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PubMed1976

Disproportionate tonotopic representation for processing CF-FM sonar signals in the mustache bat auditory cortex.

The extent of cortical representation of the peripheral sensory field depends on its importance for species behavior. The orientation sound of the mustache bat (Pteronotus parnellii rubiginosus) invariably consists of long constant-frequency and short frequency-modulated components and is indispensable for its survival. A disproportionately large part of the auditory cortex of this bat is occupied by neurons processing the predominant components in the orientation signal and Doppler-shifted echoes. This disproportionate cortical representation related to features of biologically significant signals is comparable to that in the somatosensory and visual systems in many mammals, but it has not previously been observed in the auditory system.

Action Potentials↗
PubMed2003

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Animals↗
PubMed2005

Duration selectivity of neurons in the inferior colliculus of the big brown bat: tolerance to changes in sound level.

At and above the level of the inferior colliculus (IC), some neurons respond maximally to a limited range of sound durations, with little or no excitatory response to durations outside of this range. Such neurons have been termed "duration tuned" or "duration selective." In this study we examined the effects of varying signal amplitude on best duration, width of tuning, and first spike latency of duration tuned neurons in the IC of the big brown bat, Eptesicus fuscus. Response areas as a function of stimulus duration and intensity took a variety of forms, including open (V-shaped), narrow and level tolerant (U-shaped), or closed (O-shaped). The majority (82%) of duration tuned neurons had narrow U-shaped or O-shaped duration response areas. Those with narrow U-shaped response areas retained their duration tuning across a broad dynamic range, < or = 50 dB above threshold, whereas those with O-shaped response areas were narrowly tuned to both stimulus duration and amplitude. For about one-half (55%) of the neurons with either a U- or O-shaped response areas, best duration (BD) changed by <1 ms across the range of suprathreshold amplitudes tested. Changes in BD most often took the form of a shift to slightly shorter durations as stimulus level increased. For the majority (65%) of U- and O-shaped neurons, 50% width of duration tuning changed by <2 ms with increasing amplitude. Latency of response at BD remained stable across changes in sound level, suggesting that the relative strengths of excitatory and inhibitory inputs to duration tuned neurons remain in balance over a wide dynamic range of sound pressure levels.

Acoustic Stimulation↗
PubMed2005

Differing roles of inhibition in hierarchical processing of species-specific calls in auditory brainstem nuclei.

Here we report on response properties and the roles of inhibition in three brain stem nuclei of Mexican-free tailed bats: the inferior colliculus (IC), the dorsal nucleus of the lateral lemniscus (DNLL) and the intermediate nucleus of the lateral lemniscus (INLL). In each nucleus, we documented the response properties evoked by both tonal and species-specific signals and evaluated the same features when inhibition was blocked. There are three main findings. First, DNLL cells have little or no surround inhibition and are unselective for communication calls, in that they responded to approximately 97% of the calls that were presented. Second, most INLL neurons are characterized by wide tuning curves and are unselective for species-specific calls. The third finding is that the IC population is strikingly different from the neuronal populations in the INLL and DNLL. Where DNLL and INLL neurons are unselective and respond to most or all of the calls in the suite we presented, most IC cells are selective for calls and, on average, responded to approximately 50% of the calls we presented. Additionally, the selectivity for calls in the majority of IC cells, as well as their tuning and other response properties, are strongly shaped by inhibitory innervation. Thus we show that inhibition plays only limited roles in the DNLL and INLL but dominates in the IC, where the various patterns of inhibition sculpt a wide variety of emergent response properties from the backdrop of more expansive and far less specific excitatory innervation.

Acoustic Stimulation↗
PubMed2004

Interaural level difference processing in the lateral superior olive and the inferior colliculus.

Interaural level differences (ILDs) provide salient cues for localizing high-frequency sounds in space, and populations of neurons that are sensitive to ILDs are found at almost every synaptic level from brain stem to cortex. These cells are predominantly excited by stimulation of one ear and predominantly inhibited by stimulation of the other ear, such that the magnitude of their response is determined in large part by the intensities at the 2 ears. However, in many cases ILD sensitivity is also influenced by overall intensity, which challenges the idea of unambiguous ILD coding. We investigated whether ambiguity is reduced from one synaptic level to another for 2 centers in the so-called ILD processing pathway. We recorded from single cells in the free-tailed bat lateral superior olive (LSO), the first station where ILDs are coded, and the central nucleus of the inferior colliculus (ICC), which receives a strong projection from the LSO, as well as convergent projections from many other auditory centers. We assessed effects of overall intensity by comparing ILD functions generated with different fixed intensities to the excitatory ear. LSO cells were characterized by functions that shifted in a systematic manner with increasing intensity to the excitatory ear. In contrast, significantly more ICC cells had functions that were stable across overall sound intensity, indicating that hierarchical transformations increase stability. Furthermore, a population analysis based on proportion of active cells indicated that stability in the ICC was greatly enhanced when overall population activity was considered.

