scholarly journals GABA Shapes a Systematic Map of Binaural Sensitivity in the Auditory Cortex

2010 ◽  
Vol 104 (1) ◽  
pp. 517-528 ◽  
Author(s):  
Khaleel A. Razak ◽  
Zoltan M. Fuzessery

A consistent organizational feature of auditory cortex is a clustered representation of binaural properties. Here we address two questions. What is the intrinsic organization of binaural clusters and to what extent does intracortical processing contribute to binaural representation. We address these issues in the auditory cortex of the pallid bat. The pallid bat listens to prey-generated noise transients to localize and hunt terrestrial prey. As in other species studied, binaural clusters are present in the auditory cortex of the pallid bat. One cluster contains neurons that require binaural stimulation to be maximally excited, and are commonly termed predominantly binaural (PB) neurons. These neurons do not respond to monaural stimulation of either ear but show a peaked sensitivity to interaural intensity differences (IID) centered near 0 dB IID. We show that the peak IID varies systematically within this cluster. The peak IID is also correlated with the best frequency (BF) of neurons within this cluster. In addition, the IID selectivity of PB neurons is shaped by intracortical GABAergic input. Iontophoresis of GABAA receptor antagonists on PB neurons converts a majority of them to binaurally inhibited (EI) neurons that respond best to sounds favoring the contralateral ear. These data indicate that the cortex does not simply inherit binaural properties from lower levels but instead sharpens them locally through intracortical inhibition. The IID selectivity of the PB cluster indicates that the pallid bat cortex contains an increased representation of the frontal space that may underlie increased localization accuracy in this region.

1996 ◽  
Vol 75 (1) ◽  
pp. 75-96 ◽  
Author(s):  
D. R. Irvine ◽  
R. Rajan ◽  
L. M. Aitkin

1. Interaural intensity differences (IIDs) provide the major cue to the azimuthal location of high-frequency narrowband sounds. In recent studies of the azimuthal sensitivity of high-frequency neurons in the primary auditory cortex (field AI) of the cat, a number of different types of azimuthal sensitivity have been described and the azimuthal sensitivity of many neurons was found to vary as a function of changes in stimulus intensity. The extent to which the shape and the intensity dependence of the azimuthal sensitivity of AI neurons reflects features of their IID sensitivity was investigated by obtaining data on IID sensitivity from a large sample of neurons with a characteristic frequency (CF) > 5.5 kHz in AI of anesthetized cats. IID sensitivity functions were classified in a manner that facilitated comparison with previously obtained data on azimuthal sensitivity, and the effects of changes in the base intensity at which IIDs were introduced were examined. 2. IID sensitivity functions for CF tonal stimuli were obtained at one or more intensities for a total of 294 neurons, in most cases by a method of generating IIDs that kept the average binaural intensity (ABI) of the stimuli at the two ears constant. In the standard ABI range at which a function was obtained for each unit, five types of IID sensitivity were distinguished. Contra-max neurons (50% of the sample) had maximum response (a peak or a plateau) at IIDs corresponding to contralateral azimuths, whereas ipsi-max neurons (17%) had the mirror-image form of sensitivity. Near-zero-max neurons (18%) had a clearly defined maximum response (peak) in the range of +/- 10 dB IID, whereas a small group of tough neurons (2%) had a restricted range of minimal responsiveness with near-maximal responses at IIDs on either side. A final 18% of AI neurons were classified as insensitive to IIDs. The proportions of neurons exhibiting the various types of sensitivity corresponded closely to the proportions found to exhibit corresponding types of azimuthal sensitivity in a previous study. 3. There was a strong correlation between a neuron's binaural interaction characteristics and the form of its IID sensitivity function. Thus, neurons excited by monaural stimulation of only one ear but with either inhibitory, facilitatory, or mixed facilitatory-inhibitory effects of stimulation of the other ear had predominantly contra-max IID sensitivity (if contralateral monaural stimulation was excitatory) or ipsi-max sensitivity (if ipsilateral monaural stimulation was excitatory). Neurons driven weakly or not at all by monaural stimulation but facilitated binaurally almost all exhibited near-zero-max IID sensitivity. The exception to this tight association between binaural input and IID sensitivity was provided by neurons excited by monaural stimulation of either ear (EE neurons). Although EE neurons have frequently been considered to be insensitive to IIDs, our data were in agreement with two recent reports indicating that they can exhibit various forms of IID sensitivity: only 23 of 75 EE neurons were classified as insensitive and the remainder exhibited diverse types of sensitivity. 4. IID sensitivity was examined at two or more intensities (3-5 in most cases) for 84 neurons. The form of the IID sensitivity function (defined in terms of both shape and position along the IID axis) was invariant with changes in ABI for only a small proportion of IID-sensitive neurons (approximately 15% if a strict criterion of invariance was employed), and for many of these neurons the spike counts associated with a given IID varied with ABI, particularly at near-threshold levels. When the patterns of variation in the form of IID sensitivity produced by changes in ABI were classified in a manner equivalent to that used previously to classify the effects of intensity on azimuthal sensitivity, there was a close correspondence between the effects of intensity on corresponding types of azimuthal and IID sensitivity


