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

doi:10.1016/j.heares.2006.03.001

Hearing Research

Volume 215, Issues 1–2, May 2006, Pages 56-66

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Abstract

A previous study has shown that duration selectivity of neurons in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus becomes sharper with increasing pulse repetition rate (PRR). The present study examines the role of GABAergic inhibition in improving duration selectivity of bat IC neurons with PRR by means of iontophoretic application of GABA as well as its antagonist, bicuculline. Duration selectivity of IC neurons is studied by plotting the duration tuning curves with the number of impulses per pulse against the pulse duration. Duration tuning curves of IC neurons are described as band-, short-, long- and all-pass in terms of filtering properties to sound duration. Bicuculline application produces more pronounced broadening of duration tuning curves at high than at low PRR. Conversely, GABA application produces more pronounced narrowing of duration tuning curves at low than at high PRR. In either case, sharpening of duration selectivity of IC neurons with increasing PRR is abolished during drug application. The duration tuning curves of IC neurons progressively broadens with recording depth. Broadening of duration tuning curves during bicuculline application is more pronounced for neurons at upper than at deep IC. This progressive decrease in duration selectivity with recording depth is discussed in relation to spatial distribution gradient of GABA_A receptors in the IC. Possible biological significance of these findings relevant to bat echolocation is discussed.

Introduction

Sound duration is an important feature that contributes to the distinct spectral and temporal attributes of individual biological sounds. Previous studies of selectivity of auditory neurons to sound duration has been conducted in many animals including frogs (Feng et al., 1990, Gooler and Feng, 1992, Narins and Capranica, 1980), bats (Casseday et al., 1994, Casseday et al., 2000, Ehrlich et al., 1997, Fuzessery and Hall, 1999, Galazyuk and Feng, 1997, Jen and Feng, 1999, Jen and Schlegel, 1982, Jen and Zhou, 1999, Pinheiro et al., 1991, Zhou and Jen, 2001), cats (He et al., 1997), chinchillas (Chen, 1998), mice (Brand et al., 2000) and rats (Perez-Gonzalez et al., 2006). These studies show that most auditory neurons behave as band-, short- or long-pass filters to pulse duration such that they respond maximally to a specific duration or a range of durations.

In the mammalian auditory pathway, the central nucleus of the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei (Adams, 1979, Casseday and Covey, 1995, Oliver et al., 1994, Shneiderman and Oliver, 1989). Neurotransmitters that mediate the inhibitory inputs are γ-aminobutyric acid (GABA) or glycine (Fubara et al., 1996, Oliver et al., 1994, Roberts and Ribak, 1987). Previous studies show that the interplay between these two opposing inputs contributes to auditory temporal processing and shapes multi-parametric selectivity (e.g., duration, frequency, amplitude, direction, etc.) of IC neurons using single repetitive sound pulses or temporally patterned trains of sound pulses (Casseday and Covey, 1995, Casseday et al., 1994, Casseday et al., 2000, Jen and Feng, 1999, Jen and Zhang, 2000, Jen et al., 2002, Klug et al., 1995, Koch and Grothe, 1998, LeBeau et al., 1996, LeBeau et al., 2001, Lu and Jen, 2001, Lu et al., 1997, Lu et al., 1998, Zhou and Jen, 2002).

When studied with temporally patterned trains of sound pulses at different pulse repetition rates (PRR), the response selectivity of IC neurons in bats has been shown to improve with increasing PRR in multi-parametric domains (Galazyuk et al., 2000, Jen and Zhou, 1999, Jen et al., 2001, Jen et al., 2002, Smalling et al., 2001, Wu and Jen, 1995a, Wu and Jen, 1995b, Wu and Jen, 1996, Zhou and Jen, 2002). In our laboratory, we have previously studied the role of GABAergic inhibition in shaping the frequency and directional selectivity of bat IC neurons with PRR (Jen et al., 2002, Zhou and Jen, 2002). We showed that increasing GABAergic inhibition with the PRR contributes to improving frequency and directional selectivity of IC neurons. As an extension of these studies, the main objective of the present study is to show that increasing GABAergic inhibition with the PRR also contributes to improving duration selectivity of IC neurons. To achieve this objective, we studied the duration selectivity of IC neurons with pulse trains of three PRRs before and during application of GABA or bicuculline which is an antagonist for GABA_A receptor (Bormann, 1988, Cooper et al., 1982). By means of application of both drugs that produced opposite effect on duration selectivity of IC neurons, we were able to double confirm the role of GABAergic inhibition in improving duration selectivity of IC neurons with PRR.

