Interaural Intensity Differences Sensitivity Research Articles

Mechanisms underlying azimuth selectivity in the auditory cortex of the pallid bat

This study focused on mechanisms underlying azimuth selectivity in the primary auditory cortex (A1) of pallid bats. The pallid bat listens to prey-generated noise (5–35 kHz) to localize and hunt terrestrial prey. The region of A1 tuned between 5 and 35 kHz consists of two clusters of neurons distinguished by interaural intensity difference (IID) selectivity: binaurally inhibited (EI) and peaked. The first aim of this study was to use sequential dichotic/free-field stimulation to test the hypothesis that IID is the primary cue underlying azimuth selectivity in neurons tuned in the prey-generated noise frequency band. IID selectivity and ear directionality at the neuron's characteristic frequency (CF) were used to predict azimuth selectivity functions. The predicted azimuth selectivity was compared with the actual azimuth selectivity from the same neurons. Prediction accuracy was similarly high for EI neurons and peaked neurons with low CF, whereas predictions were increasingly inaccurate with increasing CF among the peaked neurons. The second aim of this study was to compare azimuth selectivity obtained with noise and CF tones to determine the extent to which stimulus bandwidth influences azimuth selectivity in neurons with different binaural properties. The azimuth selectivity functions were similar for the two stimuli in the majority of EI neurons. A greater percentage of peaked neurons showed differences in their azimuth selectivity for noise and tones. This included neurons with multiple peaks when tested with tones and a single peak when tested with noise. Taken together, data from the two aims suggest that azimuth tuning of EI neurons is primarily dictated by IID sensitivity at CF. Peaked neurons, particularly those with high CF, may integrate IID sensitivity across frequency to generate azimuth selectivity for broadband sound. The data are consistent with those found in cat and ferret A1 in that binaurally facilitated neurons depend to a greater extent (compared to EI neurons) on spectral integration of binaural properties to generate azimuth selectivity for broadband stimuli.

Low‐voltage activated Kv1.1 subunits are crucial for the processing of sound source location in the lateral superior olive in mice

Voltage-gated potassium (Kv) channels containing Kv1.1 subunits are strongly expressed in neurons that fire temporally precise action potentials (APs). In the auditory system, AP timing is used to localize sound sources by integrating interaural differences in time (ITD) and intensity (IID) using sound arriving at both cochleae. In mammals, the first nucleus to encode IIDs is the lateral superior olive (LSO), which integrates excitation from the ipsilateral ventral cochlear nucleus and contralateral inhibition mediated via the medial nucleus of the trapezoid body. Previously we reported that neurons in this pathway show reduced firing rates, longer latencies and increased jitter in Kv1.1 knockout (Kcna1−/−) mice. Here, we investigate whether these differences have direct impact on IID processing by LSO neurons. Single-unit recordings were made from LSO neurons of wild-type (Kcna1+/+) and from Kcna1−/− mice. IID functions were measured to evaluate genotype-specific changes in integrating excitatory and inhibitory inputs. In Kcna1+/+ mice, IID sensitivity ranged from +27 dB (excitatory ear more intense) to −20 dB (inhibitory ear more intense), thus covering the physiologically relevant range of IIDs. However, the distribution of IID functions in Kcna1−/− mice was skewed towards positive IIDs, favouring ipsilateral sound positions. Our computational model revealed that the reduced performance of IID encoding in the LSO of Kcna1−/− mice is mainly caused by a decrease in temporal fidelity along the inhibitory pathway. These results imply a fundamental role for Kv1.1 in temporal integration of excitation and inhibition during sound source localization.

