Neurons in the inferior colliculus of the big brown bat show maximal amplitude sensitivity at the best duration

The big brown bats, Eptesicus fuscus, emit ultrasonic signals and analyze the returning echoes in multi-parametric domains to extract target features. The variation of different pulse parameters during hunting predicts that analysis of an echo parameter by bats is inevitably affected by other co-varying echo parameters. In this study, we presented data to show that the bat inferior collicular (IC) neurons have maximal amplitude sensitivity at the best duration (BD). A family of rate-amplitude function (RAF) of each IC neuron is plotted with the BD and non-BD sound pulses. The RAF plotted with BD pulses has sharper slope (SL) and smaller dynamic range (DR) than the RAF plotted with non-BD pulses has. All RAFs can be described as monotonic, saturated or non-monotonic. IC neurons with monotonic RAF are mostly recorded at deeper IC and they have the largest average BD, best amplitude (BA) and DR. Conversely, IC neurons with non-monotonic RAF are mostly recorded at upper IC and they have the smallest average BD, BA and DR. Low best frequency (BF) neurons at upper IC have shorter BD, smaller BA and DR than high BF neurons at deeper IC have. These data suggest that IC neurons that tune to an echo duration also have the greatest sensitivity to echo amplitude. These data also suggest that sensitivity in frequency, duration and amplitude appears to be orderly represented along the dorso-ventral axis of the IC.     

Encoding repetition rate and duration in the inferior colliculus of the big brown bat,Eptesicus fuscus

1. Encoding of temporal stimulus parameters by inferior collicular (IC) neurons of Eptesicus fuscus was studied by recording their responses to a wide range of repetition rates (RRs) and durations at several stimulus intensities under free field stimulus conditions. 2. The response properties of 424 IC neurons recorded were similar to those reported in previous studies of this species. 3. IC neurons were classified as low-pass, band-pass, and high-pass according to their preference for RRs and/or durations characteristic of, respectively, search, approach, or terminal phases of echolocation. These neurons selectively process stimuli characteristic of the various phases of hunting. 4. Best RRs and best durations were not correlated with either the BFs or recording depths This suggests that each isofrequency lamina is capable of processing RRs and durations of all hunting phases. 5. Responses of one half of IC neurons studied were correlated with the stimulus duty cycle. These neurons may preferentially process terminal phase information when the bat's pulse emission duty cycle increases. 6. While the stimulus RR affected the dynamic range and overall profile of the intensity rate function, only little effect was observed with different stimulus durations.     

GABAergic disinhibition changes the recovery cycle of bat inferior collicular neurons

This study examines the contribution of GABAergic inhibition to the discharge pattern and recovery properties of 110 bat inferior collicular neurons by means of bicuculline application to their recording sites. When stimulated with single pulses, 74 (67%) neurons discharged one or two impulses (phasic responders), 19 (17%) discharged three to ten impulses (phasic bursters) and 17 (16%) discharged impulses throughout the entire stimulus duration (tonic responders). Bicuculline application changed phasic responders into phasic bursters or tonic responders, increased the number of impulses by 10–2000% and shortened the response latency of most neurons. When stimulated with pairs of sound pulses, the recovery cycles of these neurons can be described as: (1) long inhibition (n = 49, 45%); (2) short inhibition (n = 41, 37%); and (3) fast recovery (n = 20, 18%) based upon the 50% recovery time that was either longer than 20 ms, between 10 and 20 ms or shorter than 10 ms. Bicuculline application shortened the 50% recovery time of most neurons by 11–2350% allowing them to respond to pairs of sound pulses at very short interpulse intervals. These data demonstrate that GABAergic inhibition contributes significantly to auditory temporal processing. Accepted: 18 April 1997     

Multiple mechanisms shape selectivity for FM sweep rate and direction in the pallid bat inferior colliculus and auditory cortex