Section snippets

Materials and methods

Eight Eptesicus fuscus (five males, three females, 18–22 g, body weight, b.w.) were used for this study. As in previous studies (Jen et al., 1987), one or two days before the recording session, a 1.8 cm nail was glued onto the exposed skull of Nembutal-anesthetized (45–50 mg/kg b.w.) bat with acrylic glue and dental cement. Exposed tissue was treated with an antibiotic (Neosporin) to prevent infection. During the day of recording, the bat was administered the neuroleptanalgesic Innovar-Vet

Duration tuning properties of IC neurons determined with pulse trains

As in our previous studies (Jen and Zhou, 1999, Jen et al., 2001, Zhou and Jen, 2002), IC neurons differed in the number of impulses discharged to each pulse and in the ability in response to each pulse of a pulse train. Among 178 neurons studied, 134 (75%) neurons discharged impulses to each pulse of all three presented pulse trains. The remaining 44 (25%) neurons only discharged impulses to each pulse of pulse trains of 10 and 30 pps (26, 15%) or to each pulse of pulse train of 10 pps only (18,

The role of GABAergic inhibition in improving duration selectivity of IC neurons with PRR

The opposite effect of bicuculline and GABA application on duration tuning curves of IC neurons observed in the present study (i.e., Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7) clearly supports the role of GABAergic inhibition in shaping the duration selectivity of IC neurons as reported earlier (Casseday et al., 1994, Casseday et al., 2000, Jen and Feng, 1999). Sharpening of duration tuning curve by GABAergic inhibition is a result of varying degree of inhibition with pulse duration. This

Acknowledgements

We thank two anonymous reviewers for commenting on an earlier version of this manuscript. This work was supported by a grant and fellowship from the Graduate School and matching fund from the Division of Biological Sciences and College and Arts and Sciences of University of Missouri-Columbia.

References (48)

J. Bormann
Electrophysiology of GABA_A and GABA_B receptor subtypes
Trends Neurosci.
(1988)
G.D. Chen
Effect of stimulus duration on responses of neurons in the chinchilla inferior colliculus
Hear. Res.
(1998)
A.S. Feng et al.
Neural basis of sound pattern recognition in anurans
Prog. Neurobiol.
(1990)
Z.M. Fuzessery et al.
Sound duration selectivity in the pallid bat inferior colliculus
Hear. Res.
(1999)
P.H.-S. Jen et al.
Auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus
Brain Res.
(1987)
P.H.-S. Jen et al.
GABAergic inhibition contributes to pulse repetition rate-dependent frequency selectivity in inferior colliculus of the big brown bat, Eptesicus fuscus
Brain Res.
(2002)
P.H.-S. Jen et al.
The role of GABAergic inhibition on direction-dependent sharpening of frequency tuning in bat inferior collicular neurons
Brain Res.
(2000)
M. Wu et al.
Responses of pontine neurons of the big brown bat, Eptesicus fuscus, to temporally patterned sound pulses
Hearing Res.
(1995)
J.C. Adams
Ascending projections to the inferior colliculus
J. Comp. Neurol.
(1979)
A. Brand et al.
Duration tuning in mouse auditory midbrain
J. Neurophysiol.
(2000)

J.H. Casseday et al.

Mechanisms for analysis of auditory temporal patterns in the brainstem of echolocating bats

J.H. Casseday et al.

Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus

Science

(1994)

J.H. Casseday et al.

Neural measurement of sound duration: control by excitatory–inhibitory interaction in the inferior colliculus

J. Neurophysiol.

(2000)

J.R. Cooper et al.

The Biomedical Basis of Neuropharmacology

(1982)

D. Ehrlich et al.

Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus

J. Neurophysiol.

(1997)

B.M. Fubara et al.

Distribution of GABA_A, GABA_B and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus

J. Comp. Neurol.

(1996)

A.V. Galazyuk et al.

Encoding of sound duration by neurons in the auditory cortex of the little brown bat, Myotis lucifugus

J. Comp. Physiol. A

(1997)

A.V. Galazyuk et al.

Temporal dynamics of acoustic stimuli enhance amplitude tuning of inferior colliculus neurons

J. Neurophysiol.

(2000)

S.A. Gelfand

Hearing

(1990)

D.M. Gooler et al.

Temporal coding in frog auditory midbrain: the influence of duration and rise-fall time on processing of complex amplitude-modulated stimuli

J. Neurophysiol.

(1992)

D.R. Griffin

Listening in the Dark

(1958)

J.F. He et al.