Erratum to: Regularly firing neurons in the inferior colliculus have a weak interaural intensity difference sensitivity

Erratum to: Regularly firing neurons in the inferior colliculus have a weak interaural intensity difference sensitivity

Regularly firing neurons in the inferior colliculus have a weak interaural intensity difference sensitivity

The spike discharge regularity may be important in the processing of information in the auditory pathway. It has already been shown that many cells in the central nucleus of the inferior colliculus fire regularly in response to monaural stimulation by the best frequency tones. The aim of this study was to find how the regularity of units was affected by adding ipsilateral tone, and how interaural intensity difference sensitivity is related to regularity. Single unit recordings were performed from 66 units in the inferior colliculus of the anaesthetized guinea pig in response to the best frequency tone. Regularity of firing was measured by calculating the coefficient of variation as a function of time of a unit's response. There was a positive correlation between coefficient of variation and interaural intensity difference sensitivity, indicating that highly regular units had very weak and irregular units had strong interaural intensity difference sensitivity responses. Three effects of binaural interaction on the sustained regularity were observed: constant coefficient of variation despite change in rate (66% of the units), negative (20%) and positive (13%) rate-CV relationships. A negative rate-coefficient of variation relationship was the dominant pattern of binaural interaction on the onset regularity.

Tuning bat LSO neurons to interaural intensity differences through spike-timing dependent plasticity

Bats, like other mammals, are known to use interaural intensity differences (IID) to determine azimuthal position. In the lateral superior olive (LSO) neurons have firing behaviors which vary systematically with IID. Those neurons receive excitatory inputs from the ipsilateral ear and inhibitory inputs from the contralateral one. The IID sensitivity of a LSO neuron is thought to be due to delay differences between the signals coming from both ears, differences due to different synaptic delays and to intensity-dependent delays. In this paper we model the auditory pathway until the LSO. We propose a learning scheme where inputs to LSO neurons start out numerous with different relative delays. Spike timing-dependent plasticity (STDP) is then used to prune those connections. We compare the pruned neuron responses with physiological data and analyse the relationship between IID's of teacher stimuli and IID sensitivities of trained LSO neurons.

Development of functional organization of the pallid bat auditory cortex

The primary auditory cortex is characterized by a tonotopic map and a clustered organization of binaural properties. The factors involved in the development of overlain representation of these two properties are unclear. We addressed this issue in the auditory cortex of the pallid bat. The adult pallid bat cortex contains a systematic relationship between best frequency (BF) and binaural properties. Most neurons with BF <30 kHz are binaurally inhibited (EO/I), while most neurons with BF >30 kHz are monaural (EO). As in other species, binaural properties are clustered. The EO/I cluster contains a systematic map of interaural intensity difference (IID) sensitivity. We asked if these properties are present at the time the bat acquires its full audible range (postnatal day [P] 15). Tonotopy, relationship between BF and binaural properties, and the map of IID sensitivity are adult-like at P15. However, binaural facilitation is only observed in pups older than P25. Frequency selectivity shows a BF-dependent sharpening during development. Thus, overlain representation of binaural properties and tonotopy in the pallid bat cortex is remarkably adult-like at an age when the full audible range is first present, suggesting an experience-independent development of overlapping feature maps.

Mechanisms underlying the sensitivity of neurons in the lateral superior olive to interaural intensity differences.

The initial processing of interaural intensity differences (IIDs), the major cue to the azimuthal location of high-frequency sounds in mammals, is carried out by neurons in the lateral superior olivary nucleus (LSO) that receive excitatory input from the ipsilateral ear and inhibitory input from the contralateral ear (IE neurons). The "latency" hypothesis asserts that it is the effects of intensity differences on the latency, and hence the relative timing, of the synaptic inputs to these neurons that is the basis of their sensitivity to IIDs, while other models assign the major role to changes in the relative amplitude of the inputs. To test the latency hypothesis and to determine the contributions of changes in the relative timing and amplitude of synaptic inputs to the IID sensitivity of LSO neurons, a method was developed of generating sets of stimuli that produced either the same changes in the relative timing of inputs without any change in their amplitude (equivalent interaural time difference stimuli) or the same differences in amplitude without any difference in timing (delay-cancelled IID stimuli) as a given range of IIDs. Data were obtained from a sample of IE neurons in the LSO of anesthetized rats using these stimulus paradigms and click and tone-burst stimuli. For click stimuli, the IID sensitivity of a small proportion of neurons was explained entirely by sensitivity to differences in input timing, but the sensitivity of most neurons reflected either sensitivity to the relative amplitude of inputs or to the joint operation of both factors. In neurons whose sensitivity was tested at a number of different absolute sound pressure levels (SPLs), the relative contributions of the two factors tended to differ at different SPLs. The IID sensitivity of onset responses to tone stimuli could be classified into the same three categories but was explained for a larger proportion of neurons by sensitivity to differences in input timing. The IID sensitivity of the late response component of neurons with sustained responses to tones in all cases reflected sensitivity to the relative amplitude of the inputs. The results confirm the contribution of changes in latency produced by intensity changes to the IID sensitivity of the onset responses of many IE neurons in LSO but require rejection of the strong form of the latency hypothesis, which asserts that this factor alone accounts for such sensitivity.

