tuned neurons are systemically arranged along the rostrocaudal axis of the frequency-modulated-signal processing area according to the delays to which they best respond, and thus represent target range in terms of cortical organization. The frequency-modulated-signal processing area therefore shows odotopic representation.

Long-latency "subthreshold" collicular responses to the constant-frequency components emitted by a bat.

A previously undescribed response pattern has been observed in certain single units in the posterior colliculus of Pteronotus suapurensis. These units, constituting about one-third of those tuned to the region of the dominant constant-frequency (CF) components of the orientation sounds, respond to a tone pip with a burst of spikes at a latency of 3 to 6 milliseconds, within the frequency-intensity domain of a normal V-shaped response area. In these units, however, as intensity is dropped below threshold for this response, a response of 5-to 10-milliseconds longer latency appears and persists throughout another 10 to 30 decibels of attenuation. These late responses can be very vigorous, are sharply tuned to frequencies at or just above the CF components of the signal, and are often strongest and of lowest threshold at stimulus durations of 1.5 to 3 milliseconds--approximately the duration of the CF component. These properties imply that the late responses are concerned with analysis of the CF components of echoes, apparently in ways not as prominent in other bats.

Amplitude-spectrum representation of acoustic signals in the primary auditory cortex of the mustache bat

The mustache bat (Pteronotus parnellii rubiginosus) emits orientation sounds containing a long constant-frequency (CF) component suited for echo-detection and Doppler-shift measurement. About 30% of the primary auditory cortex of this bat is chiefly devoted to processing the CF-component in Doppler-shifted echoes. In this “Doppler-shifted—CF-processing area,” single neurons recorded in any electrode penetration orthogonal to the cortex have identical best frequencies (BFs) and best amplitudes (BAs) at which the neurons show maximum excitation. The BF and BA systematically vary with the location of the neurons in the cortex, showing tonotopic and “amplitopic” representations. The representation axes are radial and eccentric, respectively. The amplitude spectrum of an acoustic signal, that is, both the relative velocity and subtended angular information about a target is thus represented in the coordinates parallel to the cortical surface. This amplitude-spectrum representation is disproportionate, projecting an echo with more perceptual significance to a larger area. Outside this Doppler-shifted—CF-processing area are found neurons specialized for responding to a particular information-bearing element or a particular combination of information-bearing elements in orientation sounds and echoes. [Work supported by NSF.]

Further studies on the peripheral auditory system of 'CF-FM' bats specialized for fine frequency analysis of Doppler-shifted echoes.

ABSTRACT In the mustache bat (Pteronotus parnellii rubiginosus), the cochlear microphonie (CM) recorded from the round window is sharply tuned at 61 kHz and shows a prominent transient response to a tone burst at about 61 kHz (i.e. its amplitude increases exponentially at the onset of the stimulus and decreases at its cessation). In terms of the time constant (1·1± 0·3 ms) and the resonance frequency (61·1±0·43 kHz) of this transient response, the Q of this system, assumed to correspond to a second-order filter, is 204 + 57. Peripheral neurones sensitive to 61 kHz have a very sharp excitatory area (or tuning curve). The Q of a tuning curve markedly increases with the rise in best frequency up to 61 kHz and decreases beyond 61 kHz. The Q value of a single neurone with best frequencies between 60·76 and 61·75 kHz is 210±189. If the assumption that the CM is directly related to the mechanical motion of the basilar membrane is correct, the very sharp tuning curves of single neurones at about 61 kHz could be simply due to the mechanical timing of the basilar membrane. Since this animal predominantly uses a 61 kHz sound for echolocation and peripheral auditory neurones show a low threshold and extremely sharp tuning at about 61 kHz, its peripheral auditory system is specialized for the reception and fine-frequency analysis of the principle component of orientation sounds and echoes. Sharply tuned neurones can code a frequency modulation as small as 0·01%, so that the wing beat of an insect would be easily coded by them. Unlike the CM, N1 is tuned at 64 kHz. This difference in best frequency is simply due to the properties of a sharply tuned resonator and N1, and not due to a mechanism comparable to lateral inhibition.

