scholarly journals Roles of Inhibition in Complex Auditory Responses in the Inferior Colliculus: Inhibited Combination-Sensitive Neurons

2006 ◽  
Vol 95 (4) ◽  
pp. 2179-2192 ◽  
Author(s):  
Kiran Nataraj ◽  
Jeffrey J. Wenstrup

We studied the functional properties and underlying neural mechanisms associated with inhibitory combination-sensitive neurons in the mustached bat's inferior colliculus (IC). In these neurons, the excitatory response to best frequency tones was suppressed by lower frequency signals (usually in the range of 12–30 kHz) in a time-dependant manner. Of 143 inhibitory units, the majority (71%) were type I, in which low-frequency sounds evoked inhibition only. In the remainder, however, the low-frequency inhibitory signal also evoked excitation. Of these, excitation preceded the inhibition in type E/I units (16%), whereas in type I/E units (13%), excitation followed the inhibition. Type E/I and I/E units were distinct in the tuning and threshold sensitivity of low-frequency responses, whereas type I units overlapped the other types in these features. In 71 neurons, antagonists to receptors for glycine [strychnine (STRY)] or GABA [bicuculline (BIC)] were applied microiontophoretically. These antagonists failed to eliminate combination-sensitive inhibition in 92% (STRY), 93% (BIC), and 87% (BIC + STRY) of the type I units tested. However, inhibition was reduced in many neurons. Results were similar for type E/I and I/E inhibitory neurons. The results indicate that there are distinct populations of combination-sensitive inhibited neurons in the IC and that these populations are at least partly independent of glycine or GABAA receptors in the IC. We propose that these populations originate in different brain stem auditory nuclei, that they may be modified by interactions within the IC, and that they may perform different spectrotemporal analyses of vocal signals.

2009 ◽  
Vol 102 (1) ◽  
pp. 167-180 ◽  
Author(s):  
Donald Gans ◽  
Kianoush Sheykholeslami ◽  
Diana Coomes Peterson ◽  
Jeffrey Wenstrup

This report examines temporal features of facilitation and suppression that underlie spectrally integrative responses to complex vocal signals. Auditory responses were recorded from 160 neurons in the inferior colliculus (IC) of awake mustached bats. Sixty-two neurons showed combination-sensitive facilitation: responses to best frequency (BF) signals were facilitated by well-timed signals at least an octave lower in frequency, in the range 16–31 kHz. Temporal features and strength of facilitation were generally unaffected by changes in duration of facilitating signals from 4 to 31 ms. Changes in stimulus rise time from 0.5 to 5.0 ms had little effect on facilitatory strength. These results suggest that low frequency facilitating inputs to high BF neurons have phasic-on temporal patterns and are responsive to stimulus rise times over the tested range. We also recorded from 98 neurons showing low-frequency (11–32 kHz) suppression of higher BF responses. Effects of changing duration were related to the frequency of suppressive signals. Signals <23 kHz usually evoked suppression sustained throughout signal duration. This and other features of such suppression are consistent with a cochlear origin that results in masking of responses to higher, near-BF signal frequencies. Signals in the 23- to 30-kHz range—frequencies in the first sonar harmonic—generally evoked phasic suppression of BF responses. This may result from neural inhibitory interactions within and below IC. In many neurons, we observed two or more forms of the spectral interactions described here. Thus IC neurons display temporally and spectrally complex responses to sound that result from multiple spectral interactions at different levels of the ascending auditory pathway.


