Binaural processing of sound pressure level in the inferior colliculus

1987 ◽  
Vol 57 (4) ◽  
pp. 1130-1147 ◽  
Author(s):  
M. N. Semple ◽  
L. M. Kitzes

The central auditory system could encode information about the location of a high-frequency sound source by comparing the sound pressure levels at the ears. Two potential computations are the interaural intensity difference (IID) and the average binaural intensity (ABI). In this study of the central nucleus of the inferior colliculus (ICC) of the anesthetized gerbil, we demonstrate that responses of 85% of the 97 single units in our sample were jointly influenced by IID and ABI. For a given ABI, discharge rate of most units is a sigmoidal function of IID, and peak rates occur at IIDs favoring the contralateral ear. Most commonly, successive increments of ABI cause successive shifts of the IID functions toward IIDs favoring the ipsilateral ear. Neurons displaying this behavior include many that would conventionally be classified EI (receiving predominantly excitatory input arising from one ear and inhibitory input from the other), many that would be classified EE (receiving predominantly excitatory input arising from each ear), and all that are responsive only to contralateral stimulation. The IID sensitivity of a very few EI neurons is unaffected by ABI, except near threshold. Such units could provide directional information that is independent of source intensity. A few EE neurons are very sensitive to ABI, but are minimally sensitive to IID. Nevertheless, our data indicate that responses of most EE units in ICC are strongly dominated by excitation of contralateral origin. For some units, discharge rate is nonmonotonically related to IID and is maximal when the stimuli at the two ears are of comparable sound pressure. This preference for zero IID is common for all binaural levels. Many EI neurons respond nonmonotonically to ABI. Discharge rates are greater for IIDs representative of contralateral space and are maximal at a single best ABI. For a subset of these neurons, the influence arising from the ipsilateral ear is comprised of a mixture of excitation and inhibition. As a consequence, discharge rates are nonmonotonically related not only to ABI but also to IID. This dual nonmonotonicity creates a clear focus of peak response at a particular ABI/IID combination. Because of their mixed monaural influences, such units would be ascribed to different classes of the conventional (EE/EI) binaural classification scheme depending on the binaural level presented. Several response classes were identified in this study, and each might contribute differently to the encoding of spatial information.(ABSTRACT TRUNCATED AT 400 WORDS)

1987 ◽  
Vol 57 (4) ◽  
pp. 1185-1200 ◽  
Author(s):  
L. M. Aitkin ◽  
R. L. Martin

The responses to changes in stimulus azimuth of 220 high best-frequency (BF) (greater than 3 kHz) units in the central nucleus of the inferior colliculus of the anesthetized cat were studied with BF tones (220 units) and noise stimuli (84 units). By this means we hoped to gain some insights into the way the azimuthal locations of high BF stimuli were represented in the inferior colliculus. For each unit the discharge rate was determined for stimuli located along a plane tilted at 20 degrees above the horizontal. This plane was chosen to optimize pinna directionality. Locations in the frontal field were sampled in 10-20 degree steps around a 170 degree arc. These measurements were repeated at a number of different stimulus intensities until the directional properties of the unit became clear. Units for which the functions relating discharge rate to azimuth for a given stimulus showed a clear feature (peak or border), the azimuthal location of which varied little with intensities between 20 and 40 dB above threshold, were defined as being azimuth selective for that stimulus. Only 13% of units were azimuth selective for BF tones, whereas 44% were selective for noise. Many azimuth functions for selective units were of the plateau-shaped type for which relatively high discharge rates occurring at most contralateral azimuths declined steeply to near zero and remained low for most ipsilateral azimuths. These plateau-shaped functions were most common for tonal stimuli. Other functions showed a fixed azimuth of maximum firing (best azimuth); these were more common for noise than for tonal stimuli. Detailed azimuth functions for both tone and noise stimuli were measured for 63 units. Some exhibited the same kind of azimuth function to both stimuli. However, 18 units were azimuth selective to noise but not to tones. The borders of plateau-shaped functions obtained using both noise and tonal stimuli were concentrated within 20 degrees of the median plane. Very few units had borders that spanned peripheral ipsilateral or contralateral azimuths. Although the best azimuths of some noise azimuth functions were observed to lie at these peripheral azimuths, the majority occurred around 20 degrees contralateral to the median plane. The recording sites for units were related to a three-by-three matrix of rostrocaudal and mediolateral locations across the central nucleus. Units that were azimuth selective to noise were distributed fairly evenly throughout the central nucleus, whereas units azimuth selective to tones formed highest proportions rostrally.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 82 (1) ◽  
pp. 164-175 ◽  
Author(s):  
Kevin A. Davis ◽  
Ramnarayan Ramachandran ◽  
Bradford J. May