1994 ◽  
Vol 71 (6) ◽  
pp. 1999-2013 ◽  
Author(s):  
L. Yang ◽  
G. D. Pollak

1. We studied the monaural and binaural response properties of 99 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat before and during the iontophoretic application of antagonists that blocked gamma-aminobutyric acid-A (GABAA) receptors (bicuculline) or glycine receptors (strychnine). All cells were driven by monaural stimulation of the contralateral ear, whereas monaural stimulation of the ipsilateral ear never evoked discharges. The binaural properties of 81 neurons were determined by holding the intensity constant at the contralateral ear and presenting a variety of intensities to the ipsilateral ear. This procedure generated interaural intensity disparity (IID) functions and allowed us to determine the effect of ipsilaterally evoked inhibition on a constant excitatory drive evoked by the contralateral ear. 2. One of the main findings is that the IID functions in the majority of DNLL neurons were not affected by application of either strychnine or bicuculline. Blocking glycinergic inhibition with strychnine had no effect on the IID functions in 75% of the cells studied. However, strychnine did change the IID functions in approximately 25% of the DNLL population. In those cells glycinergic inhibition appeared to be partially, or, in a few cases, entirely responsible for the ipsilaterally evoked spike suppression. In contrast, blocking GABAergic inhibition with bicuculline had no discernible effect on the ipsilaterally evoked spike suppression in any of the excitatory/inhibitory cells that we recorded. GABAergic inhibition, therefore, plays no role in the formation of IID functions of neurons in the DNLL. Furthermore, the results suggest that glycinergic inhibition also does not contribute to the suppression of spikes evoked by stimulation of the contralateral ear in the vast majority of DNLL neurons. 3. Although the majority of IID functions were not influenced when either GABAergic or glycinergic innervation was blocked, ipsilateral stimulation alone evoked both a glycinergic and GABAergic inhibition in most DNLL cells. These inhibitory events were demonstrated in 18 other cells by evoking discharges with the iontophoretic application of glutamate. Stimulating the ipsilateral ear alone under these conditions caused a suppression of the glutamate-evoked discharges. Furthermore, the spike suppression persisted for a period of time that was longer than the duration of the tone burst at the ipsilateral ear. 4. The application of bicuculline or strychnine had different effects on the glutamate-elicited spikes. Bicuculline reduced the duration of the inhibition, and it was always the latter portion of the inhibition that was abolished by bicuculline. In more than half of the cells studied strychnine also reduced the duration of the inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 70 (2) ◽  
pp. 492-511 ◽  
Author(s):  
F. K. Samson ◽  
J. C. Clarey ◽  
P. Barone ◽  
T. J. Imig

1. Single-unit recordings were carried out in primary auditory cortex (AI) of barbiturate-anesthetized cats. Neurons, sensitive to sound direction in the horizontal plane (azimuth), were identified by their responses to noise bursts, presented in the free field, that varied in azimuth and sound pressure level (SPL). SPLs typically varied between 0 and 80 dB and were presented at each azimuth that was tested. Each azimuth-sensitive neuron responded well to some SPLs at certain azimuths and did not respond well to any SPL at other azimuths. This report describes AI neurons that were sensitive to the azimuth of monaurally presented noise bursts. 2. Unilateral ear plugging was used to test each azimuth-sensitive neuron's response to monaural stimulation. Ear plugs, produced by injecting a plastic ear mold compound into the concha and ear canal, attenuated sound reaching the tympanic membrane by 25-70 dB. Binaural interactions were inferred by comparing responses obtained under binaural (no plug) and monaural (ear plug) conditions. 3. Of the total sample of 131 azimuth-sensitive cells whose responses to ear plugging were studied, 27 were sensitive to the azimuth of monaurally presented noise bursts. We refer to these as monaural directional (MD) cells, and this report describes their properties. The remainder of the sample consisted of cells that either required binaural stimulation for azimuth sensitivity (63/131), because they were insensitive to azimuth under unilateral ear plug conditions or responded too unreliably to permit detailed conclusions regarding the effect of ear plugging (41/131). 4. Most (25/27) MD cells received either monaural input (MD-E0) or binaural excitatory/inhibitory input (MD-EI), as inferred from ear plugging. Two MD cells showed other characteristics. The contralateral ear was excitatory for 25/27 MD cells. 5. MD-E0 cells (22%, 6/27) were monaural. They were unaffected by unilateral ear plugging, showing that they received excitatory input from one ear, and that stimulation of the other ear was without apparent effect. On the other hand, some monaural cells in AI were insensitive to the azimuth of noise bursts, showing that sensitivity to monaural directional cues is not a property of all monaural cells in AI. 6. MD-EI cells (70%, 19/27) exhibited an increase in responsiveness on the side of the plugged ear, showing that they received excitatory drive from one ear and inhibitory drive from the other. MD-EI cells remained azimuth sensitive with the inhibitory ear plugged, showing that they were sensitive to monaural directional cues at the excitatory ear.(ABSTRACT TRUNCATED AT 400 WORDS)