Amplitude Spectrum Representation in the Doppler-Shifted-CF Processing Area of the Auditory Cortex of the Mustache Bat

The mustache bat, Pteronotus parnellii rubiginosus, emits orientation sounds containing a long constant-frequency (CF) component that is ideal for echo detection and Doppler shift measurement. About 30 percent of the primary auditory cortex of this bat is chiefly devoted to processing the second harmonic of the CF component in Doppler-shifted echoes. In this Doppler-shifted-CF processing area, single neurons recorded in any electrode penetration perpendicular to the cortical surface have nearly identical best frequencies and best amplitudes (or best pressure levels) at which the neurons show maximum excitation. The best frequency and best amplitude vary systematically with the location of the neurons in the cerebral cortex, so that there are tonotopic and "amplitopic" representation axes, which are radial and eccentric, respectively. In other words, the best-frequency and best-amplitude contours are eccentric and radial, respectively. The amplitude spectrum of a signal is thus represented in the coordinates of amplitude and frequency parallel to the cortical surface. This amplitude spectrum representation is disproportionate according to perceptual significance, so that a signal of 61.5 to 62.0 kilohertz and 30 to 50 decibels SPL (sound pressure level) is projected to a larger area than other signals. Just outside this Doppler-shifted-CF processing area, neurons are found which are specialized for responding to a particular information-bearing element or a particular combination of information-bearing elements in orientation sounds and echoes consisting of CF and frequency-modulated components.

Directional sensitivity of echolocation in the horseshoe bat,Rhinolophus ferrumequinum

The directionality of sound emission by a horseshoe bat (Rhinolophus ferrumequinum) has been determined for the constant frequency component of its orientation sounds. The bat was fixed in the center of an acoustic perimeter and the SPL of the orientation sounds measured with a scanning microphone at different angles compared with the SPL measured by another microphone located in the direction perpendicular to the plane of the horseshoe-like structure of the nose-leaf. The maximum SPL was always found in this direction which also corresponds to the flight direction of a bat in horizontal flight. Above and lateral to this direction the SPL decreases steadily with -6 dB-points at 24 ‡ above and 23 ‡ lateral. Below the flight direction we found a prominent side lobe with a -6 dB-point at 64 ‡.

Echo delay and overlap with emitted orientation sounds and doppler-shift compensation in the bat,Rhinolophus ferrumequinum

The compensation of Doppler-shifts by the bat,Rhinolophus ferrumequinum, functions only when certain temporal relations between the echo and the emitted orientation sound are given. Three echo configurations were used: With increasing delay or decreasing duration of the Doppler-shifted echo the compensation amplitude for a sinusoidally modulated +3 kHz Dopplershift (modulation rate 0.08 Hz) decreases for all stimulus configurations (Figs. 1, 2, 3). The range of the Doppler-shift compensation system is therefore limited by the delay due to acoustic travel time to about 4 m distance between bat and target. In this range the overlap duration of the echo with the emitted orientation sound is always sufficiently long, when compared with data on the orientation pulse length during target approach from Schnitzler (1968) (Fig. 5).

Directional coding by binaural brainstem units of the CF-FM bat,Rhinolophus ferrumequinum

1. Monaural and binaural neurophysiological data were obtained from 264 units in the medullary and mesencephalic levels of the central auditory system in the CF-FM bat,Rhinolophus ferrumequinum, using earphones for acoustically separated stimulation of the two ears. 2. The units responded to pure tones delivered at their best frequencies with typical basic patterns (PST-histograms) which were classified according to the literature. 3. The latencies of the units' responses changed systematically with the recording depth from about 8 to 1.5ms when passing from the inferior colliculus at the brain's surface through the nucleus of the lateral lemniscus down to the superior olivary complex. 4. Best frequencies covered almost the whole hearing range from 2kHz up to 96kHz, but 50% of all units lay between 75 and 85kHz, the animal's best hearing range, the emission frequency of orientation sounds being between 82 and 84kHz (CF-part). 5. All lowest thresholds of single units put together demonstrate an almost perfect fitting with the behavioural hearing curve. 6. Monaural excitatory impulse count functions were mostly monotonic but many were very non-monotonic and intermediate. 7. The binaural classification (Table 1) confirmed the classical concept of the pathway and the theory of binaural interaction. The most frequently observed types were E/I (ipsilateral inhibitory, contralateral excitatory; 53 %) and E/E (both sides excitatory; 22%). 8. In all cases tested so far, best frequencies and tuning curves were the same for both sides regardless of the kind of binaural interaction. 9. The most interesting units found (13% of the total) showed together with binaural inhibition, strong facilitation in certain ranges of their dynamic range thus reinforcing the response to particular stimulus combinations. These units may be called directional specialists, useful for angular sensitivity. 10. The excitatory impulse count functions were usually steep covering a best dynamic range of 10–30dB, whereas inhibitory curves were much flatter but covered a wide dynamic range of 30–100dB. 11. Since therefore the excitatory influence is always predominant in any unit tested, coding of the sound direction is ambiguous when the absolute intensity is altered. Hence the response is not only a function of the interaural intensity difference as postulated by the theory, but also dependent upon absolute intensity levels. Neural mechanisms to compensate such ambiguities in presumably higher centers are postulated and discussed.