Temporal integration and duration tuning in dorsal zone of cat auditory cortex

J. Neurosci.

(1997)

P.H.-S. Jen et al.

Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons

J. Comp. Physiol. A

(1999)

P.H.-S. Jen et al.

Auditory physiological properties of the neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus

J. Comp. Physiol.

(1982)

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Citation Excerpt :
Because the temporal window for masking reduces with decreasing of sound duration, a neuron's recovery cycle would also shorten with decreasing duration of paired sounds (Wang et al., 2010; Wu and Jen, 1998). Many studies have shown that interaction of excitation and GABAergic and/or glycinergic inhibition contributes to auditory temporal processing and shapes multi-parametric selectivity (e.g., duration, frequency, amplitude, direction, etc.) of collicular neurons using single repetitive sound pulses or temporally patterned trains of sound pulses (Casseday et al., 1994; Jen and Feng, 1999; Jen et al., 2002; Klug et al., 1995; Koch and Grothe, 1998; LeBeau et al., 2001; Lu et al., 1997, 1998; Lu and Jen, 2001; Park and Pollak, 1993; Wu and Jen, 2006a,b). Conceivably, this interaction of excitation and GABAergic and/or glycinergic inhibition may also shape the recovery cycle of collicular neurons.
Our previous study showed that when stimulated with constant frequency–frequency modulation (CF–FM) sounds, neurons in the central nucleus of the inferior colliculus of the CF–FM bat, Hipposideros armiger, either only discharged impulses to the onset of CF–FM sounds (76%, single-on neurons) or to the onset of both CF and FM components of CF–FM sounds (24%, double-on neuron) (Fu et al., 2010). The present paper reports the recovery cycles of these two types of neurons using paired CF, FM and CF–FM sounds as stimuli. Both types of neurons had similar recovery cycle for CF sounds but had the shortest recovery cycle for FM sounds. Whereas single-on neurons had similar recovery cycle for CF and CF–FM sounds, double-on neurons had longer recovery cycle for CF sounds than for CF–FM sounds. In addition, double-on neurons had significantly shorter recovery cycles than single-on neurons for FM and CF–FM sounds. Most neurons did not respond to the second sound when each pair of sounds overlapped. However, when stimulated with paired CF–FM sounds, 3 single-on and 7 double-on neurons discharged to the second sound even when both sounds overlapped. As such, they had “cyclic” recovery cycles that varied between maximum and minimum with inter-pulse intervals. Possible mechanisms underlying the different recovery cycles of these neurons are proposed. Possible biological significance of these neurons in relation to responding to varied pulse repetition rate during hunting is discussed.
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Fast glutamatergic and GABAergic transmission in the central nucleus of the inferior colliculus (ICC), a major auditory midbrain structure, is mediated respectively by alpha-amino-3-hydroxy-5-methylisoxazole-4 propionic acid (AMPA) and γ-aminobutyric acid (GABA)_A receptors. In this study, we used whole-cell patch clamp recordings in brain slices to investigate the effects of activation of metabotropic glutamate receptors (mGluRs) on synaptic responses mediated by AMPA and GABA_A receptors in ICC neurons of young rats. Excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs) mediated respectively by AMPA and GABA_A receptors were elicited by stimulation of the lateral lemniscus, the major afferent pathway to the ICC. The agonists for groups I and II mGluRs, (±)-1-aminocyclopentane-trans-1,3-dicarboxylic acid (ACPD), and for group III mGluRs, l-2-amino-3-hydroxypropanoic acid 3-phosphate (l-SOP), did not affect intrinsic membrane properties of the ICC neurons. The agonist for group II mGluRs, (1R,4R,5S,6R)-4-amino-2-oxabicyclo[3.1.0] hexane-4,6-dicarboxylic acid (LY379268), significantly reduced the AMPA receptor-mediated EPSCs and GABA_A receptor-mediated IPSCs. The effects were reversed by the group II mGluR antagonist, (2S)-2-amino-2-[(1S,2S)-2-carboxycycloprop-1-yl]-3-(xanth-9-yl) propanoic acid (LY341495). The agonists for groups I and III, (RS)-3,5-dihydroxyphenylglycine (DHPG) and l-SOP, respectively, did not affect AMPA or GABA_A receptor-mediated responses. The reduction of the synaptic responses by LY379268 was accompanied by a substantial increase in a ratio of the second to the first AMPA receptor-mediated EPSCs and GABA_A receptor-mediated IPSCs to paired-pulse stimulation. The results suggest that group II mGluRs regulate both fast glutamatergic and GABAergic synaptic transmission in the ICC, probably through a presynaptic mechanism due to reduction of transmitter release.
The physiological role of pre- and postsynaptic GABA<inf>B</inf> receptors in membrane excitability and synaptic transmission of neurons in the rat's dorsal cortex of the inferior colliculus
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In the inferior colliculus (IC), GABAergic inhibition mediated by GABA_A receptors has been shown to play a significant role in regulating physiological responses, but little is known about the physiological role of GABA_B receptors in IC neurons. In the present study, we used whole-cell patch clamp recording in vitro to investigate the effects of activation of GABA_B receptors on membrane excitability and synaptic transmission of neurons in the rat's dorsal cortex of the inferior colliculus (ICD). Repetitive stimulation of GABAergic inputs to ICD neurons at high frequencies could elicit a slow and long-lasting postsynaptic response, which was reversibly abolished by the GABA_B receptor antagonist, CGP 35348. The results suggest that postsynaptic GABA_B receptors can directly mediate inhibitory synaptic transmission in ICD. The role of postsynaptic GABA_B receptors in regulation of membrane excitability was further investigated by application of the GABA_B receptor agonist, baclofen. Baclofen hyperpolarized the cell, reduced the membrane input resistance and firing rate, increased the threshold for generating action potentials (APs), and decreased the amplitude of the AP and its associated after-hyperpolarization. The Ca²⁺-mediated rebound depolarization following hyperpolarization and the depolarization hump at the beginning of membrane depolarization were also suppressed by baclofen. In voltage clamp experiments, baclofen induced inward rectifying K⁺ current and reduced low- and high-threshold Ca²⁺ currents, which may account for the suppression of membrane excitability by postsynaptic GABA_B receptors. Application of baclofen also reduced excitatory synaptic responses mediated by α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors, and inhibitory synaptic responses mediated by GABA_A receptors. Baclofen increased the ratios of 2nd/1st excitatory and inhibitory postsynaptic currents to paired-pulse stimulation of the synaptic inputs. These results suggest that fast glutamatergic and GABAergic synaptic transmission in ICD can be modulated by presynaptic GABA_B receptors.