Processing of interaural intensity differences in the LSO: role of interaural threshold differences.

Cells in the lateral superior olive (LSO) are known to be sensitive to interaural intensity differences (IIDs) in that they are excited by IIDs that favor the ipsilateral ear and inhibited by IIDs that favor the contralateral ear. For each LSO neuron there is a particular IID that causes a complete inhibition of discharges, and the IID of complete inhibition varies from neuron to neuron. This variability in IID sensitivity among LSO neurons is a key factor that allows for the coding of a variety of IIDs among the population of cells. A fundamental question concerning the coding of IIDs is: how does each cell in the LSO derive its particular IID sensitivity? Although there have been a large number of neurophysiological studies on the LSO, this question has received little attention. Indeed, the only reports that have directly addressed this question are those of Reed and Blum, who modeled the binaural properties of LSO neurons and proposed that the IID at which discharges are completely suppressed should correspond to the difference in threshold between the excitatory, ipsilateral and inhibitory, contralateral inputs that innervate each LSO cell. The main purpose of this study was to test the threshold difference hypothesis proposed by Reed and Blum by recording responses to monaural stimulation and to IIDs from single cells in the LSO of the mustache bat. Our results show that although the IID sensitivities of some LSO cells correspond to the difference in threshold between the excitatory and inhibitory ears, in the majority of cells the difference in thresholds did not correspond to the cell's IID sensitivity. The results lead us to propose two models to account for IID sensitivities. One model is similar to that proposed by Reed and Blum and emphasizes differences in the thresholds of the excitatory and inhibitory inputs. This model accounts for the minority of cells in which the IID of complete inhibition corresponded to the difference in threshold of the inputs from the two ears. The other model, which accounts for the cells in which the IID of complete inhibition did not correspond to the difference in the thresholds of the inputs from the two ears (the majority of cells), places emphasis on differences in latencies of the excitatory and inhibitory inputs. The models incorporate features that are concordant with the known properties of the neurons that project to the LSO and together can account for the diversity of IID sensitivities among the population of LSO neurons.

Sensitivity to interaural intensity differences of neurons in primary auditory cortex of the cat. I. types of sensitivity and effects of variations in sound pressure level.

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

Decreased inhibition to lateral superior olive neurons in young and aged Sprague-Dawley rats

Lateral superior olive (LSO) neurons in young and aged Sprague-Dawley rats have functional properties consistent with a limited contralateral inhibition, which is markedly different from other animals. An unusually low proportion of LSO cells ( 36 113 ) exhibited contralateral inhibition (and ipsilateral excitation, IE), while over 25% of LSO units exhibited excitatory responses to contralateral stimuli. Inhibition of most IE LSO neurons was evident only when the contralateral intensity was greater than the ipsilateral intensity, resulting in a marked shift in sensitivity to interaural intensity differences (IID). The firing rate of IE neurons was also affected more by a change in intensity of ipsilateral compared to contralateral stimuli. The shift in the IID sensitivity and the relative decrease in effectiveness of contralaterally driven inhibition in Sprague-Dawley rat LSO neurons could be due to decreased inhibitory inputs from the MNTB principal cells, increased contralateral excitatory effects and/or increased ipsilateral excitatory effects. Age-related decreases in the numbers of MNTB neurons observed anatomically is not reflected in a change in LSO function. The Sprague-Dawley rat may be a useful model for the effect of reduced inhibition in the superior olivary complex on auditory behavior.