Acoustic Stimulation↗
PubMed1983

Frequency and amplitude representations in anterior primary auditory cortex of the mustached bat.

The orientation sound emitted by the Panamanian mustached bat, Pteronotus parnellii rubiginosus, consists of four harmonics. The third harmonic is 6-12 dB weaker than the predominant second harmonic and consists of a long constant-frequency component (CF3) at about 92 kHz and a short frequency-modulated component (FM3) sweeping from about 92 to 74 kHz. Our primary aim is to examine how CF3 and FM3 are represented in a region of the primary auditory cortex anterior to the Doppler-shifted constant-frequency (DSCF) area. Extracellular recordings of neuronal responses from the unanesthetized animal were obtained during free-field stimulation of the ears with pure tones. FM sounds, and signals simulating their orientation sounds and echoes. Response properties of neurons and tonotopic and amplitopic representations were examined in the primary and the anteroventral nonprimary auditory cortex. In the anterior primary auditory cortex, neurons responded strongly to single pure tones but showed no facilitative responses to paired stimuli. Neurons with best frequencies from 110 to 90 kHz were tonotopically organized rostrocaudally, with higher frequencies located more rostrally. Neurons tuned to 92-94 kHz were overpresented, whereas neurons tuned to sound between 64 and 91 kHz were rarely found. Consequently a striking discontinuity in frequency representation from 91 to 64 kHz was found across the anterior DSCF border. Most neurons exhibited monotonic impulse-count functions and responded maximally to sound pressure level (SPL). There were also neurons that responded best to weak sounds but unlike the DSCF area, amplitopic representation was not found. Thus, the DSCF area is quite unique not only in its extensive representation of frequencies in the second harmonic CF component but also in its amplitopic representation. The anteroventral nonprimary auditory cortex consisted of neurons broadly tuned to pure tones between 88 and 99 kHz. Neither tonotopic nor amplitopic representation was observed. Caudal to this area and near the anteroventral border of the DSCF area, a small cluster of FM-FM neurons sensitive to particular echo delays was identified. The responses of these neurons fluctuated significantly during repetitive stimulation.

Animals↗
PubMed1985

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↗
PubMed1986

Biosonar signals and cerebellar auditory neurons of the mustached bat.

In the vermis (VIp, VIIa, VIIp, and VIII), crus, and paraflocculus of unanesthetized mustached bats Pteronotus parnellii parnellii, responses of single neurons to acoustic stimuli were studied. The stimuli delivered were constant-frequency (CF) tones, frequency-modulated (FM) sounds, noise bursts (NBs), and sounds similar to the orientation sounds (pulses) of the species and echoes. The effect of ablation of the cerebellar cortex on vocalization was also investigated to explore whether the cerebellum was involved in sound emission. In the cerebellum of the mustached bat, auditory neurons are predominantly tuned to frequencies within the bands between 23 and 30, 55 and 63, or 85 and 94 kHz, which are found in the first, second, and third harmonics of bat's biosonar signals, respectively. The first harmonic is represented in the paraflocculus. The second harmonic is represented in vermis VIp and VIIa and crus I and IIa. The third harmonic is mainly represented in vermis VIIp and crus IIp. Different lobules represent different frequencies, but there is no systematic tonotopic representation in each lobule. The resting frequency of the CF component of the second harmonic (CF2) of the pulse differs among bats. The majority of auditory neurons in vermis VIp and VIIa and crus IIa are tuned to the CF2 frequency of the bat's own pulse. The frequency-tuning curves of cerebellar neurons are broader than those of peripheral neurons, reflected in significantly lower quality factors of Q-10, -30, and -50 dBs. In vermis VIp and VIIa, there are tiny clusters of FM-FM and CF/CF combination-sensitive neurons. They show strong facilitation of responses when two FM or CF sounds are delivered with particular relationships in the frequency, amplitude, and time domains. Because the clusters of these combination-sensitive neurons in the cerebellum are so small, we found no sign of a systematic representation of certain acoustic parameters, unlike that found in the auditory cortex. In vermis VIp and VIIa, there is a large cluster of NB-sensitive neurons that are more sensitive to NBs than to CF tones. The wider the bandwidth of the NBs, the better are the responses of these NB-sensitive neurons. The ablation of the vermis (VIp, VIIa, and VIIp), crus, and paraflocculus increases the variation of the CF frequency of the pulse. The ablation of the crus and paraflocculus causes a clear increase in the variation of CF frequency. The ablation of vermis (VIp, VIIa, and VIIp) has only a small effect on the variation. Any of the above ablations has little effect on the repetition rate of the pulse emission and the duration of pulses.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed1990

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↗
PubMed1990

Delay-tuned neurons in auditory cortex of mustached bat are not suited for processing directional information.