Single units in the central nucleus of the inferior colliculus (ICC) of unanesthetized decerebrate cats can be grouped into three distinct types (V, I, and O) according to the patterns of excitation and inhibition revealed in contralateral frequency response maps. This study extends the description of these response types by assessing their ipsilateral and binaural response map properties. Here the nature of ipsilateral inputs is evaluated directly using frequency response maps and compared with results obtained from methods that rely on sensitivity to interaural level differences (ILDs). In general, there is a one-to-one correspondence between observed ipsilateral input characteristics and those inferred from ILD manipulations. Type V units receive ipsilateral excitation and show binaural facilitation (EE properties); type I and type O units receive ipsilateral inhibition and show binaural excitatory/inhibitory (EI) interactions. Analyses of binaural frequency response maps show that these ILD effects extend over the entire receptive field of ICC units. Thus the range of frequencies that elicits excitation from type V units is expanded with increasing levels of ipsilateral stimulation, whereas the excitatory bandwidth of type I and O units decreases under the same binaural conditions. For the majority of ICC units, application of bicuculline, an antagonist for GABAA-mediated inhibition, does not alter the basic effects of binaural stimulation; rather, it primarily increases spontaneous and maximum discharge rates. These results support our previous interpretations of the putative dominant inputs to ICC response types and have important implications for midbrain processing of competing free-field sounds that reach the listener with different directional signatures.


1987 ◽  
Vol 58 (3) ◽  
pp. 543-561 ◽  
Author(s):  
J. C. Chan ◽  
T. C. Yin ◽  
A. D. Musicant

1. We studied cells in the central nucleus of the inferior colliculus of the cat that were sensitive to interaural time delays (ITDs) in order to evaluate the influence of the stimulus spectrum of noise signals. Stimuli were sharply filtered low-, high-, and band-pass noise signals whose cutoff frequencies and bandwidths were systematically varied. The responses to ITDs of these noise signals were compared with responses obtained to ITDs of broadband noise and pure tones. 2. The discharge rate in response to band-pass noise as a function of ITD was usually a cyclic function with decreasing peak amplitudes at longer ITDs. The reciprocal of the mean interval between adjacent peaks indicated how rapidly the response rate varied with ITD and was termed the response frequency (RF). This RF was approximately equal to the median frequency of the stimulus spectrum filtered by the cell's sync-rate curve, which was the product of the synchronization to interaural phase and the discharge rate plotted against frequency. This suggests that the RF was determined by all the spectral components in the stimulus that fell within the frequency range in which the cell's response was synchronized. The contribution of each component was proportional to the sync-rate for that frequency. 3. The central peak of the ITD function usually fell within the physiological range of ITDs (+/- 400 microseconds). The location of this peak did not vary significantly with changes in stimulus spectrum by comparison with responses to tones of different frequency. Its shape also remained constant, except for a decrease in width when high-frequency components within the range of the sync-rate curve were added to the stimulus. A few cells responded with a minimal discharge instead of a maximal near-zero ITD, and this central minimum had similar properties as the central peak. The amplitude of the secondary peaks of the ITD function decreased as the stimulus bandwidth that overlapped the sync-rate curve broadened. 4. The sum of the ITD functions to two band-pass signals was similar to that of a broadband signal whose spectrum was composed of the sum of the band-pass spectra. 5. From these binaural responses we could make inferences about the response characteristics of the monaural inputs to binaural neurons. We then verified these predictions by studying responses of low-frequency trapezoid body fibers to band-pass noises.