1989 ◽  
Vol 62 (1) ◽  
pp. 144-161 ◽  
Author(s):  
L. H. Carney ◽  
T. C. Yin

1. We studied extracellular responses of low-frequency cells in the central nucleus of the inferior colliculus (ICC) to interaural time differences (ITDs) of clicks and compared their responses to ITDs of noise and tones. Most cells that displayed sensitivity to ITDs of clicks responded cyclically as a function of ITD with central peaks and troughs at the same ITDs as in response to noise. The positions of these peaks and troughs also matched those predicted from tonal ITD curves. Thus over the range of physiologically relevant ITDs, the binaural cells in the ICC showed similar sensitivity to ITDs of tones, noise, and clicks. 2. The transient nature of the response to a click allowed association of individual discharges with either the ipsilateral or contralateral stimulus when the binaural stimulus included a large ITD. We studied the influence of the click presented to one side on responses to the click presented to the other side. By examining responses to clicks with large ITDs, ranging from 2 to 3 up to 200 ms, we could identify both excitatory and inhibitory components in response to binaural clicks. 3. For many cells, there was evidence for a short-lasting excitation arising from one or both inputs of the binaural stimulus. Inhibitory interactions could also be demonstrated over a large range of ITDs. Long-lasting, late inhibitory components arose from both contralateral and ipsilateral inputs. In 87% of cells that were driven by the contralateral input, a late inhibitory component originating from the ipsilateral side was detected. In all cells that were driven by the ipsilateral side, a late inhibitory contralateral component was detected. This late inhibition of the excitatory response to one side by a leading stimulus to the other side could be evoked even when the leading stimulus was not effective in evoking an excitatory response. 4. Some cells also exhibited an early inhibitory component that preceded the excitation. An early contralateral inhibition was detected in 44% of cells that were driven by the ipsilateral input, whereas an early ipsilateral component was detected in 17% of cells driven by the contralateral input. 5. We confirmed hypotheses about the laterality and time course of the inhibitory and excitatory components by introducing interaural level differences (ILDs) into the binaural clicks and thus varying the strengths of the different components. 6. Inhibitory components may play a role in shaping the sensitivity of individual cells to ITDs of stimuli other than clicks; they were also apparent in responses to noise.(ABSTRACT TRUNCATED AT 400 WORDS)


2005 ◽  
Vol 93 (6) ◽  
pp. 3294-3312 ◽  
Author(s):  
Kiran Nataraj ◽  
Jeffrey J. Wenstrup

We studied roles of inhibition on temporally sensitive facilitation in combination-sensitive neurons from the mustached bat's inferior colliculus (IC). In these integrative neurons, excitatory responses to best frequency (BF) tones are enhanced by much lower frequency signals presented in a specific temporal relationship. Most facilitated neurons (76%) showed inhibition at delays earlier than or later than the delays causing facilitation. The timing of inhibition at earlier delays was closely related to the best delay of facilitation, but the inhibition had little influence on the duration or strength of the facilitatory interaction. Local iontophoretic application of antagonists to receptors for glycine (strychnine, STRY) and γ-aminobutyric acid (GABA) (bicuculline, BIC) showed that STRY abolished facilitation in 96% of tested units, but BIC eliminated facilitation in only 28%. This suggests that facilitatory interactions are created in IC and reveals a differential role for these neurotransmitters. The facilitation may be created by coincidence of a postinhibitory rebound excitation activated by the low-frequency signal with the BF-evoked excitation. Unlike facilitation, inhibition at earlier delays was not eliminated by application of antagonists, suggesting an origin in lower brain stem nuclei. However, inhibition at delays later than facilitation, like facilitation itself, appears to originate within IC and to be more dependent on glycinergic than GABAergic mechanisms. Facilitatory and inhibitory interactions displayed by these combination-sensitive neurons encode information within sonar echoes and social vocalizations. The results indicate that these complex response properties arise through a series of neural interactions in the auditory brain stem and midbrain.


2003 ◽  
Vol 90 (5) ◽  
pp. 2827-2836 ◽  
Author(s):  
W. R. D'Angelo ◽  
S. J. Sterbing ◽  
E.-M. Ostapoff ◽  
S. Kuwada

In our companion paper, we reported on interaural time difference (ITD)-sensitive neurons that enhanced, suppressed, or did not change their response when identical AM was added to both ears. Here, we first examined physical factors such as the difference in the interaural correlation, spectrum, or energy between the modulated and unmodulated signals. These were insufficient to explain the observed enhancement and suppression. We then examined neural mechanisms by selectively modulating the signal to each ear, varying modulation depth, and adding background noise to the unmodulated signal. These experiments implicated excitatory and inhibitory monaural inputs to the inferior colliculus (IC). These monaural inputs are postulated to adapt to an unmodulated signal and adapt less to a modulated signal. Thus enhancement or suppression is created by the convergence of these excitatory or inhibitory inputs with the inputs from the binaural comparators. Under modulation, the role of the monaural input is to shift the threshold of the IC neuron. Consistent with this role, background noise mimicked the effect of modulation. Functionally, enhancement and suppression may serve in detecting the degree of modulation in a sound source while preserving ITD information.