1. The mustached bat, Pteronotus parnellii parnellii, emits bisonar pulses each consisting of eight components: CF1-4 and FM1-4. In the auditory cortex of the bat there are arrays of FM-FM neurons that are tuned to particular delays of echo FMn (n = 2, 3, or 4) from pulse FM1. They are specialized for the processing of target-range information. The FM signal is suited for ranging and also for target localization. Therefore we studied the directional sensitivity of FM-FM neurons with pulse FM1 and echo FMn. One of the FM1-FMn pair was moved around the bat's head while the other was fixed in front of the bat. 2. FM-FM neurons are sharply tuned in echo delay and are broadly tuned in echo amplitude. That is, they are tuned to a target that has a particular cross-sectional area and that is located at a particular distance from the bat. Their best amplitudes for echoes range between 8 and 73 dB sound pressure level (SPL). The best amplitude is approximately 30 dB higher than minimum threshold in the majority of neurons. 3. The higher the best amplitude is relative to minimum threshold, the larger the receptive field is at the best amplitude. The receptive field of FM-FM neurons at 30 dB above minimum threshold is always so large that it covers the entire contralateral auditory field or the entire contralateral field and the medial half of the ipsilateral auditory field. The large size of the receptive field and the uniform distribution of response magnitudes within the receptive field indicate that FM-FM neurons are not suited for sound localization. Directional information is probably processed in parallel by a separate population of neurons other than FM-FM neurons. 4. The receptive field of FM-FM neurons at 10 dB above minimum threshold is much smaller than that at 30 dB above minimum threshold, but it is still large. The mean azimuthal and elevational widths for echo FMn are greater than 70 degrees in all directions. There is no sign that FM-FM neurons are more directional than peripheral neurons. Furthermore, there is neither an azimuthal nor an elevational axis within the FM-FM area. 5. Mean best azimuths of FM-FM neurons are different for each echo FM harmonic: lateral 35 degrees for FM2 and lateral 19 degrees for FM3 and FM4.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation↗
PubMed1990

Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation.

1. The biosonar signal (pulse) of the mustached bat, Pteronotus parnellii parnellii, has four harmonics (H1-4), each consisting of a long constant-frequency component (CF1-4) followed by a short frequency-modulated component (FM1-4). As the bat approaches a target, it systematically modifies its pulses to optimize the extraction of information from the echoes. These behavioral responses include 1) Doppler-shift (DS) compensation in which the bat adjusts the frequency of its pulses to correct for the DS in the echoes. This maintains the echo CF2 at a frequency to which the bat's cochlea is very sharply tuned, slightly above the CF2 frequency of the bat's pulses when it is at rest (Frest, approximately 61 kHz); 2) echo intensity compensation, in which the bat lowers its pulse intensity as it approaches a large target, thus maintaining the echo intensity within a suitable range for auditory processing; and 3) and 4) duration and rate adjustments, in which the bat first increases its pulse duration to facilitate target identification, then shortens its pulse duration while increasing its pulse rate to facilitate target analysis. 2. We examined these responses, especially DS compensation, by swinging bats on a pendulum toward a large target over a distance of 3.6 m. Eight bats were given 15-30 swings per day for 6-25 days. 1) On 97% of all swings the bats showed strong DS compensation as the pendulum approached the target. They did not show DS compensation on the backswing. 2) On 40-50% of all swings, the bats clearly displayed the other responses. The bats typically increased their pulse intensity a small amount early in the pendulum swing, then decreased pulse intensity by as much as 18 dB as the target was more closely approached. They increased their pulse intensity during the backswing. 3) Pulse duration increased from approximately 20 to 23 ms early in the forward swing, decreased to approximately 18 ms as the target was more closely approached, and then increased to 20 ms by the end of the backswing. 4) The instantaneous repetition rate increased from approximately 17 pulses/s at the start of the forward swing to approximately 28 pulses/s near the target, then decreased to approximately 10 pulses/s by the end of the backswing. Pulses usually occurred in trains of 1-2 pulses, with longer trains occasionally occurring near the target. 3. The maximum DS on the pendulum was 1.34 kHz, and the maximum DS compensation was 146 +/- 98 (SD) Hz less than this value.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