1990 ◽  
Vol 64 (2) ◽  
pp. 582-597 ◽  
Author(s):  
B. J. Blatchley ◽  
J. F. Brugge

1. Responses of single neurons to monaural or binaural CF tones delivered through a closed and calibrated sound delivery system were studied in the central nucleus of the inferior colliculus (ICC) in ketamine and barbiturate-anesthetized kittens 4-105 days old. 2. Neurons from young kittens had elevated thresholds, some greater than 100 dB in the youngest kittens tested. Average thresholds in the ICC matched those previously measured in the auditory nerve (AN), cochlear nuclei (CN), and auditory cortex (CTX), suggesting that the drop in threshold as a function of age is primarily determined by development at the periphery. 3. Minimal first-spike latencies were relatively long in the youngest kittens, approaching adult values by the end of the third postnatal week. Latencies were distributed between values previously determined for the CN and auditory cortex and can be attributed to the centripetal development of the auditory system. 4. The range of frequencies that were effective in exciting ICC neurons was restricted in young kittens. Neurons having characteristic frequencies (CFs) greater than 7 kHz were not recorded before postnatal day 10. CF distribution matched that obtained in previous experiments from AN, CN, and CTX, reflecting the development of the cochlea. 5. Both monotonic and nonomonotonic spike count-versus-intensity functions were found in the youngest kittens. There was a tendency for monotonic functions from the youngest kittens to be steeper than those from older kittens. No age-related changes in the shapes of non-monotonic functions were found. 6. Sensitivity to interaural intensity difference (IID), tested by holding the intensity to the excitatory ear at a suprathreshold level and increasing the intensity of the stimulus to the inhibitory ear, was exhibited as early as 8 days after birth. The majority of the cells exhibiting sensitivity to IID (89.5%) were classified as EI cells, and almost all IID sensitive cells had CFs between 3 and 25 kHz. Within our sample the shapes of IID functions, as well as the operating range of the IID functions, closely resembled those obtained from the adult cat. Thresholds of excitation and of inhibition were highly correlated, suggesting that the ipsilateral and contralateral inputs to the ICC develop as a matched set. 7. Sensitivity to interaural phase difference (IPD), tested either by shifting the onset phase of a CF tone to one ear relative to the other or by presenting tones of slightly different frequency to the two ears, was present as early as 12 days after birth.(ABSTRACT TRUNCATED AT 400 WORDS)


2006 ◽  
Vol 96 (2) ◽  
pp. 813-825 ◽  
Author(s):  
Yoram Gutfreund ◽  
Eric I. Knudsen

Auditory neurons in the owl’s external nucleus of the inferior colliculus (ICX) integrate information across frequency channels to create a map of auditory space. This study describes a powerful, sound-driven adaptation of unit responsiveness in the ICX and explores the implications of this adaptation for sensory processing. Adaptation in the ICX was analyzed by presenting lightly anesthetized owls with sequential pairs of dichotic noise bursts. Adaptation occurred in response even to weak, threshold-level sounds and remained strong for more than 100 ms after stimulus offset. Stimulation by one range of sound frequencies caused adaptation that generalized across the entire broad range of frequencies to which these units responded. Identical stimuli were used to test adaptation in the lateral shell of the central nucleus of the inferior colliculus (ICCls), which provides input directly to the ICX. Compared with ICX adaptation, adaptation in the ICCls was substantially weaker, shorter lasting, and far more frequency specific, suggesting that part of the adaptation observed in the ICX was attributable to processes resident to the ICX. The sharp tuning of ICX neurons to space, along with their broad tuning to frequency, allows ICX adaptation to preserve a representation of stimulus location, regardless of the frequency content of the sound. The ICX is known to be a site of visually guided auditory map plasticity. ICX adaptation could play a role in this cross-modal plasticity by providing a short-term memory of the representation of auditory localization cues that could be compared with later-arriving, visual–spatial information from bimodal stimuli.