Responses of neurons in the inferior colliculus of the rat to interaural time and intensity differences in transient stimuli: Implications for the latency hypothesis

Although the sensitivity to interaural intensity differences (IIDs) of neurons receiving excitatory — inhibitory binaural input (EI neurons) has been examined in numerous studies, the mechanisms underlying this sensitivity remain unclear. According to the ‘latency hypothesis’, neuronal sensitivity to IIDs reflects sensitivity to differences in the timing of ipsilateral and contralateral inputs that are produced as a consequence of the effects of intensity upon latency. If the latency hypothesis is correct, a neuron's responses over any given IID range should be predicted by its responses to the interaural time differences (ITDs) that are ‘equivalent’ to the IIDs tested, in the sense that they produce the same changes in the relative timing of inputs. This prediction from the latency hypothesis was examined by determining the sensitivity of EI neurons in the inferior colliculus of anesthetized rats to IIDs and ITDs in click stimuli, under conditions that allowed ‘equivalent’ ITDs to be estimated. In approximately 10% of the 41 neurons tested, the IID-sensitivity function was a perfect or near-perfect match to the equivalent-ITD function, indicating that IID sensitivity could be entirely accounted for in terms of sensitivity to intensity-produced neural time differences, as asserted by the latency hypothesis. For the majority of neurons, however, sensitivity to equivalent ITDs accounted only partially for the characteristics of the IID-sensitivity function; other features of the function in these cases appeared to reflect the operation of an additional factor, most probably the relative magnitude of the inputs from the two ears. Although the conclusions are qualified by the fact that one of the assumptions on which the estimation of equivalent ITDs was based was probably not satisfied for some neurons, the results suggest that intensity-produced changes in both the magnitude and the timing of excitatory and inhibitory inputs shape the IID sensitivity of most EI neurons.

Maps of frequency and space in the Mammalian auditory system: Generation and plasticity

Abstract A basic organisational feature of the major sensory systems is the existence of topographically organised representations (or “maps”) of various stimulus features in the brain. Some of these maps reflect orderly connections between the receptor epithelium and the brain, whereas others are derived computationally. In the auditory system, frequency maps in cortical and subcortical structures reflect orderly connections, whereas maps of spatial location must be derived computationally. One of the major cues on which behavioural localisation of auditory stimuli depends is provided by interaural intensity differences (IIDs). In one region of the brain, a topographic organisation of IID sensitivity based on different types of binaural interaction has been demonstrated and has been shown to be the basis of a map of auditory space. Topographic maps based on orderly connections with the receptor epithelium have generally been thought not to be modifiable by experience in adult animals. However, the freque...

Binaural interaction in high-frequency neurons in inferior colliculus of the cat: effects of variations in sound pressure level on sensitivity to interaural intensity differences

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)

Binaural neurons in the mustache bat's inferior colliculus. I. Responses of 60-kHz EI units to dichotic sound stimulation.

1. Single-unit responses to closed-field, dichotic sound stimuli were obtained from EI neurons in the mustache bat's inferior colliculus; these neurons are excited by sound to the contralateral ear and inhibited by sound to the ipsilateral ear. All units were tuned to the 60-kHz component of the bat's sonar signal. The goal of the study was to describe basic features of the sensitivity to interaural intensity differences (IIDs) and sound intensity among an isofrequency population of EI neurons. The following paper describes how these features of IID sensitivity shape the response to free-field sounds. 2. Three features of IID sensitivity were considered. The inhibitory threshold (Figs. 1 and 2) described the IID at which inhibitory effects became pronounced; it was defined as the IID at which the excitatory response to contralateral sound was suppressed by 50%. Most units (68%) were inhibited at positive IID values, for which the ipsilateral (inhibitory) sound was more intense. The maximum inhibition (Figs. 1 and 3) described the strength of ipsilateral inhibition; it was defined as the percent that each unit was inhibited below its response to monaural stimulation of the contralateral ear. The majority of units (58%) were almost totally suppressed by a sufficiently intense ipsilateral sound. The IID range (Figs. 1 and 4) described the sharpness or slope of the IID cutoff; it was defined as the IID range over which the response changed from nearly unsuppressed (80% of maximum response) to near maximum suppression (20% of maximum response). Most units (71%) had IID ranges of less than or equal to 15 dB. 3. A significant correlation between the inhibitory threshold and the maximum inhibition (Fig. 5) among the sample of EI units suggests that some common neural mechanisms underlie these features of IID sensitivity. 4. The response of EI neurons to binaural stimuli was a function of sound intensity as well as IID (Fig. 7). In part, this resulted from intensity-dependent changes in properties of binaural inhibition. For most units, basic measures of IID sensitivity changed to a limited extent as the sound intensity changed.(ABSTRACT TRUNCATED AT 400 WORDS)