Echolocation by the long-eared bat,Plecotus phyllotis

The echolocating bat,Plecotus phyllotis (Vespertilionidae), uses long-CF/FM and FM sonar sounds in different situations. The CF component in long-CF/FM sounds occurs at 27 kHz and has a duration of 20 to 200 ms. The FM component sweeps down from 24 to 12 kHz, with a prominent second harmonic from 40 to 22 kHz. This second harmonic sweep is interrupted at 28 to 25 kHz, providing a notch in the spectrum of the FM component at the CF frequency. This notch probably permits isolation of CF and FM components in echoes for separate processing, thus avoiding mutual interference with the different kinds of target information the two components convey. The FM component is also used without the CF component as a sonar sound. Two other FM orientation sounds are used when the bat is in a confined space such as a room. One contains only the second and fourth harmonics of the 24 to 12 kHz fundamental sweep, while the other contains only the fifth harmonic. This bat's repertoire of sonar sounds closely matches the hearing capacities of the genus.

Neurophysiological studies on the echolocation system of bats sensitive to Doppler-shifted echoes

Rhinolophus ferrumequinum and Pteronotus parnellii emit orientation sounds consisting of a long CF component and a short FM component. The CF component is used for “Doppler-shift compensation.” In rf, the gate used to obtain the frequency information for the compensation is probably opened at the beginning of the sound emission and is closed shortly after the end of the emission. The cricothyroid muscle is highly developed and its activity decreases proportionately with the amount of Doppler-shift compensation. These bats have peripheral auditory systems highly specialized for the reception of the CF component in orientation signals. The extent of cortical representation of the peripheral sensory field depends on its important for species behavior. In p. p., neurons processing the CF components in the orientation signal and Doppler-shifted echoes occupy a disproportionately large part of the auditory cortex. The separate FM signal processing area is also large. This disproportionate cortical representation related to features of biologically significant signals is comparable to that found in the somato-sensory and visual systems in many mammals. [Work supported by NSF.]

Adaptation of the peripheral auditory system of CF-FM bats for reception and analysis of predominant components in orientation sounds and echoes

In Rhinolophus ferrumequinum and Pteronotus parnellii, each orientation sound consists of long constant-frequency (CF) and short frequency-modulated components. The CF component, which is predominant in the orientation signal, is about 83 kHz in R.f. and 61 kHz in P.p.r. The peripheral auditory system of these bats in terms of CM and N1 is so sharply tuned to the sound at either 83 or 61 kHz, that signal-to-noise ratios significantly increase at these frequencies. The excitatory tuning curves of primary auditory neurons tuned at either 81–86 kHz (R.f.) or 60–63 kHz (P.p.r.) are very narrow. The Q10 dB values, 100 on the average, can be as high as 400. These neurons can code a very minor frequency shift such as ±0.012%. The peripheral auditory system is thus specialized for the reception and free frequency analysis of the predominant component of orientation sounds and echoes. This specialization is not due to suppression or inhibition, but due to the mechanical specialization of the cochlea. [Work supported by NSF.]

Coordinated activities of middle-ear and laryngeal muscles in echolocating bats.

The middle-ear muscles and laryngeal muscles of the little brown bat (Myotis lucifugus) are highly developed. When the bat emits orientation sounds, action potentials of middle-ear muscles appear approximately 3 milliseconds after those of the laryngeal muscles; this activity of middle-ear muscles attenuates the vocal self-stimulation and improves the performance of the echolocation system. When an acoustic stimulus is delivered, both types of muscles contract; action potentials of the laryngeal muscles appear approximately 3 milliseconds after those of the middle-ear muscles. These two groups of muscles are apparently activated in a coordinated manner not only by the nerve impulses from the vocalization center, but also by those from the auditory system.

Storage of Doppler-shift information in the echolocation system of the ?CF-FM?-bat,Rhinolophus ferrumequinum

The greater horseshoe bat (Rhinolophus ferrumequinum) emits echolocation sounds consisting of a long constant-frequency (CF) component preceeded and followed by a short frequency-modulated (FM) component. When an echo returns with an upward Doppler-shift, the bat compensates for the frequency-shift by lowering the emitted frequency in the subsequent orientation sounds and stabilizes the echo image. The bat can accurately store frequency-shift information during silent periods of at least several minutes. The stored frequency-shift information is not affected by tone bursts delivered during silent periods without an overlap with an emitted orientation sound. The system for storage of Doppler-shift information has properties similar to a sample and hold circuit with sampling at vocalization time and with a rather flat slewing rate for the stored frequency information.