1990 ◽  
Vol 63 (3) ◽  
pp. 570-591 ◽  
Author(s):  
D. R. Irvine ◽  
G. Gago

1. Development of models of the manner in which interaural intensity differences (IIDs), the major binaural cue for the azimuthal location of high-frequency sounds, are coded by populations of neurons requires knowledge of the extent to which the IID sensitivity of individual neurons is invariant with changes in sound pressure level (SPL) and other stimulus parameters. To examine this tissue, recordings were obtained from a large sample (n = 458) of neurons with characteristic frequency (CF) greater than 3 kHz in the central nucleus of the inferior colliculus (ICC) of anesthetized cats. The sensitivity to IIDs and the effects of changes in SPL on this sensitivity were examined in neurons receiving excitatory contralateral input and inhibitory or mixed inhibitory/facilitatory ipsilateral input (EI neurons). 2. The form of an EI neuron's IID sensitivity and the effects of changes in SPL on that sensitivity were found to be determined in part by the characteristics of the neuron's rate-intensity function for monaural contralateral stimulation, and detailed rate-intensity functions were therefore obtained for 91 neurons. Many ICC neurons have nonmonotonic rate-intensity functions, the proportion so classified depending on the criterion of nonmonotonicity employed. 3. IID sensitivity functions for CF tonal stimuli were obtained at one or more intensities for 90 neurons, using 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 in which a function was obtained for each unit, the majority of EI neurons (72%) had monotonic (sigmoidal) or near-monotonic IID sensitivity functions. The remainder had nonmonotonic (peaked) IID sensitivity functions, which were attributable either to mixed inhibitory and facilitatory ipsilateral influences or to the fact that the effects of ipsilateral stimulation were superimposed on nonmonotonic effects of changes in intensity at the excitatory ear. 4. IID sensitivity was examined at two or more ABIs (3-5 in most cases) for 40 neurons classified as having monotonic or near-monotonic functions in the standard ABI range and for 7 neurons classified as nonmonotonic. For a small proportion of neurons with monotonic IID sensitivity functions, the form of the function was relatively invariant with changes in ABI. In those monotonic neurons in which the form of the IID sensitivity function varied with changes in ABI, the most common type of variation was that the position of the sloping portion of the function shifted systematically in the direction of larger IIDs favoring the ipsilateral ear as ABI increased.(ABSTRACT TRUNCATED AT 400 WORDS)


2019 ◽  
Author(s):  
Nathaniel T. Greene ◽  
Kevin A. Davis

ABSTRACTNeurons in the central nucleus of the inferior colliculus (ICC) of decerebrate cats show three major response patterns when tones of different frequencies and levels are presented to the contralateral ear. The frequency response maps of type I units uniquely exhibit a narrowly tuned I-shaped area of excitation around best frequency (the most sensitive frequency) and flanking regions of inhibition at lower and higher frequencies. Type I units receive ipsilateral inhibition, and show binaural excitatory/inhibitory interactions. Lateral superior olive (LSO) principal cells display a similar receptive field organization and sensitivity to interaural level differences (ILDs) and project directly to the ICC, therefore are supposed to be the dominant source of excitatory input for type I units. To test this hypothesis, the responses of ICC units were compared before and after reversible inactivation of the LSO by injection of the non-specific excitatory amino-acid antagonist kynurenic acid. When excitatory activity within the LSO was blocked, many ICC type I units (~50%) were silenced or showed substantially decreased activitycomparable. By contrast, the responses of the other two ICC unit types were largely unaffected. With regard to the origins of unaffected ICC type I units, evidence indicates that the LSO was inactivated in an incomplete, anisotropic manner, and the monaural and binaural responses of such units are similar to those of affected type I units. Taken together, these results support the interpretation that most type I units are the midbrain components of a functionally segregated ILD processing pathway initiated by the LSO.


