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Z M Fuzessery

Publications and source records attributed to Z M Fuzessery.

15 recordsLinked to original sources

Single cortical neurons serve both echolocation and passive sound localization.

The pallid bat uses passive listening at low frequencies to detect and locate terrestrial prey and reserves its high-frequency echolocation for general orientation. While hunting, this bat must attend to both streams of information. These streams are processed through two parallel, functionally specialized pathways that are segregated at the level of the inferior colliculus. This report describes functionally bimodal neurons in auditory cortex that receive converging input from these two pathways. Each brain stem pathway imposes its own suite of response properties on these cortical neurons. Consequently, the neurons are bimodally tuned to low and high frequencies, and respond selectively to both noise transients used in prey detection, and downward frequency modulation (FM) sweeps used in echolocation. A novel finding is that the monaural and binaural response properties of these neurons can change as a function of the sound presented. The majority of neurons appeared binaurally inhibited when presented with noise but monaural or binaurally facilitated when presented with the echolocation pulse. Consequently, their spatial sensitivity will change, depending on whether the bat is engaged in echolocation or passive listening. These results demonstrate that the response properties of single cortical neurons can change with behavioral context and suggest that they are capable of supporting more than one behavior.

Animals

Acute sensitivity to interaural time differences in the inferior colliculus of a bat that relies on passive sound localization.

Gleaning bats rely on passive hearing to detect and localize terrestrial prey, and display remarkable accuracy in their passive sound localization. This study examines binaural processing in the inferior colliculus (IC) of the pallid bat (Antrozous pallidus), a gleaner that attends to prey-generated noise transients to locate prey. The primary focus is to determine whether neurons in its lateral IC, a region that appears dedicated to passive localization, possess a level of sensitivity to interaural time difference (ITD) sensitivity sufficient to indicate the use of ITDs in sound localization. Such a sensitivity was suspected because the pallid bat is capable of very accurate passive sound localization at the lower end of its audible range, where interaural intensity differences (IIDs) are small and may not provide sufficient spatial information. Because the pallid bat's audible range is too high for neurons to phase-lock to carrier frequencies, neurons were tested with square-wave, amplitude-modulated tones and noise to determine their sensitivity to ITDs in the sound envelope. Their sensitivity to the bat's behaviorally relevant ITD range of +/- 70 micros, and their low average interaural time/ intensity trading ratios (18 micros/dB) suggest that the pallid bat IC may have the greatest ITD sensitivity reported in a high-frequency mammalian auditory system.

Acoustic Stimulation

Monaural and binaural spectral cues created by the external ears of the pallid bat.

The acoustic properties of external ears transform the spectra of incident sound in a location-dependent manner, and provide monaural and binaural spectral information used in 2-dimensional localization. Human studies suggest that binaural spectral differences, and spectral peaks and notches in monaural transfer functions, may all provide spatial information. This study examined the acoustic properties of the pallid bat ear to determine directionality, interaural intensity differences spectral peaks and notches in transfer functions, as well as acoustic gain. The pallid bat is a gleaning bat that uses passive sound localization to find prey, and echolocation for general orientation. It is capable of very accurate passive sound localization, and the primary focus of this study was to determine the spectral cues that might support this localization acuity. Results show that the external ears of this bat create spectral maxima and minima that vary systematically with azimuth and elevation. The monaural spectral cues resemble those reported in humans and cats and suggest that similar spectral cues are used across taxa. The ears also create robust interaural spectral differences that vary systematically with both sound azimuth and elevation. These monaural and binaural spectral cues may provide the basis for the 1 degrees angular resolution apparent in it this bat's passive sound localization performance.

Acoustic Stimulation

Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus.