Laryngeal mechanisms for the emission of CF-FM sounds in the Doppler-shift compensating bat,Rhinolophus ferrumequinum

1. The laryngeal mechanisms for the production of CF-FM orientation sounds in the horseshoe bat,Rhinolophus ferrumequinum, were studied with 3 different methods: a) denervation of laryngeal muscles, b) recordings of electrical activity of the cricothyroid muscle during vocalization and Doppler-shift compensation, and c) electrical stimulation of the cricothyroid muscles. 2. Unilateral section of the inferior laryngeal nerve (i.e. denervation of the intrinsic laryngeal muscles) had no effect on the sound pattern, the frequency of the orientation sounds and the Doppler-shift compensation. Bilateral denervation led always to suffocation. 3. Unilateral section of the superior laryngeal nerve (i.e. the denervation of the cricothyroid muscles) did not change the sound pattern, but caused a decrease in the frequency of the emitted CF by 4–6 kHz. Doppler-shift compensation was possible, but it was unstable and was not accurate. 4. Bilateral denervation of the cricothyroid muscles introduced several strong harmonics in the orientation sounds. The fundamental frequencies changed considerably between 12 and 42 kHz after surgery. The frequency pattern in each harmonic is the same as in normal orientation sounds (Fig. 1). 5. The spike number per vocalization of cricothyroid muscle fibres was proportional to the frequency of the CF component of the orientation sound in a range between the resting frequency and 5 kHz below it (Fig. 2). 6. Electrical stimulation of the cricothyroid muscles increased the frequency of the emitted CF. The maximum frequency change due to electrical stimulation was about 45 Hz per ms when measured during the CF component of the orientation sound (Fig. 3). 7. Tetanus fusion frequency of the cricothyroid muscle was about 200 Hz for continuous stimulation and 400 Hz for short stimulation applied during vocalization.

Peripheral auditory tuning for fine frequency analysis by the CF-FM bat,Rhinolophus ferrumequinum

For echolocation,Rhinolophus ferrumequinum emits orientation sounds, each of which consists of a long constant-frequency (CF) component and short frequency-modulated (FM) components. The CF component is about 83 kHz and is used for Doppler-shift compensation. In this bat, single auditory nerve fibers and cochlear nuclear neurons tuned at about 83 kHz show low threshold and very sharp filter characteristics. The slopes of their tuning curves ranged between 1,000 and 3,500 dB/octave and their Q-10 dB values were between 20 and 400, 140 on the average (Figs. 3–5). The peripheral auditory system is apparently specialized for the reception and fine frequency analysis of the CF component in orientation sounds and Doppler-shift compensated echoes. This specialization is not due to suppression or inhibition comparable to lateral inhibition, but due to the mechanical specialization of the cochlea. Peripheral auditory neurons with the best frequency between 77 and 87 kHz showed not only on-responses, but also off-responses to tonal stimuli (Figs. 1, 2, and 6). The off-responses with a latency comparable to that of N1-off were not due to a rebound from either suppression or inhibition, but probably due to a mechanical transient occurring in the cochlea at the cessation of a tone burst.

Peripheral specialization for fine analysis of doppler-shifted echoes in the auditory system of the "CF-FM" bat Pteronotus parnellii.

Pteronotus parnellii uses the second harmonic (61-62 kHz) of the CF component in its orientation sounds for Doppler-shift compensation. The bat's inner ear is mechanically specialized for fine analysis of sounds at about 61-62 kHz. Because of this specialization, cochlear microphonics (CM) evoked by 61-62 kHz tone bursts exhibit prominent transients, slow increase and decrease in amplitude at the onset and cessation of these stimuli. CM-responses to 60-61 kHz tone bursts show a prominent input-output non-linearity and transients. Accordingly, a summated response of primary auditory neurones (N1) appears not only at the onset of the stimuli, but also at the cessation. N1-off is sharply tuned at 60-61 kHz, while N1-on is tuned at 63-64 kHz, which is 2 kHz higher than the best frequency of the auditory system because of the envelope-distortion originating from sharp mechanical tuning. Single peripheral neurones sensitive to 61-62 kHz sounds have an unusually sharp tuning curve and show phase-locked responses to beats of up to 3 kHz. Information about the frequencies of Doppler-shifted echoes is thus coded by a set of sharply tuned neurones and also discharges phase-locked to beats. Neurones with a best frequency between 55 and 64 kHz show not only tonic on-responses but also off-responses which are apparently related to the mechanical off-transient occuring in the inner ear and not to a rebound from neural inhibition.