The inferior colliculus and auditory cortex of the pallid bat contain a large percentage of neurons that are highly selective for the direction and rate of the downward frequency modulated (FM) sweep of the bat’s echolocation pulse. Approximately 25% of neurons tuned to the echolocation pulse respond exclusively to downward FM sweeps. This review focuses on the finding that this selectivity is generated by multiple mechanisms that may act alone or in concert. In the inferior colliculus, selectivity for sweep rate is shaped by at least three mechanisms: shortpass or bandpass tuning for signal duration, delayed high-frequency inhibition that prevents responses to slow sweep rates, and asymmetrical facilitation that occurs only when two tones are presented at appropriate delays. When acting alone, the three mechanisms can produce essentially identical rate selectivity. Direction selectivity can be produced by two mechanisms: an early low-frequency inhibition that prevents responses to upward sweeps, and the same asymmetrical two-tone inhibition that shapes rate tuning. All mechanisms except duration tuning are also present in the auditory cortex. Discussion centers on whether these mechanisms are redundant or complementary.     

Corticofugal regulation of auditory sensitivity in the bat inferior colliculus

Under free-field stimulation conditions, corticofugal regulation of auditory sensitivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus, was studied by blocking activities of auditory cortical neurons with Lidocaine or by electrical stimulation in auditory cortical neuron recording sites. The corticocollicular pathway regulated the number of impulses, the auditory spatial response areas and the frequency-tuning curves of inferior colliculus neurons through facilitation or inhibition. Corticofugal regulation was most effective at low sound intensity and was dependent upon the time interval between acoustic and electrical stimuli. At optimal interstimulus intervals, inferior colliculus neurons had the smallest number of impulses and the longest response latency during corticofugal inhibition. The opposite effects were observed during corticofugal facilitation. Corticofugal inhibitory latency was longer than corticofugal facilitatory latency. Iontophoretic application of γ-aminobutyric acid and bicuculline to inferior colliculus recording sites produced effects similar to what were observed during corticofugal inhibition and facilitation. We suggest that corticofugal regulation of central auditory sensitivity can provide an animal with a mechanism to regulate acoustic signal processing in the ascending auditory pathway. Accepted: 15 July 1998     

Coding of sinusoidally amplitude modulated acoustic stimuli in the inferior colliculus of the rufous horseshoe bat,Rhinolophus rouxi

Summary Single neuron responses to sinusoidally amplitude modulated (SAM) signals were studied in the inferior colliculus of the horseshoe bat,Rhinolophus rouxi.57% of the neurons responded to SAM stimuli with periodical discharges synchronized to the modulation cycle. The proportion of cells driven by amplitude modulated signals was independent of the best frequency of the neurons. Best modulation frequencies were at or below 100 Hz in about 70% of the neurons. Synchronized activity could be elicited by modulation frequencies up to 400 Hz.Best SAM responses were observed at stimulus intensities 10 dB above threshold. Generally the BMF of a neuron did not change with intensity. The BMF decreased with decreasing modulation depth of the amplitude modulation.A trend for a topographical organization of neurons according to best modulation frequencies was detected. The results did not reveal any significant specialization of the bat's auditory system for coding of amplitude modulations as compared to other mammals.Abbreviations BF best frequency - BMF best modulation frequency - CF constant frequency - FM frequency modulation - IC inferior colliculus - SAM sinusoidal amplitude modulation - SFM sinusoidal frequency modulation     

Temporally patterned pulse trains affect duration tuning characteristics of bat inferior collicular neurons

 This study examines the effect of temporally patterned pulse trains on duration tuning characteristics of inferior collicular neurons of the big brown bat, Eptesicus fuscus, under free-field stimulation conditions. Using a 50% difference between maximal and minimal responses as a criterion, the duration tuning characteristics of inferior collicular neurons determined with pulse trains of different pulse durations are described as band-pass, long-pass, short-pass, and all-pass. Each band-pass neuron discharged maximally to a specific pulse duration that was at least 50% larger than the neuron's responses to a long- and a short-duration pulse. In contrast, each long- or short-pass neuron discharged maximally to a range of long- or short-duration pulses that were at least 50% larger than the minimal responses. The number of impulses of an all-pass neuron never differed by more than 50%. When pulse trains were delivered at different pulse repetition rates, the number of short-pass and band-pass neurons progressively increased with increasing pulse repetition rates. The slope of the duration tuning curves also became sharper when determined with pulse trains at high pulse repetition rates. Possible mechanisms underlying these findings are discussed. Accepted: 25 August 1999     