1. We examined the role of gamma-aminobutyric acid (GABA)-mediated inhibition in shaping excitatory tuning curves and creating selectivity for frequency-modulated (FM) sweeps in 29 neurons in the central nucleus of the inferior colliculus (ICC) of the pallid bat, with the use of single-unit recording coupled with the iontophoretic application of bicuculline methiodide (BIC), an antagonist of GABAA receptors. 2. BIC increased response magnitude 2 to 6 times over pretreatment levels in > 80% of neurons tested, and converted > 50% of nonmonotonic intensity-rate functions to monotonic or plateaued functions, demonstrating that GABAergic input normally limited response magnitude and inhibited responses at higher intensities. BIC typically had little effect on response thresholds, except in more specialized neurons that normally responded poorly to tones. In these cases, BIC disinhibited the neurons' responses to tones and lowered excitatory thresholds as much as 25 dB. 3. We examined the effects of BIC application on both excitatory and inhibitory tuning curves (measured with simultaneous 2-tone inhibition) to determine whether inhibitory curves were GABA mediated and whether removal of this inhibition was accompanied by an expansion of the excitatory curve. BIC had variable effects on the width of excitatory curves. In most cases, excitatory curves were at least slightly broadened, and expanded into regions previously occupied by inhibitory curves. In most cases, excitatory curves were at least slightly broadened, and expanded into regions previously occupied by inhibitory curves. However, in a few cases, inhibitory curves could be eliminated without an expansion of the excitatory curve. The greatest effect was seen in neurons with closed excitatory tuning curves; blocking GABAergic input caused the curves to open, allowing the neurons to respond at higher intensities. 4. Approximately 50% of the neurons in the ICC tuned to the spectrum of the bat's downward FM sweeping biosonar pulse respond preferentially to downward FM sweeps and not to upward sweeps, tones, or noise. In all neurons tested, BIC at least partially destroyed selectivity for sweep direction. This destruction could occur, however, without a loss of response exclusivity; in some cases, the neurons still did not respond to tones or noise. These results suggest that response selectivity for a species-specific signal is created by GABAergic input to ICC neurons. These results are used to suggest a mechanism that creates selectivity for FM sweep direction.

Acoustic Stimulation

Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus.

1. While hunting, the pallid bat uses passive sound localization at low frequencies to find terrestrial prey, and echolocation for general orientation. It must therefore process two different types of acoustic input at the same time. The pallid bat's echolocation pulse is a downward frequency-modulated (FM) sweep from 60 to 30 kHz. This study examined the response selectivity of single neurons in the pallid bat's central nucleus of the inferior colliculus (ICC) for FM sweeps, comparing the response properties of the high-frequency population, tuned to the biosonar pulse, with the low-frequency population, tuned below the pulse. The working hypothesis was that the high-frequency population would exhibit a response selectivity for downward FM sweeps that was not present in the low-frequency population. 2. Neurons were tested for their selectivity for FM sweep direction, duration, frequency range and bandwidth, and rate of frequency change. The extent to which they responded exclusively to tones, noise, and FM sweeps was also examined. Significant differences in the response properties of neurons in the two populations were found. In the low-frequency population, all neurons responded to tones, but only 50% responded to FM sweeps. Only 23% were selective for sweep direction. In the high-frequency population, all neurons responded to FM sweeps, but 31% did not respond to tones. Over one-half of this population was selective for sweep direction, and of those that were selective, all preferred the downward sweep direction of the biosonar pulse. A large percentage (31%) responded exclusively to downward sweeps, and not to tones or upward sweeps. None of the cells in either population responded to noise, or did so only at very high relative thresholds. 3. Both populations contained neurons that were selective for short stimulus durations that approximated the duration of the biosonar pulse, although the percentage was greater in the high-frequency population (58% vs. 20%). In the high-frequency population, 31% of the neurons tested for duration responded exclusively to both the sweep direction and duration of the biosonar pulse. 4. Downward FM-selective neurons, with one exception, were generally insensitive to the rate of frequency change of the FM sweep, as well as the frequency range and bandwidth of the sweep. They responded similarly to both the full 60- to 30-kHz sweep and to 5-kHz bandwidth portions of the full sweep.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Passive sound localization of prey by the pallid bat (Antrozous p. pallidus).

The pallid bat (Antrozous p. pallidus) uses passive sound localization to capture terrestrial prey. This study of captive pallid bats examined the roles of echolocation and passive sound localization in prey capture, and focused on their spectral requirements for accurate passive sound localization. Crickets were used as prey throughout these studies. All tests were conducted in dim, red light in an effort to preclude the use of vision. Hunting performance did not differ significantly in red light and total darkness, nor did it differ when visual contrast between the terrestrial prey and the substrate was varied, demonstrating that the bats did not use vision to locate prey. Our bats apparently used echolocation for general orientation, but not to locate prey. They did not increase their pulse emission rate prior to prey capture, suggesting that they were not actively scanning prey. Instead, they required prey-generated sounds for localization. The bats attended to the sound of walking crickets for localization, and also attacked small, inanimate objects dragged across the floor. Stationary and/or anesthetized crickets were ignored, as were crickets walking on substrates that greatly attenuated walking sounds. Cricket communication sounds were not used in prey localization; the bats never captured stationary, calling crickets. The accuracy of their passive sound localization was tested with an open-loop passive sound localization task that required them to land upon an anesthetized cricket tossed on the floor. The impact of a cricket produced a single 10-20 ms duration sound, yet with this information, the bats were able to land within 7.6 cm of the cricket from a maximum distance of 4.9 m. This performance suggests a sound localization accuracy of approximately +/- 1 degree in the horizontal and vertical dimensions of auditory space. The lower frequency limit for accurate sound localization was between 3-8 kHz. A physiological survey of frequency representation in the pallid bat inferior colliculus suggests that this lower frequency limit is around 5 kHz.