1984 ◽  
Vol 51 (5) ◽  
pp. 1028-1039 ◽  
Author(s):  
S. S. Orman ◽  
D. P. Phillips

In the auditory cortex of barbiturate-anesthetized cats, the posterior auditory field (area P) was identified by its tonotopic organization, and single neurons in that field were studied quantitatively with regard to their binaural interactions at their respective best frequencies, using calibrated, sealed stimulating systems. Almost 60% of the neurons studied displayed " summative " binaural interactions in that their responses to binaural, equally intense stimulation of the two ears were stronger than were their responses to monaural stimuli of the same intensity. For these neurons, latent periods were shorter for binaural stimuli than for monaural stimuli. Some field P neurons were sensitive to interaural intensity disparities and manifested that sensitivity in one of two forms. Cells that were excited by stimulation of one ear and inhibited by stimulation of the other typically displayed a sigmoidal relation of spike count to intensive disparity, with spike counts being larger when the disparity favored the contralateral ear. Cells that were unresponsive to monaural stimuli but responded securely to binaural stimuli usually displayed a peaked, nonmonotonic relation of spike count to interaural intensity disparity, with maximal responses being elicited by stimuli with zero or near-zero disparity. Some neurons of low best frequency were sensitive to variations in interaural phase delay. In all cases, this sensitivity was manifested as a cyclical relation of spike count to interaural delay, with the period of the cycle being that of the stimulating tone. The fact that the binaural interactions of field P neurons were similar to those of cells in the primary auditory cortex suggests that the previously described heightened spectral-amplitude selectivity of field P neurons has been achieved without cost to their sensitivity to a variety of parameters of binaural stimulation. The particular sensitivity of cortical neurons to variations in interaural disparities associated with midline or near-midline azimuths might constitute a neural mechanism for the behavioral finding that animals and humans show their greatest acuity in sound localization for stimulus locations in or near the midsagittal plane.


1994 ◽  
Vol 71 (6) ◽  
pp. 2194-2216 ◽  
Author(s):  
F. K. Samson ◽  
P. Barone ◽  
J. C. Clarey ◽  
T. J. Imig

1. Single-unit recordings were carried out in primary auditory cortex (AI) of barbiturate-anesthetized cats. Observations were based on a sample of 131 high-best-frequency (> 5 kHz), azimuth-sensitive neurons. These were identified by their responses to a set of noise bursts, presented in the free field, that varied in azimuth and sound-pressure level (SPL). Each azimuth-sensitive neuron responded well to some levels at certain azimuths, but did not respond well to any level at other azimuths. 2. Unilateral ear plugging was used to infer each neuron's response to monaural stimulation. Ear plugs, produced by injecting a plastic ear mold compound into the external ear, attenuated sound reaching the tympanic membrane by 25–70 dB. The azimuth tuning of a large proportion of the sample (62/131), referred to as binaural directional (BD), was completely dependent upon binaural stimulation because with one ear plugged, these cells were insensitive to azimuth (either responded well at all azimuths or failed to respond at any azimuth) or in a few cases exhibited striking changes in location of azimuth function peaks. This report describes patterns of monaural responses and binaural interactions exhibited by BD neurons and relates them to each cell's azimuth and level tuning. The response of BD cells to ear plugging is consistent with the hypothesis that they derive azimuth tuning from interaural level differences present in noise bursts. Another component of the sample consisted of monaural directional (27/131) cells that derived azimuth tuning in part or entirely from monaural spectral cues. Cells in the remaining portion of the sample (42/131) responded too unreliably to permit specific conclusions. 3. Binaural interactions were inferred by statistical comparison of a cell's responses to monaural (unilateral plug) and binaural (no plug) stimulation. A larger binaural response than either monaural response was taken as evidence for binaural facilitation. A smaller binaural than monaural response was taken as evidence for binaural inhibition. Binaural facilitation was exhibited by 65% (40/62) of the BD sample (facilitatory cells). Many of these exhibited mixed interactions, i.e., binaural facilitation occurred in response to some azimuth-level combinations, and binaural inhibition to others. Binaural inhibition in the absence of binaural facilitation occurred in 35% (22/62) of the BD sample, a majority of which were EI cells, so called because they received excitatory (E) input from one ear (excitatory ear) and inhibitory (I) input from the other (inhibitory ear). One cell that exhibited binaural inhibition received excitatory input from each ear.(ABSTRACT TRUNCATED AT 400 WORDS)