The inferior colliculus of the mustached bat has the frequency-vs-latency coordinates

In the mustached bat, the central auditory system contains FM–FM (delay-tuned) neurons which are specialized for processing target-distance information carried by echo delays. Mechanisms for creating the FM–FM neurons involve delay lines, coincidence detection and amplification. A neural basis for delay lines can be a map representing response latencies. The aim of the present study is to explore whether the central nucleus of the inferior colliculus has a latency axis incorporated into iso-best frequency slabs. Responses of single or multiple neurons were recorded from the inferior colliculus of unanesthetized mustached bats with tungsten-wire electrodes, and their response latencies were measured with tone bursts at their best frequencies and best amplitudes or 65 dB SPL. In the dorsoventral electrode penetrations across the inferior colliculus, response latency systematically shortens from ˜12 to ˜4␣ms. Tonotopic representation in the inferior colliculus is somewhat complex. Iso-best frequency slabs are tilted and/or curved, but they orient more or less ventrodorsally. Nevertheless, the latency axis is evident in each iso-best frequency slab, regardless of best frequency. The inferior colliculus has the frequency-vs-latency coordinates. Accepted: 2 October 1996     

The influence of stimulus duration on the delay tuning of cortical neurons in the FM bat,Myotis lucifugus

1. Echolocating bats use echo delay as the primary cue to determine target distance. During target-directed flight, the emitted pulses increase in repetition rate and shorten in duration as distance decreases. To determine how these parameters affect the delay tuning of neurons in the auditory cortex of the awake bat, Myotis lucifugus, we examined the responses of 104 delay-sensitive neurons as the pulse repetition rate (PRR) and duration were independently varied. Stimulus duration of 4, 2 and 1 ms and PRR of 5-100/s were used for both the pulse and echo to determine delay sensitivity. These parameter ranges span those used during the search, approach, and the initial terminal phases of echolocation. 2. As the stimulus duration was shortened, the range of PRRs for delay sensitivity was extended to higher rates in 41% of the neurons, narrowed or disappeared in 40%, and remained unchanged in 4%. The remaining 15% were not categorized since it was not possible to determine a trend in which the range of delay-sensitive PRRs changed with stimulus duration. 3. Three types of tracking neurons (i.e., neurons that change their best delay during target-directed flight) were found. For the first type, the best delay (BD) shortened with shorter stimulus duration, for the second type, BD shortened with both shorter stimulus durations and higher PRRs, and for the third type, BD shortened with higher PRRs. 4. These results suggest that the stimulus parameters of sonar emission influence delay tuning and hence processing by cortical neurons in FM bats.     

Sound duration and sound pattern affect the recovery cycles of inferior collicular neurons in leaf-nosed bat, Hipposideros armiger