2008 ◽  
Vol 100 (2) ◽  
pp. 629-645 ◽  
Author(s):  
Diana Coomes Peterson ◽  
Sergiy Voytenko ◽  
Donald Gans ◽  
Alexander Galazyuk ◽  
Jeffrey Wenstrup

In vertebrate auditory systems, specialized combination-sensitive neurons analyze complex vocal signals by integrating information across multiple frequency bands. We studied combination-sensitive interactions in neurons of the inferior colliculus (IC) of awake mustached bats, using intracellular somatic recording with sharp electrodes. Facilitated combinatorial neurons are coincidence detectors, showing maximum facilitation when excitation from low- and high-frequency stimuli coincide. Previous work showed that facilitatory interactions originate in the IC, require both low and high frequency–tuned glycinergic inputs, and are independent of glutamatergic inputs. These results suggest that glycinergic inputs evoke facilitation through either postinhibitory rebound or direct depolarizing mechanisms. However, in 35 of 36 facilitated neurons, we observed no evidence of low frequency–evoked transient hyperpolarization or depolarization that was closely related to response facilitation. Furthermore, we observed no evidence of shunting inhibition that might conceal inhibitory inputs. Since these facilitatory interactions originate in IC neurons, the results suggest that inputs underlying facilitation are electrically segregated from the soma. We also recorded inhibitory combinatorial interactions, in which low frequency sounds suppress responses to higher frequency signals. In 43% of 118 neurons, we observed low frequency–evoked hyperpolarizations associated with combinatorial inhibition. For these neurons, we conclude that low frequency–tuned inhibitory inputs terminate on neurons primarily excited by high-frequency signals; these inhibitory inputs may create or enhance inhibitory combinatorial interactions. In the remainder of inhibited combinatorial neurons (57%), we observed no evidence of low frequency–evoked hyperpolarizations, consistent with observations that inhibitory combinatorial responses may originate in lateral lemniscal nuclei.


2011 ◽  
Vol 105 (4) ◽  
pp. 1785-1797 ◽  
Author(s):  
David A. Bulkin ◽  
Jennifer M. Groh

We investigated the functional architecture of the inferior colliculus (IC) in rhesus monkeys. We systematically mapped multiunit responses to tonal stimuli and noise in the IC and surrounding tissue of six rhesus macaques, collecting data at evenly placed locations and recording nonresponsive locations to define boundaries. The results show a modest tonotopically organized region (17 of 100 recording penetration locations in 4 of 6 monkeys) surrounded by a large mass of tissue that, although vigorously responsive, showed no clear topographic arrangement (68 of 100 penetration locations). Rather, most cells in these recordings responded best to frequencies at the low end of the macaque auditory range. The remaining 15 (of 100) locations exhibited auditory responses that were not sensitive to sound frequency. Potential anatomical correlates of functionally defined regions and implications for midbrain auditory prosthetic devices are discussed.


1987 ◽  
Vol 58 (3) ◽  
pp. 562-583 ◽  
Author(s):  
T. C. Yin ◽  
J. C. Chan ◽  
L. H. Carney

1. We tested the coincidence, or cross-correlation, model of Jeffress, which proposes a neuronal mechanism for sensitivity to interaural time differences (ITDs) in low-frequency cells in the central nucleus of the inferior colliculus (ICC) of the cat. Different tokens of Gaussian noise stimuli were delivered to the two ears. We studied the neural responses to changes in ITDs of these stimuli and examined the manner in which the binaural cells responded to them. All of our results support the idea that the central binaural neurons perform an operation very similar to cross-correlation on the inputs arriving from each side. These inputs are transformed from the actual acoustic signal by the peripheral auditory system, and these transformations are reflected in the properties of the cross-correlations. 2. The responses to ITDs of identical broadband noise stimuli to the two ears varies cyclically as a function of ITD at a frequency close to the best frequency of the neuron. This cyclic response is a consequence of the narrowband filtering of the wideband acoustic signal by the auditory nerve fibers. To examine the effects of using stimuli to the two ears that were correlated to each other to different degrees, we generated pairs of noises. Each pair consisted of one standard noise, which was delivered to one ear, and a linear sum of two standard uncorrelated noises, which was delivered to the other ear. The responses of 34 neurons in the ICC to ITDs of noises with variable interaural coherence were examined. When partially correlated noises were delivered, there was a positive and approximately linear relationship between the degree of modulation of the response as a function of ITD and interaural coherence. The degree of modulation was measured by the synchronization coefficient, or vector strength, over one period of the ITD curve. 3. We examined the effects of altering the interaural phase relationships of the input noise stimuli. The phase of the noise stimuli was changed by digitally filtering the standard noise so that only a phase delay was imposed. The responses to ITDs with differing interaural phase relationships were then studied by delivering a phase-shifted noise to one ear and the standard noise to the other. The ITD curves in response to phase-shifted noise were shifted by about the same amount as the shift of the stimulus; the shift of the response was measured with respect to the case with identical noises to the two ears.(ABSTRACT TRUNCATED AT 400 WORDS)