1995 ◽  
Vol 73 (2) ◽  
pp. 449-467 ◽  
Author(s):  
R. Snyder ◽  
P. Leake ◽  
S. Rebscher ◽  
R. Beitel

1. Cochlear implants have been available for > 20 yr to profoundly deaf adults who have lost their hearing after acquiring language. The success of these cochlear prostheses has encouraged the application of implants in prelingually deaf children as young as 2 yr old. To further characterize the consequences of chronic intracochlear electrical stimulation (ICES) on the developing auditory system, the temporal-response properties of single neurons in the inferior colliculus (IC) were recorded in deafened anesthetized cats. 2. The neurons were excited by unilateral ICES with the use of a scala tympani stimulating electrode implanted in the left cochlea. The electrodes were modeled after those used in cochlear implant patients. Responses of 443 units were recorded extracellularly in the contralateral (right) IC with the use of tungsten microelectrodes. Recordings were made in three groups of adult animals: neonatally deafened/chronically stimulated animals (192 units), neonatally deafened/unstimulated animals (80 units), and adult-deafened/prior normal-hearing animals (171 units). The neonatally deafened cats were deafened by multiple intramuscular injections of neomycin sulfate and never developed demonstrable hearing. Most of the deafened, chronically stimulated animals were implanted at 6 wk of age and stimulated at suprathreshold levels for 4 h/day for 3-6 mo. The unstimulated animals were implanted as adults at least 2 wk before the acute physiological experiment and were left unstimulated until the acute experiment was conducted. Prior-normal adults were deafened and implanted at least 2 wk before the acute experiment. 3. IC units were isolated with the use of a search stimulus consisting of three cycles of a 100-Hz sinusoid. Most units responded to sinusoidal stimulation with either an onset response or a sustained response. Onset units were the predominant unit found in the external nucleus, whereas sustained units were found almost exclusively in the central nucleus. The temporal resolution of sustained response units was measured with the use of pulse trains of increasing frequency and calculating the discharges/pulse. 4. The range of electrical pulse frequencies to which IC units responded in a temporally synchronized manner was comparable with that produced by acoustic stimulation. The discharge rate/pulse-versus-pulse frequency transfer functions of IC units were uniformly low-pass, although they varied widely in their cutoff frequencies. This variation in pulse response was partially correlated with the unit's response to sinusoids. Most onset neurons responded only to pulse frequencies below 20 pulses per second (pps). Most sustained units responded best to pulse frequencies < 100 pps, and most ceased to respond to pulse frequencies > 300 pps.(ABSTRACT TRUNCATED AT 400 WORDS)


1992 ◽  
Vol 67 (6) ◽  
pp. 1428-1436 ◽  
Author(s):  
A. Moiseff ◽  
T. Haresign