Binaural processing of sound pressure level in the inferior colliculus.

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)

Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus: implications for auditory spatial representation.

Sensitivity to interaural intensity difference (IID) was examined for 103 neurons in the deep layers of superior colliculus (SC) in ketamine barbiturate-anesthetized cats. Noise stimuli were presented dichotically, and IID sensitivity functions were generated while keeping the average binaural intensity (ABI) of stimulation constant. Neurons of three binaural classes were found to be IID sensitive. Neurons receiving excitatory contralateral input and inhibitory ipsilateral input (EO/I cells, 55% of sample) had steplike IID functions, with maximum response at IIDs corresponding to contralateral azimuths (positive IIDs), total suppression at IIDs corresponding to ipsilateral azimuths (negative IIDs), and cutoffs at different positions along the IID axis for different neurons. Neurons responsive only to binaural stimulation (OO/F cells, 15% of sample) had IID functions with a sharp peak in the range of 0 to 10 dB IID. Cells receiving excitatory input contralaterally and a facilitatory ipsilateral input (EO/F cells, 7% of sample) had IID functions of intermediate shape, with a peak in the range of 10 to 20 dB IID and a sharper cutoff near zero IID than at larger positive IIDs. The sharpness of IID cutoff for EO/I cells was quantified by measuring an 80% IID dynamic range. Neurons with 80% IID dynamic ranges of less than 26 dB were judged to have sharp cutoffs. The position along the IID axis of the IID cutoff for these cells was quantified by recording the IID at which the response was at 50% of maximum (half-maximal IID). A topographic organization of EO/I cells with sharp IID cutoffs was found along the rostrocaudal axis of SC, such that rostral EO/I cells had IID functions with half-maximal IIDs near zero, while increasingly caudal EO/I cells had progressively larger (positive) half-maximal IIDs. Although detailed maps could not be obtained in individual animals, the topography was observed in each of nine experiments in which EO/I cells were located in two or more rostrocaudal locations (P = 0.00002). The effect of stimulus level on the stability of IID cutoff was examined for 13 EO/I cells. The majority (85%) showed less than 10 dB variation in half-maximal IID across a range of suprathreshold ABIs, indicating that EO/I cells in SC generally exhibit stability in cutoff with changes in intensity of broadband stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

Interaural intensity difference sensitivity based on facilitatory binaural interaction in cat superior colliculus.

Sensitivity to interaural intensity difference (IID) has generally been identified as a property of neurons exhibiting inhibitory binaural interaction, viz. contralateral excitatory and ipsilateral inhibitory input (EI cells). In the deep layers of the superior colliculus, however, almost 30% of IID-sensitive cells are characterised by facilitatory or mixed facilitatory/inhibitory interactions. Such cells typically have peaked IID sensitivity functions in contrast to the step functions characteristic of EI cells. There appears to be a continuum in IID sensitivity from pure step functions to sharply-peaked functions. The observation that a given form of IID sensitivity can be associated with patterns of binaural interaction other than that by which it is most commonly produced suggests that IID-sensitive neurons are better classified on the basis of the form of their IID sensitivity than their binaural input pattern. It seems probable that IID sensitivity based on facilitatory and mixed facilitatory/inhibitory binaural interactions is a general characteristic of the primary auditory pathway, although only fragmentary data are so far available.