2021 ◽  
Vol 15 ◽  
Author(s):  
Arianna Gentile Polese ◽  
Sunny Nigam ◽  
Laura M. Hurley

Neuromodulatory systems may provide information on social context to auditory brain regions, but relatively few studies have assessed the effects of neuromodulation on auditory responses to acoustic social signals. To address this issue, we measured the influence of the serotonergic system on the responses of neurons in a mouse auditory midbrain nucleus, the inferior colliculus (IC), to vocal signals. Broadband vocalizations (BBVs) are human-audible signals produced by mice in distress as well as by female mice in opposite-sex interactions. The production of BBVs is context-dependent in that they are produced both at early stages of interactions as females physically reject males and at later stages as males mount females. Serotonin in the IC of males corresponds to these events, and is elevated more in males that experience less female rejection. We measured the responses of single IC neurons to five recorded examples of BBVs in anesthetized mice. We then locally activated the 5-HT1A receptor through iontophoretic application of 8-OH-DPAT. IC neurons showed little selectivity for different BBVs, but spike trains were characterized by local regions of high spike probability, which we called “response features.” Response features varied across neurons and also across calls for individual neurons, ranging from 1 to 7 response features for responses of single neurons to single calls. 8-OH-DPAT suppressed spikes and also reduced the numbers of response features. The weakest response features were the most likely to disappear, suggestive of an “iceberg”-like effect in which activation of the 5-HT1A receptor suppressed weakly suprathreshold response features below the spiking threshold. Because serotonin in the IC is more likely to be elevated for mounting-associated BBVs than for rejection-associated BBVs, these effects of the 5-HT1A receptor could contribute to the differential auditory processing of BBVs in different behavioral subcontexts.


2003 ◽  
Vol 90 (5) ◽  
pp. 2818-2826 ◽  
Author(s):  
S. J. Sterbing ◽  
W. R. D'Angelo ◽  
E.-M. Ostapoff ◽  
S. Kuwada

Most sounds in the natural environment are amplitude-modulated (AM). To determine if AM alters the neuronal sensitivity to interaural time differences (ITDs) in low-frequency sounds, we tested neuronal responses to a binaural beat stimulus with and without modulation. We recorded from single units in the inferior colliculus of the unanesthetized rabbit. We primarily used low frequency (∼25 Hz) modulation that was identical at both ears. We found that modulation could enhance, suppress, or not affect the discharge rate. In extreme cases, a neuron that showed no response to the unmodulated binaural beat did so when modulation was added to both ears. At the other extreme, a neuron that showed sensitivity to the unmodulated binaural beat ceased firing with modulation. Modulation could also affect the frequency range of ITD sensitivity, best ITD, and ITD tuning width. Despite these changes in individual neurons, averaging across all neurons, the peak and width of the population ITD function remained unchanged. Because ITD-sensitive neurons also time-locked to the modulation frequency, the location and sound attributes are processed simultaneously by these neurons.


1992 ◽  
Vol 1 (4) ◽  
pp. 52-55 ◽  
Author(s):  
Gail L. MacLean ◽  
Andrew Stuart ◽  
Robert Stenstrom

Differences in real ear sound pressure levels (SPLs) with three portable stereo system (PSS) earphones (supraaural [Sony Model MDR-44], semiaural [Sony Model MDR-A15L], and insert [Sony Model MDR-E225]) were investigated. Twelve adult men served as subjects. Frequency response, high frequency average (HFA) output, peak output, peak output frequency, and overall RMS output for each PSS earphone were obtained with a probe tube microphone system (Fonix 6500 Hearing Aid Test System). Results indicated a significant difference in mean RMS outputs with nonsignificant differences in mean HFA outputs, peak outputs, and peak output frequencies among PSS earphones. Differences in mean overall RMS outputs were attributed to differences in low-frequency effects that were observed among the frequency responses of the three PSS earphones. It is suggested that one cannot assume equivalent real ear SPLs, with equivalent inputs, among different styles of PSS earphones.


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