The effects of sound duration and sound pattern on the recovery cycles of inferior collicular (IC) neurons in constant frequency-frequency modulation (CF-FM) bats were explored in this study. Five leaf-nosed bats, Hipposideros armiger (4 males, 1 female, 43-50 g body weight), were used as subjects. The extracellular responses of IC neurons to paired sound stimuli with different duration and patterns were recorded, and the recovery was counted as the ratio of the second response to the first response. Totally, 169 sound-sensitive IC neurons were recorded in the experiment. According to the interpulse interval (IPI) of paired sounds when neurons reached 50% recovery (50% IPI), the recovery cycles of these IC neurons were classified into 3 types: fast recovery (F, the 50% IPI was less than 15 ms), short recovery (S, the 50% IPI was between 15.1 and 30 ms) and long recovery (L, the 50% IPI was more than 30 ms). When paired CF stimuli with 2 ms duration was used, the ratio of F neurons was 32.3%, and it decreased to 18.1% and 18.2% respectively when 5 and 7 ms CF stimuli were used. The ratios of S and L neurons were 41.5%, 33.7%, 29.1% and 26.2%, 48.2%, 52.7% respectively when 2, 5 and 7 ms CF stimuli were used. The average 50% IPI determined after stimulation with paired 2 ms, 5 ms and 7 ms CF sounds were (30.2 ± 27.6), (39.9 ± 29.1) and (49.4 ± 34.7) ms, respectively, and the difference among them was significant (P< 0.01). When the stimuli of paired 2 ms CF sounds were shifted to paired 2 ms FM sounds, the proportion of F, S and L neurons changed from 32.3%, 41.5%, 26.2% to 47.7%, 24.6%, 27.7%, respectively, and the average 50% IPI decreased from (30.2 ± 27.6) to (23.9 ± 19.0) ms (P< 0.05, n = 65). When paired 5+2 ms CF-FM pulses were used instead of 7 ms CF sounds, the proportion of F, S and L neurons changed from 18.2%, 29.1%, 52.7% to 29.1%, 27.3%, 43.6%, respectively, and the average 50% IPI decreased from (49.4 ± 34.7) to (36.3 ± 29.4) ms (P< 0.05, n = 55). All these results suggest that the CF and FM components in echolocation signal of CF-FM bats play different roles during bats' hunting and preying on. The FM component of CF-FM signal presenting in the terminal phase can increase the number of F type neurons and decrease the recovery cycles of IC neurons for processing high repetition echo information, which ensures the bat to analyze the target range and surface texture more accurately.     

The role of GABAergic inhibition in shaping directional selectivity of bat inferior collicular neurons determined with temporally patterned pulse trains

This study examined the role of GABAergic inhibition in shaping directional selectivity of neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus. When determined with temporally patterned pulse trains at different pulse repetition rates, 93 inferior colliculus neurons displayed three types of directional selectivity curves. A directionally selective curve always showed a maximum to a certain azimuthal angle (the best angle). A hemifield curve showed a maximum to a range of contralateral azimuthal angles. A non-directional curve did not show a maximum to any particular azimuthal angles. Directional selectivity curves of 42% neurons changed from hemifield or non-directional to directionally selective and the best angles of 16-21% neurons shifted toward the midline with increasing pulse repetition rate of pulse trains. Directional selectivity curves of most (74%) neurons that discharged impulses to each pulse of a pulse train also became sharper with increasing pulse repetition rate of pulse trains. Bicuculline application produced more pronounced broadening of directional selective curves of inferior colliculus neurons at higher than at lower pulse repetition rates. As a result, pulse repetition rate-dependent directional selectivity of inferior colliculus neurons was abolished. Possible mechanisms and biological significance of these findings are discussed.     

抑制性频谱整合对大棕蝠下丘神经元声强敏感性的影响

自由声场条件下 ,采用特定双声刺激方法研究了不同频率通道之间的非线性整合对下丘神经元声强敏感性的调制作用。实验在 1 2只麻醉与镇定的大棕蝠 (Eptesicusfuscus)上进行 ,双电极同步记录 2个配对神经元的声反应动作电位。主要结果如下 :1 )所获 1 1 0个 (5 5对 )配对神经元中 ,85 5 %表现为抑制性频谱整合作用 ,其余 1 4 5 %为易化性频谱整合 ;2 )阈上 1 0dB (SPL)放电率抑制百分比与神经元最佳频率 (BF)及记录深度呈负相关 ;3)抑制效率随声刺激强度升高而逐步下降 ;4 )当掩蔽声分别位于神经元兴奋性频率调谐曲线(FTC)内 (MSin) /外 (MSout)时 ,其抑制效率存在差异。前者的放电率抑制百分比及声反应动力学范围(DR)下降百分比均显著高于后者 ;5 )抑制性频谱整合导致 3类DR改变 :6 1 6 %为下降、 1 0 9%增加、另有2 7 5 %变化小于 1 0 %。本结果进一步支持如下设想 :下丘不同频率通道之间的抑制性频谱整合参与了对强度编码的主动神经调制活动     