Topographic organization of interaural-intensity-difference sensitivity in deep superior colliculus

The sensitivity to interaural intensity differences (IIDs) of acoustically responsive neurons was examined in multiple microelectrode penetrations along the rostro-caudal axis of deep superior colliculus (SC) in anesthetized cats. The most rostrally located neurons were unresponsive to monaural stimulation but were strongly excited binaurally. IID sensitivity functions for these “predominantly binaural” (PB) neurons were sharply peaked with maximum response at or near zero IID. Caudal to the PB cell area, most neurons were excited by contralateral stimulation and inhibited by ipsilateral stimulation (EI cells). All EI cells were maximally excited over a range of IIDs favoring the contralateral ear and were totally inhibited over a range favoring the ipsilateral ear. The position of the cutoff between excitatory and inhibitory regions was located near zero IID (corresponding to the median plane) for the most rostrally located EI neurons and was shifted progressively to IIDs favoring the contralateral ear (corresponding to increasing contralateral azimuths) for more caudally located EI neurons. The consequence of this topography is that IID, and hence azimuthal location, is represented by the extent of deep SC activated.

Auditory response properties of neurons in deep layers of cat superior colliculus.

1. The auditory responses of 207 single neurons in the intermediate and deep layers of the superior colliculus (SC) of barbiturate -or chloralose-anesthetized cats were recorded extracellularly. Sealed stimulating systems incorporating calibrated probe microphone assemblies were employed to present tone- and noise-burst stimuli. 2. All acoustically activated neurons responded with onset responses to noise bursts. Of those neurons also tested with tonal stimuli, approximately 30% were unresponsive over the frequency range tested (0.1-40 kHz), while the others had higher thresholds to tones than to noise. 3. Details of frequency responsiveness were obtained for 55 neurons; 21 were broadly tuned, while 34 were sharply tuned with clearly defined characteristic frequencies (CFs). All sharply tuned neurons had CFs greater than or equal to 10 kHz. 4. The majority of neurons (81%) responded with latencies in the range 8-20 ms; only 11% of neurons had latencies greater than 30 ms. 5. Binaural response properties were examined for 165 neurons. The great majority (79%) received monaural excitatory input only from the contralateral ear (EO). However, most EO cells were binaurally influenced, the contralateral response being either inhibited (EO/I; 96 of 131 units) or facilitated (EO/F; 33 of 131 units) by simultaneous ipsilateral stimulation. Small subgroups were monaurally excited by either ear (EE cells; 8%) or were unresponsive monaurally but responded strongly to binaural stimulation (OO/F cells; 7%). 6. EO/I, EO/F, and OO/F neurons showed characteristic forms of sensitivity to interaural intensity differences (IIDs). The IID functions of EO/I neurons would be expected to produce large contralateral spatial receptive fields with clearly defined medial borders, such as have been described in studies of deep SC neurons employing free-field stimuli. 7. Preliminary evidence suggests a possible topographic organization of IID sensitivity in deep SC, such that the steeply sloping portion of the function (corresponding to the medial edge of the receptive field) is shifted laterally for EO/I neurons located more caudally in the nucleus. 8. The auditory properties of deep SC neurons are compared with previous reports and implications for the organization of auditory input are considered. The binaural properties and auditory spatial fields of deep SC neurons suggest that any representation of auditory space in this structure is unlikely to be based on restricted spatial fields.

Plasticity of binaural interaction in the cat inferior colliculus

Responses of single neurones in the inferior colliculus (IC) to acoustic interaural intensity difference (IID) were examined in normal, adult cats and in cats that had been reared for 3–4 months, either from birth or as adults, with unilateral ligation of the external meatus. There were significantly fewer units displaying IID sensitivity in either of the ligated groups than there were in the normal group. The loss of IID sensitivity in the ligated animals reflected a diminished inhibitory input from the non-ligated ear.