Echo frequency selectivity of duration-tuned inferior collicular neurons of the big brown bat, Eptesicus fuscus, determined with pulse-echo pairs
2008, Neuroscience
Citation Excerpt :
As shown in our previous studies (Jen et al., 2001, 2002), increasing pulse repetition rate improves frequency selectivity of IC neurons. As described in the introduction, many of our previous studies have shown that analysis of an echo parameter by neurons is inevitably affected by other co-varying echo parameters (Jen and Zhou, 1999; Jen and Wu, 2006; Jen et al., 2001, 2002; Wu and Jen, 1996, 2006a,b, 2007, 2008; Zhou and Jen, 2001, 2002). Recently, we have further shown that when determined with P-E pairs, ED selectivity of IC neurons improves with decreasing PD, P-E gap and P-E amplitude difference (Jen and Wu, 2008).
During hunting, insectivorous bats such as Eptesicus fuscus progressively vary the repetition rate, duration, frequency and amplitude of emitted pulses such that analysis of an echo parameter by bats would be inevitably affected by other co-varying echo parameters. The present study is to determine the variation of echo frequency selectivity of duration-tuned inferior collicular neurons during different phases of hunting using pulse-echo (P-E) pairs as stimuli. All collicular neurons discharge maximally to a tone at a particular frequency which is defined as the best frequency (BF). Most collicular neurons also discharge maximally to a BF pulse at a particular duration which is defined as the best duration (BD). A family of echo iso-level frequency tuning curves (iso-level FTC) of these duration-tuned collicular neurons is measured with the number of impulses in response to the echo pulse at selected frequencies when the P-E pairs are presented at varied P-E duration and gap. Our data show that these duration-tuned collicular neurons have narrower echo iso-level FTC when measured with BD than with non-BD echo pulses. Also, IC neurons with low BF and short BD have narrower echo iso-level FTC than IC neurons with high BF and long BD have. The bandwidth of echo iso-level FTC significantly decreases with shortening of P-E duration and P-E gap. These data suggest that duration-tuned collicular neurons not only can facilitate bat's echo recognition but also can enhance echo frequency selectivity for prey feature analysis throughout a target approaching sequence during hunting. These data also support previous behavior studies showing that bats prepare their auditory system to analyze expected returning echoes within a time window to extract target features after pulse emission.
Responses of inferior colliculus neurons to sounds presented at different rates in anesthetized albino mouse
2008, Hearing Research
We recorded extracellular activity from 402 single units located in the inferior colliculus (IC) of barbiturate-anesthetized albino mice. The stimuli were pure tones at characteristic frequency (CF) with durations of 10, 40 and 100 ms and intensities ranged from 5 to 25 dB above unit’s minimum threshold (MT). The tones were presented with different repetition rates (RRs) ranging from 0.2 to 20.0 Hz. At low intensities (5 dB above MT, determined at RR of 0.5 Hz) the great majority of units exhibited a strong decline of their responses when the stimulus RR was increased. About one-half of the units did not respond to 40 ms tones when they were stimulated with the RR of 3.0 Hz. This effect was even more pronounced for 100 ms tones. Generally, the increase in stimulus intensity led to an increase in the high-frequency border of RR. Nevertheless, even at intensities of 20–30 dB above MT, some units showed no response when the RR exceeded 5.0 Hz. In many cases the band-pass or high-pass duration tuning of the single unit was transformed to low-pass or all-pass when the rate was low enough to guarantee the independence of successive presentations of the stimuli. Responses of a very small group of IC units, however, were enhanced when the RR was increased. Our data have shown that the changes in the RR radically modify many features of the neural response (number of spikes, latency, discharge pattern, duration selectivity). We suggest that long-lasting inhibitory processes may be induced by low intensity stimuli in many units of the IC.
Bat inferior collicular neurons have the greatest frequency selectivity when determined with best-duration pulses
2008, Neuroscience Letters
During hunting, insectivorous bats such as Eptesicus fuscus progressively increase the pulse repetition rate, shorten the pulse duration, and lower the frequency and amplitude of emitted pulses as they search, approach and finally intercept insects or negotiate obstacles. As such, analysis of an echo parameter by the bat is inevitably affected by other co-varying echo parameters. The present study examined the effect of pulse duration on frequency selectivity of neurons in the central nucleus of the inferior colliculus (IC) of the big brown bat. A family of iso-level frequency tuning curves of each IC neuron was first measured with tone bursts of different durations. The bandwidth of iso-level frequency tuning curves within each family was then compared. Our data show that most IC neurons discharge maximally to a particular pulse duration which is defined as the best duration (BDu). The iso-level frequency tuning curves of these duration-selective neurons have the narrowest bandwidth when measured with the BDu pulse than with non-BDu pulses. They also have the narrowest bandwidth when measured with a short than with a long BDu pulse. These data suggest that frequency selectivity of duration-selective IC neurons becomes sharper when short echo duration at the final phase of hunting is encoded by IC neurons that have short BDu.