Animals

Spatial processing within the mustache bat echolocation system: possible mechanisms for optimization.

1. The directionality of an echolocation system is determined by the acoustic properties of both the emitter and receiver, i.e., by the radiation pattern of the emitted pulse and the directionally of the external ears. We measured the directionality of the echolocation system of the greater mustache bat (Pteronotus parnellii) at the 30 kHz, 60 kHz and 90 kHz harmonics of its echolocation pulse by summing, at points throughout the frontal sound field, the echo attenuation due to the spread of pulse energy and the attenuation due to the spread of pulse energy and the attenuation due to the directionality of its external ears. The pulse radiation pattern at the 3 harmonics was measured by comparing the output of a microphone moved throughout the frontal sound field against a second reference microphone at the center of the field. External ear directionality at the 3. harmonics was measured by presenting free-field sounds throughout the frontal sound field, and recording the intensity thresholds of cochlear microphonic potentials, and the intensity thresholds of monaural neurons in the inferior colliculus tuned to one of the 3 harmonics. 2. When compared with ear directionality, the echolocation system was found to be more directional for the center of the sound field in several respects. At all harmonics, attenuation of sounds originating in the peripheral part of the field was increased by 10 to 13 dB. Areas of maximum sound intensity contracted toward the center of the field. Also, the isointensity contours of the echolocation system were more radially symmetrical about the center of the field. 3. At 60 kHz, sound intensity along the azimuth within the echolocation system was nearly constant 26 degrees to either side of the center of the field. This suggests that the radiation pattern of the echolocation pulse and the directionality of the external ears complement one another to produce an acoustic environment at the center of the sound field in which stimulus intensity is stabilized to allow more effective analysis of various aspects of the echolocation target. In particular, we suggest that this intensity stabilization may allow the bat to more effectively resolve the interaural intensity differences it uses to localize prey. 4. Predictions of the azimuthal spatial tuning of binaurally sensitive neurons in the inferior colliculus within the echolocation system were compared with their spatial tuning when only ear directionality is considered.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation

A microcomputer-controlled system for use in auditory physiology.

This report describes a digitally controlled system for use in auditory physiology in which signal generation and data acquisition are under the control of a single microcomputer. The system is designed to generate the complex waveforms required in neuroethological studies, and is able to generate these signals at frequencies of up to 160 kHz with a resolution of 1 Hz. The system is built around a commercially available digital hardware system, and augmented with custom components to enhance operation speed, precision and flexibility.

Hearing

Determinants of horizontal sound location selectivity of binaurally excited neurons in an isofrequency region of the mustache bat inferior colliculus.