1964 ◽  
Vol 7 (3) ◽  
pp. 271-278 ◽  
Author(s):  
Donald Dirks ◽  
Carolyn Malmquist

Two experiments were conducted to determine the effects of central masking on both air and bone-conduction thresholds. In the first investigation, 10 normal listeners were tested by air conduction and by bone conduction via the mastoid process and the frontal bone as various levels of narrow-band noise were presented to the contralateral ear. Generally, as the noise level increased, there was a small but gradual increase in the threshold on the test ear. However, the threshold shift for frontal bone measurements was always greater than comparable air-conduction or bone-conduction thresholds from the mastoid process. The additional shift in threshold for frontal bone measurements may have been the result of changing from binaural stimulation in quiet to monaural stimulation during the masking conditions. This proposition was investigated in Experiment II. The test ears of 6 subjects were occluded with plugs which induced an appreciable increase in bone-conduction sensitivity. Thus, the frontal bone threshold as well as the mastoid threshold was monaural, even in the quiet condition. If the above proposition were correct, it was predicted that identical shifts in threshold due to central masking would be found for frontal bone measurements as for mastoid measurements. The threshold shifts for air conduction and bone conduction via mastoid or frontal bone vibrator placements were found to be similar.


1975 ◽  
Vol 38 (2) ◽  
pp. 418-429 ◽  
Author(s):  
L. M. Aitkin ◽  
J. Boyd

The responses of 146 cerebellar neurons to tone stimuli were studied in 29 cats anesthetized with chloralose-urethan and in 7 decerebrate preparations. Units were classified as onset or sustained firing. Onset spikes occurred on stimulation of either ear and showed binaural facilitation, while sustained discharges were frequently only excited by monaural stimulation. The latent periods of sustained discharges appeared to be shorter than those of onset responses, and sustained discharges were also more sharply tuned than the onset units. Evidence was presented suggesting that onset responses reflected input from the inferior colliculus and sustained responses, the cochlear nucleus. The sterotyped facilitatory behavior of onset units suggested that a maximal discharge might occur if sounds were of equal intensity at each ear; 26 neurons were examined with variable interaural time or intensity differences and 10 of these exhibited maximal firing when the interaural time and intensity difference was zero--i.e., if the sound was located directly in front of the head.


NeuroImage ◽  
2002 ◽  
Vol 17 (2) ◽  
pp. 1010-1017 ◽  
Author(s):  
François Lazeyras ◽  
Colette Boëx ◽  
Alain Sigrist ◽  
Mohamed L. Seghier ◽  
Grégoire Cosendai ◽  
...  

2016 ◽  
Vol 68 (6) ◽  
pp. 1422-1430 ◽  
Author(s):  
G.D Stanciu ◽  
M. Musteață ◽  
M. Armașu ◽  
G. Solcan

ABSTRACT The present study aimed to analyse the wave morphology, amplitude, latency, and intervals of the brainstem auditory evoked responses (BAERs) in dogs with central vestibular syndrome (CVS) recorded with surface electrodes. Ten dogs with CVS were examined by mono- and binaural stimulation, using the Neuropack electrodiagnostic system, with stimulus intensities of 90 dBSPL. BAERs examinations revealed morphological changes of waves I, II, III, and V and decreased amplitudes of all waves in 7/10 dogs. P values obtained were = 0.014 for wave I amplitude, 0.031 for II, and III and 0.032 for V. Comparing the latencies of waves I, II, III, and V generated by right and left monoaural stimulation in dogs with CVS, we did not observe significant differences (P>0.05). No statistical differences were observed for BAERs latencies of the waves recorded after binaural and monaural stimulation (left or right). As far as we know, this is the first study of BAERs using surface electrodes, obtained from dogs with CVS.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jennifer Resnik ◽  
Daniel B Polley

Cortical neurons remap their receptive fields and rescale sensitivity to spared peripheral inputs following sensory nerve damage. To address how these plasticity processes are coordinated over the course of functional recovery, we tracked receptive field reorganization, spontaneous activity, and response gain from individual principal neurons in the adult mouse auditory cortex over a 50-day period surrounding either moderate or massive auditory nerve damage. We related the day-by-day recovery of sound processing to dynamic changes in the strength of intracortical inhibition from parvalbumin-expressing (PV) inhibitory neurons. Whereas the status of brainstem-evoked potentials did not predict the recovery of sensory responses to surviving nerve fibers, homeostatic adjustments in PV-mediated inhibition during the first days following injury could predict the eventual recovery of cortical sound processing weeks later. These findings underscore the potential importance of self-regulated inhibitory dynamics for the restoration of sensory processing in excitatory neurons following peripheral nerve injuries.


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