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¹: Present address: Department of Life Science, National Taiwan Normal University, Taipei, Republic of China.

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Research paperThe role of GABAergic inhibition in shaping duration selectivity of bat inferior collicular neurons determined with temporally patterned sound trains

Abstract

Introduction

Section snippets

Materials and methods

Duration tuning properties of IC neurons determined with pulse trains

The role of GABAergic inhibition in improving duration selectivity of IC neurons with PRR

Acknowledgements

Trends Neurosci.

Hear. Res.

Prog. Neurobiol.

Hear. Res.

Brain Res.

Brain Res.

Brain Res.

Hearing Res.

Ascending projections to the inferior colliculus

J. Comp. Neurol.

Duration tuning in mouse auditory midbrain

J. Neurophysiol.

Mechanisms for analysis of auditory temporal patterns in the brainstem of echolocating bats

Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus

Science

Neural measurement of sound duration: control by excitatory–inhibitory interaction in the inferior colliculus

J. Neurophysiol.

The Biomedical Basis of Neuropharmacology

Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus

J. Neurophysiol.

Distribution of GABAA, GABAB and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus

J. Comp. Neurol.

Encoding of sound duration by neurons in the auditory cortex of the little brown bat, Myotis lucifugus

J. Comp. Physiol. A

Temporal dynamics of acoustic stimuli enhance amplitude tuning of inferior colliculus neurons

J. Neurophysiol.

Hearing

Temporal coding in frog auditory midbrain: the influence of duration and rise-fall time on processing of complex amplitude-modulated stimuli

J. Neurophysiol.

Listening in the Dark

Temporal integration and duration tuning in dorsal zone of cat auditory cortex

J. Neurosci.

Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons

J. Comp. Physiol. A

Auditory physiological properties of the neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus

J. Comp. Physiol.

Research paper
The role of GABAergic inhibition in shaping duration selectivity of bat inferior collicular neurons determined with temporally patterned sound trains

Distribution of GABA_A, GABA_B and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus