scholarly journals GABAergic Inhibition Controls Neural Gain in Inferior Colliculus Neurons Sensitive to Interaural Time Differences

2005 ◽  
Vol 25 (26) ◽  
pp. 6187-6198 ◽  
Author(s):  
N. J. Ingham
2005 ◽  
Vol 93 (6) ◽  
pp. 3390-3400 ◽  
Author(s):  
W. R. D’Angelo ◽  
S. J. Sterbing ◽  
E.-M. Ostapoff ◽  
S. Kuwada

A major cue for the localization of sound in space is the interaural time difference (ITD). We examined the role of inhibition in the shaping of ITD responses in the inferior colliculus (IC) by iontophoretically ejecting γ-aminobutyric acid (GABA) antagonists and GABA itself using a multibarrel pipette. The GABA antagonists block inhibition, whereas the applied GABA provides a constant level of inhibition. The effects on ITD responses were evaluated before, during and after the application of the drugs. If GABA-mediated inhibition is involved in shaping ITD tuning in IC neurons, then applying additional amounts of this inhibitory transmitter should alter ITD tuning. Indeed, for almost all neurons tested, applying GABA reduced the firing rate and consequently sharpened ITD tuning. Conversely, blocking GABA-mediated inhibition increased the activity of IC neurons, often reduced the signal-to-noise ratio and often broadened ITD tuning. Blocking GABA could also alter the shape of the ITD function and shift its peak suggesting that the role of inhibition is multifaceted. These effects indicate that GABAergic inhibition at the level of the IC is important for ITD coding.


Neuroscience ◽  
2019 ◽  
Vol 407 ◽  
pp. 135-145 ◽  
Author(s):  
Adam Sheppard ◽  
Xiaopeng Liu ◽  
Anaam Alkharabsheh ◽  
Guang-Di Chen ◽  
Richard Salvi

2015 ◽  
Vol 114 (5) ◽  
pp. 2941-2954 ◽  
Author(s):  
Björn Herrmann ◽  
Aravindakshan Parthasarathy ◽  
Emily X. Han ◽  
Jonas Obleser ◽  
Edward L. Bartlett

Stimulus-specific adaptation refers to a neural response reduction to a repeated stimulus that does not generalize to other stimuli. However, stimulus-specific adaptation appears to be influenced by additional factors. For example, the statistical distribution of tone frequencies has recently been shown to dynamically alter stimulus-specific adaptation in human auditory cortex. The present study investigated whether statistical stimulus distributions also affect stimulus-specific adaptation at an earlier stage of the auditory hierarchy. Neural spiking activity and local field potentials were recorded from inferior colliculus neurons of rats while tones were presented in oddball sequences that formed two different statistical contexts. Each sequence consisted of a repeatedly presented tone (standard) and three rare deviants of different magnitudes (small, moderate, large spectral change). The critical manipulation was the relative probability with which large spectral changes occurred. In one context the probability was high (relative to all deviants), while it was low in the other context. We observed larger responses for deviants compared with standards, confirming previous reports of increased response adaptation for frequently presented tones. Importantly, the statistical context in which tones were presented strongly modulated stimulus-specific adaptation. Physically and probabilistically identical stimuli (moderate deviants) in the two statistical contexts elicited different response magnitudes consistent with neural gain changes and thus neural sensitivity adjustments induced by the spectral range of a stimulus distribution. The data show that already at the level of the inferior colliculus stimulus-specific adaptation is dynamically altered by the statistical context in which stimuli occur.


1994 ◽  
Vol 72 (3) ◽  
pp. 1080-1102 ◽  
Author(s):  
T. J. Park ◽  
G. D. Pollak

1. In this study we examine the effects of GABAergic inhibition on the response properties and the constructed azimuthal receptive fields of 54 excitatory/inhibitory (EI) neurons tuned to 60 kHz in the inferior colliculus of the mustache bat. The constructed azimuthal receptive fields predict the spike counts that would be evoked by different intensities of 60-kHz sounds presented from each of 13 azimuthal locations in the frontal sound field. 2. Action potentials were recorded with a micropipette attached to a multibarrel glass electrode. Bicuculline, an antagonist specific for gamma-aminobutyric acid-A (GABAA) receptors, was iontophoretically applied through the multibarrel electrode. Both monaural and binaural response properties were initially recorded at a variety of interaural intensity disparities (IIDs) and absolute intensities, and the same response properties were subsequently assessed while GABAergic inhibition was blocked by bicuculline. Azimuthal receptive fields both before and during the application of bicuculline were constructed from response properties obtained with earphones after correcting for the directional properties of the ear and the IIDs generated by 60-kHz sounds presented from a variety of azimuthal locations. 3. Bicuculline had virtually no effect on either the monaural or binaural properties of 19 cells (35%). The constructed azimuthal receptive fields of these cells were also unaffected by bicuculline. Presumably the properties of these cells were formed in a lower nucleus, most likely the contralateral lateral superior olive (LSO), and were imposed on the collicular cell via the crossed projection from the LSO to the inferior colliculus, which is known to be excitatory. 4. In more than half of the neurons (65%) GABAergic inhibition influenced one or more features of the cell's response properties and thus its azimuthal receptive field. Some response properties were formed in the colliculus through GABAergic inhibition, whereas others appear to have been shaped initially in a lower nucleus and then further modified by GABAergic inhibition in the inferior colliculus. Moreover, a number of features of GABAergic inhibition that acted on inferior collicular cells were evoked by stimulation of the contralateral (excitatory) ear, whereas other features were influenced by stimulation of the ipsilateral (inhibitory) ear. 5. In 20 cells (37%) blocking GABAergic inhibition reduced or abolished the inhibition evoked by the ipsilateral ear. The receptive fields of cells in which the ipsilaterally evoked inhibition was reduced by bicuculline expanded further into the ipsilateral sound field than they did before bicuculline.(ABSTRACT TRUNCATED AT 400 WORDS)


2009 ◽  
Vol 101 (5) ◽  
pp. 2348-2361 ◽  
Author(s):  
Katrin Vonderschen ◽  
Hermann Wagner

Barn owls process sound-localization information in two parallel pathways, the midbrain and the forebrain pathway. Exctracellular recordings of neural responses to auditory stimuli from far advanced stations of these pathways, the auditory arcopallium in the forebrain and the external nucleus of the inferior colliculus in the midbrain, demonstrated that the representations of interaural time difference and frequency in the forebrain pathway differ from those in the midbrain pathway. Specifically, low-frequency representation was conserved in the forebrain pathway, while it was lost in the midbrain pathway. Variation of interaural time difference yielded symmetrical tuning curves in the midbrain pathway. By contrast, the typical forebrain-tuning curve was asymmetric with a steep slope crossing zero time difference and a less-steep slope toward larger contralateral time disparities. Low sound frequencies contributed sensitivity to contralateral leading sounds underlying these asymmetries, whereas high frequencies enhanced the steepness of slopes at small interaural time differences. Furthermore, the peaks of time-disparity tuning curves were wider in the forebrain than in the midbrain. The distribution of the steepest slopes of best interaural time differences in the auditory arcopallium, but not in the external nucleus of the inferior colliculus, was centered at zero time difference. The distribution observed in the auditory arocpallium is reminiscent of the situation observed in small mammals. We speculate that the forebrain representation may serve as a population code supporting fine discrimination of central interaural time differences and coarse indication of laterality of a stimulus for large interaural time differences.


1995 ◽  
Vol 74 (4) ◽  
pp. 1701-1713 ◽  
Author(s):  
A. Klug ◽  
T. J. Park ◽  
G. D. Pollak

1. The mammalian inferior colliculus contains large populations of binaural cells that are excited by stimulation of the contralateral ear and are inhibited by stimulation of the ipsilateral ear, and are called excitatory/inhibitory (EI) cells. Neurons with EI properties are initially created in the lateral superior olive (LSO), which, in turn, sends strong bilateral projections to the inferior colliculus. The questions that we address in this report are 1) whether the inhibition evoked by stimulation of the ipsilateral ear occurs at the inferior colliculus or whether it occurs in a lower nucleus, presumably the LSO; and 2) if the ipsilaterally evoked inhibition occurs at the inferior colliculus, is the inhibition a consequence of glycinergic innervation or is it a consequence of GABAergic innervation. To study these questions, we recorded from 61 EI neurons in the inferior colliculus of the mustache bat before and during the iontophoretic application of the glycine receptor antagonist, strychnine. We also tested the effects of the gamma-aminobutyric acid-A (GABAA) receptor antagonist, bicuculline, on 38 of the 61 neurons that were tested with strychnine. The main finding is that glycinergic or GABAergic inhibition, or both, contribute to the ipsilaterally evoked inhibition in approximately 50% of the EI neurons in the inferior colliculus. 2. Strychnine and bicuculline had different effects on the magnitude of the spike counts evoked by stimulation of the contralateral (excitatory) ear. On average, strychnine caused the maximum spike count evoked by contralateral stimulation to increase by only 23%. The relatively small effects of strychnine on response magnitude are in marked contrast to the effects of bicuculline, which usually caused much larger increases in spike counts. For example, although strychnine caused spike counts to more than double in approximately 25% of the collicular neurons, bicuculline caused a doubling of the spike count in approximately 60% of the cells. 3. The inhibitory influences of ipsilateral stimulation were evaluated by driving the neurons with a fixed intensity at the contralateral ear and then documenting the reductions in spike counts due to the presentation of progressively higher intensities at the ipsilateral ear. In 64% of the neurons sampled, blocking glycinergic inhibition with strychnine had little or no effect on the ipsilaterally evoked inhibition. These cells remained as strongly inhibited during the application of strychnine as they did before its application. In addition, the ipsilateral intensity that produced complete or nearly complete spike suppression in the predrug condition was also unchanged by strychnine. 4. In 36% of the neurons, strychnine markedly reduced the degree of ipsilaterally evoked spike suppression. In five of these neurons, there was a complete elimination of the ipsilateral inhibition: these neurons were transformed from strongly inhibited EI neurons into monaural neurons. 5. The influence of both strychnine and bicuculline was tested sequentially in 38 neurons. In about one-half of these cells, (53%, 20/38) the ipsilaterally evoked inhibition was unaffected by either drug. In 10 other units (26%), both drugs substantially reduced or eliminated the ipsilaterally evoked inhibition. In most of these cells, both bicuculline and strychnine reduced the ipsilaterally evoked inhibition to a similar degree. In the remaining eight cells studied with both drugs (21%), the ipsilaterally evoked inhibition was reduced or eliminated by one of the drugs, but not by both. 6. These results show that both glycinergic and GABAergic projections influence the ipsilaterally evoked inhibition in about one-half of the EI neurons in the inferior colliculus. The glycinergic inhibition elicited by ipsilateral stimulation is most likely due to projections from the ipsilateral lateral superior olive, whereas the GABAergic inhibition evoked by ipsilateral stimulation is most likely caused b


1985 ◽  
Vol 53 (1) ◽  
pp. 89-109 ◽  
Author(s):  
G. Harnischfeger ◽  
G. Neuweiler ◽  
P. Schlegel

Single-unit responses to tonal stimulation with interaural disparities were recorded in the nuclei of the superior olivary complex (SOC) and the central nucleus of the inferior colliculus (ICC) of the echolocating bat, Molossus ater. Seventy-six units were recorded from the ICC and 74 from the SOC; of the SOC units, 31 were histologically verified in the medial superior olive (MSO), 10 in the lateral superior olive (LSO), and 33 in unidentified areas of the SOC. Best frequencies (BFs) of the units ranged from 10.3 to 89.6 kHz, and Q10 dB values ranged from 2 to 70 dB. Most ICC neurons responded phasically to stimulus onset and were either inhibitory/excitatory [I/E; (53)] or excitatory/excitatory [E/E; (21)] units. In the MSO, 23 units responded tonically and 7 phasically on, 18 were E/E or E/OF (facilitatory for other input) units, and 11 were I/E neurons. All LSO neurons responded in a "chopper" fashion, and the binaural neurons were E/I units. In E/E units the excitatory response to binaural stimulation was frequently larger than the sum of the monaurally evoked responses. Many neurons with E/I or I/E inputs had very steep binaural impulse-count functions and were sensitive to small interaural intensity differences. Twenty-eight units (24%) responded with a change in firing rate of at least 20% to interaural time differences of +/- 500 microseconds. Within this sample, 11 units (8 from ICC, 2 from MSO, and 1 from SOC) were sensitive to interaural time differences of only +/- 50 microseconds. Of these 11 units, 10 were I/E units responding phasically only to stimulus onset and were also sensitive to intensity differences (delta I), being suppressed completely by the inhibitory input over a delta I range of 20 dB or less. Of 117 units tested in the ICC and SOC nuclei, 86 units (76%) were not sensitive to interaural time disparities within +/- 500 microseconds. Because the BFs of these units sensitive to interaural transient time differences (delta t) ranged between 18 and 90 kHz, responses were elicited by pure tones, and responses did not change periodically with the period equal to that of the stimulus frequency, we conclude that the neurons reacted to interaural differences of stimulus-onset time (transient time difference) but not to phase differences (ongoing time difference). Sensitivity to interaural time differences was also correlated with interaural intensity differences.(ABSTRACT TRUNCATED AT 400 WORDS)


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