1. We studied the response of single units in the central nucleus of the inferior colliculus (ICc) of the barn owl (Tyto alba) to continuously varying interaural phase differences (IPDs) and static IPDs. Interaural phase was varied in two ways: continuously, by delivering tones to each ear that varied by a few hertz (binaural beat, Fig. 1), and discretely, by delaying in fixed steps the phase of sound delivered to one ear relative to the other (static phase). Static presentations were repeated at several IPDs to characterize interaural phase sensitivity. 2. Units sensitive to IPDs responded to the binaural beat stimulus over a broad range of delta f(Fig. 4). We selected a 3-Hz delta f for most of our comparative measurements on the basis of constraints imposed by our stimulus generation system and because it allowed us to reduce the influence of responses to stimulus onset and offset (Fig. 3A). 3. Characteristic interaural time or phase sensitivity obtained by the use of the binaural beat stimulus were comparable with those obtained by the use of the static technique (Fig. 5; r2 = 0.93, Fig. 6). 4. The binaural beat stimulus facilitated the measurement of characteristic delay (CD) and characteristic phase (CP) of auditory units. We demonstrated that units in the owl's inferior colliculus (IC) include those that are maximally excited by specific IPDs (CP = 0 or 1.0) as well as those that are maximally suppressed by specific IPDs (CP = 0.5; Figs. 7 and 8). 5. The selectivity of units sensitive to IPD or interaural time difference (ITD) were weakly influenced by interaural intensity difference (IID).(ABSTRACT TRUNCATED AT 250 WORDS)


1996 ◽  
Vol 75 (1) ◽  
pp. 171-183 ◽  
Author(s):  
J. Wang ◽  
R. J. Salvi ◽  
N. Powers

1. The discharge patterns of 40 neurons in the central nucleus of the inferior colliculus (ICC) of the chinchilla were evaluated before and after acute cochlea trauma from intense tone exposure. Single-unit recordings were obtained from neurons in the ICC contralateral to the sound-stimulated ear. Cochlear trauma was induced with a short-duration (15-25 min), high-intensity pure tone (95-115 dB SPL) at a frequency above the neuron's characteristic frequency (CF). The aim of the traumatizing exposure was to damage the peripheral sensory receptors associated with frequencies above the neuron's CF. The damage was expected to attenuate inputs to the neural circuits responsible for activating the inhibitory sidebands above CF. 2. Three types of frequency-threshold tuning curves were observed before the exposure: 1) open V tuning curves (55%) that became wider as sound intensity increased; 2) level-tolerant tuning curves (37.5%) that maintained a very narrow bandwidth even at high sound intensities; and 3) upper-threshold tuning curves (7.5%) in which excitatory responses were elicited at low and moderate intensities, but not at high intensities. The traumatizing exposure caused a dramatic widening of level-tolerant (80% of sample) and upper-threshold tuning curves (100% of sample) at high sound intensities but caused almost no change in the low-threshold tip of the tuning curves. By contrast, tuning curves with an open V configuration were generally unaffected (approximately 90% of sample) by the traumatizing exposure. 3. Discharge rate-level functions in the ICC were of two general types: 1) strongly nonmonotonic (60%) or 2) saturating, monotonic (40%). The traumatizing exposure caused a significant increase in the suprathreshold discharge rates in 70% of all neurons studied. Among the neurons with strongly nonmonotonic discharge rate-level functions, 93% showed a significant increase in discharge rate. 4. The poststimulus time histograms (PSTH) to tone bursts were of three main types: 1) onset, 2) pauser, and 3) sustained responders. The traumatizing exposure had almost no effect on the PSTH of onset or sustained responders. However, pause PSTH frequently (75%) showed a significant decrease in the pause duration and an increase in the sustained discharge rate following the pause after the exposure. 5. The results suggest that the response properties of neurons with extremely narrow tuning curves and nonmonotonic discharge rate-level functions are shaped by an inhibitory circuit that is activated by frequencies above the high-frequency flank of the tuning curve. This inhibitory circuit modifies the excitatory response in the following ways: 1) it narrows the excitatory response area at suprathreshold intensities particularly at frequencies below CF, 2) it alters the shape of the discharge rate-level function by suppressing the discharge rates at suprathreshold intensities, and 3) it modifies the temporal discharge pattern of the pause PSTH by suppressing neural activity that occurs after the onset response. The effects of these inhibitory inputs can be reduced (disinhibition) by damaging the sensory cells in the inner ear that activate this circuit. The exact locus of the inhibitory circuit(s) is unknown but may involve inhibitory inputs located at the level of the cochlear nucleus and/or at levels up to the inferior colliculus.


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