Spatial tuning of neurons in the inferior colliculus of the big brown bat: effects of sound level, stimulus type and multiple sound sources

We examined factors that affect spatial receptive fields of single units in the central nucleus of the inferior colliculus of Eptesicus fuscus. Pure tones, frequency- or amplitude-modulated sounds, or noise bursts were presented in the free-field, and responses were recorded extracellularly. For 58 neurons that were tested over a 30 dB range of sound levels, 7 (12%) exhibited a change of less than 10° in the center point and medial border of their receptive field. For 28 neurons that were tested with more than one stimulus type, 5 (18%) exhibited a change of less than 10° in the center point and medial border of their receptive field.The azimuthal response ranges of 19 neurons were measured in the presence of a continuous broadband noise presented from a second loudspeaker set at different fixed azimuthal positions. For 3 neurons driven by a contralateral stimulus only, the effect of the noise was simple masking. For 11 neurons driven by sound at either side, 8 were unaffected by the noise and 1 showed a simple masking effect. For the remaining 2, as well as for 5 neurons that were excited by contralateral sound and inhibited by ipsilateral sound, the peak of the azimuthal response range shifted toward the direction of the noise.Abbreviations E/E excitation at either ear - I/E inhibition at the ipsilateral ear, excitation at the contralateral ear - O/E no effect from the ipsilateral ear, excitation at the contralateral ear - FM downward frequency modulation - FM upward frequency modulation - IC inferior colliculus - ICC central nucleus of the inferior colliculus - ILD interaural level difference - ITD interaural time difference - PT pure tone - SAM sinusoidally amplitude modulated sounds - SFM sinusoidally frequency modulated sounds     

Amiloride attenuates glycine-induced currents in cultured neurons of rat inferior colliculus

Amiloride, a potassium sparing diuretic, is well known to interact with many ion transport systems and modulate the activity of several membrane receptors. However, relatively little information is available as to how amiloride affects membrane receptors of neurons in the brain areas. In the present study, we investigated the effects of amiloride on glycine-induced currents (I(Gly)) in cultured neurons of rat inferior colliculus with whole-cell patch-clamp recordings. Amiloride itself did not activate any current across the neuronal membrane but it reversibly inhibited the amplitude of the I(Gly) in a reversible and concentration-dependent manner, with an IC(50) of 487.4+/-25.3microM (n=5). Amiloride shifted the concentration-response relationship to the right without changing Hill coefficient and without changing the maximum response of the I(Gly). The pre-perfusion of amiloride produced an inhibitory effect on the I(Gly). In addition, amiloride was shown with a voltage ramp protocol to significantly reduce the conductance induced by glycine but not to change the reversal potential of the I(Gly). These results demonstrate that amiloride competitively inhibits the I(Gly) in rat inferior colliculus neurons by decreasing the affinity of glycine to its receptor. Our finding suggests that attention should be paid to the possible side effects of amiloride used as a drug on brain functions in the case of a defective blood-brain barrier and in the case of direct application of this drug into the cerebrospinal fluid for treatment of brain tumors.     

GABA-mediated modulation of the discharge pattern and rate-level function of two simultaneously recorded neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus

Neurons in the central nucleus of the inferior colliculus (IC) receive excitatory and inhibitory inputs from both lower and higher auditory nuclei. Interaction of these two opposing inputs shapes response properties of IC neurons. In this study, we examine the interaction of excitation and inhibition on the responses of two simultaneously recorded IC neurons using a probe and a masker under forward masking paradigm. We specifically study whether a sound that serves as a probe to elicit responses of one neuron might serve as a masker to suppress or facilitate the responses of the other neuron. For each pair of IC neurons, we deliver the probe at the best frequency (BF) of one neuron and the masker at the BF of the other neuron and vice versa. Among 33 pairs of IC neurons recorded, this forward masking produces response suppression in 29 pairs of IC neurons and response facilitation in 4 pairs of IC neurons. The degree of suppression decreases with recording depth, sound level and BF difference between each pair of IC neurons. During bicuculline application, the degree of response suppression decreases in the bicuculline-applied neuron but increases in the paired neuron. Our data indicate that the forward masking of responses of IC neurons observed in this study is mostly mediated through GABAergic inhibition which also shapes the discharge pattern of these neurons. These data suggest that interaction among individual IC neurons improves auditory sensitivity during auditory signal processing.     