1. The monaural and binaural response properties and the horizontal sound location sensitivity of 78 binaurally excited neurons from 26 bats were examined with a combined closed-field and free-field stimulation paradigm. The aim was to determine how the response properties of these neurons shape their selectivity for auditory space. All neurons were recorded within a single, greatly enlarged isofrequency (60 kHz) region of the mustache bat's central nucleus of the inferior colliculus (ICC). In this and two companion papers (Wenstrup et al. 1988a,b) that focused on binaurally inhibited neurons in this isofrequency region, our goal was to examine the neural mechanisms for binaural processing within a single frequency channel of the primary auditory system. 2. Binaurally excited neurons were defined as either excited by monaural input from both ears or, if excited by monaural stimulation of only one ear, facilitated by binaural stimulation. Some neurons also exhibited binaural inhibition. These neurons were divided into functional classes based on their responses to monaural and binaural stimulation presented under dichotic, closed-field conditions. The following notation was used: response to contralateral stimulation (E, excitatory; O, no effect), response to ipsilateral stimulation (E, excitatory; O, no effect)/response to binaural stimulation (F, facilitatory; I, inhibitory; O, no effect). Seven functional classes were observed: EE/O, EE/F, EE/I, EE/FI, EO/F, EO/FI, and OO/F. 3. Among EE neurons, thresholds for contralateral monaural stimulation were typically lower than for ipsilateral stimulation, and response magnitudes for contralateral stimulation were typically greater. Among EO/F and EO/FI neurons, only one eye, an OE/FI neuron, was excited by ipsilateral monaural stimulation. These results suggest that contralateral input provides the dominant excitatory influence. EE/FI and EO/FI neurons, which exhibited both binaural facilitation and inhibition, were typically inhibited at interaural intensity differences (IIDs) favoring the ipsilateral ear, suggesting that ipsilateral input provides the dominant inhibitory influence. 4. Neurons were tested over the range of naturally occurring IIDs (+/- 30 dB) at intensities of -20 to 30 dB relative to threshold. The IID functions of these neurons assumed three configurations: flat, with facilitation occurring at all IIDs; stepped, with facilitation occurring over part of the IID range, and peaked, with facilitation occurring over a limited band of IIDs. The majority of cells (90%) exhibited peaked IID functions, and most of these (73%), regardless of functional class, were maximally facilitated at an IID of 0 dB. 5. Neurons differed considerably in the strength of their binaural interactions.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials

Binaural neurons in the mustache bat's inferior colliculus. I. Responses of 60-kHz EI units to dichotic sound stimulation.

1. Single-unit responses to closed-field, dichotic sound stimuli were obtained from EI neurons in the mustache bat's inferior colliculus; these neurons are excited by sound to the contralateral ear and inhibited by sound to the ipsilateral ear. All units were tuned to the 60-kHz component of the bat's sonar signal. The goal of the study was to describe basic features of the sensitivity to interaural intensity differences (IIDs) and sound intensity among an isofrequency population of EI neurons. The following paper describes how these features of IID sensitivity shape the response to free-field sounds. 2. Three features of IID sensitivity were considered. The inhibitory threshold (Figs. 1 and 2) described the IID at which inhibitory effects became pronounced; it was defined as the IID at which the excitatory response to contralateral sound was suppressed by 50%. Most units (68%) were inhibited at positive IID values, for which the ipsilateral (inhibitory) sound was more intense. The maximum inhibition (Figs. 1 and 3) described the strength of ipsilateral inhibition; it was defined as the percent that each unit was inhibited below its response to monaural stimulation of the contralateral ear. The majority of units (58%) were almost totally suppressed by a sufficiently intense ipsilateral sound. The IID range (Figs. 1 and 4) described the sharpness or slope of the IID cutoff; it was defined as the IID range over which the response changed from nearly unsuppressed (80% of maximum response) to near maximum suppression (20% of maximum response). Most units (71%) had IID ranges of less than or equal to 15 dB. 3. A significant correlation between the inhibitory threshold and the maximum inhibition (Fig. 5) among the sample of EI units suggests that some common neural mechanisms underlie these features of IID sensitivity. 4. The response of EI neurons to binaural stimuli was a function of sound intensity as well as IID (Fig. 7). In part, this resulted from intensity-dependent changes in properties of binaural inhibition. For most units, basic measures of IID sensitivity changed to a limited extent as the sound intensity changed.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation

Binaural neurons in the mustache bat's inferior colliculus. II. Determinants of spatial responses among 60-kHz EI units.

1. The responses to closed-field and free-field sound stimuli were obtained from EI neurons in the 60-kHz isofrequency representation of the mustache bat's inferior colliculus. The goals of the study were 1) to examine how binaural interactions and the directional properties of the ear shape the spatial response of 60-kHz EI neurons and 2) to examine features of the spatial responses of these isofrequency neurons which may encode the location of a sound. 2. The free-field response of monaural neurons was used to describe directional effects of the head and external ears at 60 kHz. Monaural neurons were most sensitive to sounds originating 26 degrees into the contralateral field, with sharply reduced sensitivity in the ipsilateral field and the lateral extreme of the contralateral field. The interaural intensity difference (IID), computed by assuming that the ears had mirror-image directional sensitivities, was greatest for sounds between 26 and 52 degrees off the vertical midline, where IIDs typically ranged from 20 to 30 dB. These values agree well with previous measures of the directional sensitivity of the ear obtained from cochlear microphonic recordings. 3. The response of a monaural unit to closed-field stimulation was used to predict its response to free-field stimulation. This prediction agreed closely with the observed free-field response, indicating that the monaural unit's free-field response could be explained by the directional sensitivity of the contralateral ear and the unit's response as a function of contralateral sound intensity. 4. EI neurons differed in basic features of their binaural response properties, as described in a companion paper. To examine how these features of binaural inhibition shaped spatial responses, we obtained responses to free-field sounds among neurons whose binaural properties had been thoroughly characterized. We then compared the spatial response to a prediction based upon the directional properties of the ear and the sensitivity of the EI neurons to IIDs and intensity. The close agreement between the observed and predicted spatial responses in 11 of 12 EI units indicated that the spatial responses were determined largely by sensitivity to IIDs and intensity and by the directional properties of the ear. 5. EI neurons in our sample were most sensitive, and responded best, to sounds originating 26-39 degrees into the contralateral field. These spatial response features were independent of the binaural properties of EI neurons. Instead, they depended upon the directional properties of the ears at 60 kHz.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation

Speculations on the role of frequency in sound localization.

This presentation reviews behavioral and physiological evidence suggesting that the perceived power spectrum of a sound, as modified by the external ears, provides important cues for horizontal and vertical sound localization. This spatial information is mostly likely encoded by the relative levels of excitation among the tonotopically organized hair cells of the cochlea. This suggests that the preservation of the cochlear frequency map within the central auditory system contributes an anatomical substrate for the localization of sound.

Animals

A representation of horizontal sound location in the inferior colliculus of the mustache bat (Pteronotus p. parnellii).

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.

Animals

Determinants of sound location selectivity in bat inferior colliculus: a combined dichotic and free-field stimulation study.

This study of the neural representation of sound location in the bat Pteronotus parnellii describes how the peripheral and central components of its auditory system shape the horizontal and vertical spatial selectivity of single neurons in the inferior colliculus. Pteronotus extracts spatial information from the echoes of an emitted pulse composed of four constant-frequency harmonics (30, 60, 90, and 120 kHz), each terminated by a downward frequency sweep. To quantify the intensity cues available in the echo, cochlear microphonic response thresholds were used to measure the directional selectivity of the ear and the interaural intensity level disparities (IIDs) created between ears at standardized speaker positions in the bat's frontal sound field, at frequencies in the pulse spectrum. Speaker positions where thresholds were lowest were termed the sensitive area (SA) of the ear. Positions where IID values were greater than 10 dB were termed the difference area (DA). Ear directionality exhibited a pronounced frequency dependence, both in terms of the degree of directional selectivity and the position of the SA. At the 30-kHz harmonic of the pulse, the ear was broadly directional; the SA covered most of the lower half of the ipsilateral field. The ear was highly directional at the 60- and 90-kHz harmonics. Also, the vertical position of the SA changed dramatically between 60 and 90 kHz, from the horizontal midline at 60 kHz to 40 degrees below the midline at 90 kHz. The positions of the DAs also showed a pronounced frequency dependence. The 30-kHz DA was restricted to the extreme lateral part of the frontal sound field. The 60- and 90-kHz DAs were located in the same positions as the equivalent SAs and exhibited the same difference in vertical position. The DAs of the pulse harmonics differ in both their horizontal and vertical positions; the ears thus generate pronounced binaural spectral cues, which provide two-dimensional spatial information. In the inferior colliculus, a combined paradigm of closed-field dichotic stimulation, followed by free-field stimulation, was used to document the frequency tuning and binaural response properties of single neurons and to correlate these properties with the neuron's horizontal and vertical spatial selectivity in the frontal sound field. Where a neuron responded to free-field stimulation at the lowest intensity is termed its SA. A neuron's frequency tuning primarily influenced its degree of spatial selectivity and its sensitivity in the vertical plane, reflecting the directional properties of the external ears at the neuron's best frequency.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Neural mechanisms of sound localization in an echolocating bat.

The mustache bat emits a three-harmonic echolocation pulse. At the external ear, large interaural intensity differences are generated only when a sound originates within a limited area of two-dimensional space, and this area is different for each pulse harmonic. As a consequence, the external ear generates pronounced binaural spectral cues containing two-dimensional spatial information. This information is encoded in the inferior colliculus by neurons tuned to one of the harmonics and sensitive to interaural intensity differences.

Acoustics