Duration selectivity of bat inferior collicular neurons improves with increasing pulse repetition rate

Insectivorous big brown bats, Eptesicus fuscus, progressively increase the pulse repetition rate (PRR) throughout the course of hunting. While increasing PRR conceivably facilitates bats to extract information about the targets, it also inevitably affects sensitivity of their auditory neurons to pulse parameters. The present study examined the effect of increasing PRR on duration selectivity of this bat's inferior collicular (IC) neurons by comparing their impulse-duration functions determined at different PRRs. Impulse-duration functions plotted with the number of impulses in response to single pulses against pulse duration at different PRRs were described as short-pass, band-pass, long-pass, and all-pass. Short- or long-pass neurons discharged maximally to a range of short or long pulse durations. Band-pass neurons discharged maximally to one pulse duration. These three types of IC neurons were called duration tuned neurons. All-pass neurons were not duration tuned because they did not discharge maximally to any pulse duration. Increasing PRR improved duration selectivity of IC neurons by (1) increasing the number of duration tuned neurons; (2) decreasing the critical duration concomitant with increasing slope of the impulse-duration function; and (3) decreasing the 50% duration range of the impulse-duration function. This improved duration selectivity with PRR may potentially facilitate prey capture by bats.     

Ontogenesis of tonotopy in inferior colliculus of a hipposiderid bat reveals postnatal shift in frequency-place code

Summary The postnatal development of midbrain tonotopy was investigated in the inferior colliculus (IC) of the south Indian CF-FM batHipposideros speoris. The developmental progress of the three-dimensional frequency representation was determined by systematic stereotaxic recordings of multiunit clusters from the 1st up to the 7th postnatal week. Additional developmental measures included the tuning characteristics of single units (Figs. 3f; 4f; 5f), the analysis of the vocalised pulse repertoire (Figs. 3e, 4e, 5e), and morphometric reconstructions of the brains of all experimental animals (Fig. 1).The maturation of auditory processing could be divided into two distinct, possibly overlapping developmental periods: First, up to the 5th week, the orderly tonotopy in the IC developed, beginning with the low frequency representation and progressively adding the high frequency representation. With regard to the topology of isofrequency sheets within the IC, maturation progresses from dorsolateral to ventromedial (Figs. 3c, 4c). At the end of this phase the entire IC becomes specialised for narrowly tuned and sensitive frequency processing. This includes the establishment of the auditory fovea, i.e. the extensive spatial representation of a narrow band of behaviorally relevant frequencies in the ventromedial part of the IC. In the 5th postnatal week the auditory fovea is concerned with frequencies from 100–118 kHz (Fig. 4c, d). During subsequent development, the frequency tuning of the auditory fovea increases by 20–25 kHz and finally attains the adult range of ca. 125–140 kHz. During this process, neither the bandwidth of the auditory fovea (15–20 kHz) nor the absolute sensitivity of its units (ca. 50 dB SPL) were changed. Further maturation occurred at the single unit level : the sharpness of frequency tuning increased from the 5th to the 7th postnatal weeks (Q-₁₀-dB-values up to 30–60), and upper thresholds emerged (Figs. 4f, 5f).Although in the adult the frequency of the auditory fovea matches that of the vocalised pulses, none of the juvenile bats tested from the 5th to the 7th weeks showed such a frequency match between vocalisation and audition (Figs. 4e, 5e).The results show that postnatal maturation of audition in hipposiderid bats cannot be described by a model based on a single developmental parameter.Abbreviations BF best frequency - CF constant frequency - Cer cerebellum - CN cochlear nucleus - CO auditory cortex - CUF cuneiform nucleus - DAB days after birth - FAL forearm length - FM frequency modulation - IC inferior colliculus - NLL nucleus of the lateral lemniscus - PAG periaqueductal gray - SC superior colliculus