Interaural Intensity Disparities Research Articles

Circuits That Innervate Excitatory-Inhibitory Cells in the Inferior Colliculus Obtained with In Vivo Whole Cell Recordings

Neurons excited by stimulation of one ear and suppressed by the other, called excitatory/inhibitory (EI) neurons, are sensitive to interaural intensity disparities, the cues animals use to localize high frequencies. EI neurons are first formed in lateral superior olive, which then sends excitatory projections to the dorsal nucleus of the lateral lemniscus and the inferior colliculus (IC), both of which contain large populations of EI cells. We evaluate herein the inputs that innervate EI cells in the IC of Mexican free-tailed bats (Tadarida brasilensis mexicana) with in vivo whole-cell recordings from which we derived excitatory and inhibitory conductances. We show that the basic EI property in the majority of IC cells is inherited from lateral superior olive, but that each type of EI cell is also innervated by the ipsilateral or contralateral dorsal nucleus of the lateral lemniscus, as well as additional excitatory and inhibitory inputs from monaural nuclei. We identify three EI types, each of which receives a set of projections that is different from the other types. To evaluate the role that the various projections played in generating binaural responses, we used modeling to compute a predicted response from the conductances. We then omitted one of the conductances from the computation to evaluate the degree to which that input contributed to the binaural response. We show that the formation of the EI property in the various types is complex, and that some projections exert such subtle influences that they could not have been detected with extracellular recordings or even from intracellular recordings of postsynaptic potentials.

Intracellular Recordings Reveal Novel Features of Neurons That Code Interaural Intensity Disparities in the Inferior Colliculus

Many cells in the inferior colliculus (IC) are excited by contralateral and inhibited by ipsilateral stimulation and are thought to be important for sound localization. These excitatory-inhibitory (EI) cells comprise a diverse group, even though they exhibit a common binaural response property. Previous extracellular studies showed the diversity results from different circuits that generate the same EI property among the IC population, where some inherit the property from a lower nucleus, some are formed de novo in the IC, and others inherit EI features that are modified by inhibitory circuits. Here we evaluated the differential circuitry by recording inputs (postsynaptic potentials) and outputs (spikes) with in vivo whole-cell recordings from the IC of awake Mexican free-tailed bats. We show that in a minority of EI cells, either they inherited their binaural property from a lower binaural nucleus or the EI property was created in the IC via inhibitory projections from the ipsilateral ear, features consistent with those observed in extracellular studies. However, in a majority of EI cells, ipsilateral signals evoked subthreshold EPSPs that behaved paradoxically in that EPSP amplitudes increased with intensity, even though binaural signals with the same ipsilateral intensities generated progressively greater spike suppressions. We propose circuitry that can account for the responses we observed and suggest that the ipsilaterally evoked EPSPs could influence the responsiveness of IC cells to dynamic signals with interaural intensity disparities that change over time, such as moving sound sources or multiple sounds that occur in complex acoustic environments.

Roles of inhibition for transforming binaural properties in the brainstem auditory system

This review is concerned with the operation of circuits in the central auditory system, how they transform response features and what functional significance may be attributed to those transformations. We focus on the role that GABAergic inhibition plays in processing interaural intensity disparities (IIDs), the principal cues for localizing high frequencies, and the transformations of IID coding that occur between the superior olivary complex and the inferior colliculus (IC). IIDs are coded by excitatory–inhibitory (EI) cells, so called because they are excited by one ear and inhibited by the other. EI neurons are first created in the lateral superior olive (LSO), but they also dominate the dorsal nucleus of the lateral lemniscus (DNLL) and regions of the IC. The three nuclei are intimately linked through a complex arrangement of excitatory and inhibitory connections. One of these is a crossed excitatory projection from the LSO to both the DNLL and IC. The binaural properties of EI neurons in LSO, DNLL and IC appear strikingly similar, suggesting that the EI properties created in the LSO are simply imposed on the DNLL and IC through the crossed excitatory projections. Recent studies support the idea that EI properties created in lower centers are imposed on some IC cells. However, other studies show that the circuitry linking LSO, DNLL and IC generates a number of response transformations in many IC cells. These transformations include marked changes in EI properties with stimulus duration, the generation of highly focused spatial receptive fields, shifts in sensitivity to IIDs, and the de novo creation of the EI response property. All of these transformations are produced by inhibitory innervation of the IC. An additional emergent property is also imposed on IC cells that receive GABAergic innervation from the DNLL. That property is a change in the binaural features of the IC cell, a change produced by the reception of an earlier sound whose IID is strongly excitatory to the IC cell. We illustrate each of these transformations, propose circuitry that could account for the observed properties and suggest some functional relevance for each. In the final section, we discuss some of the inherent uncertainties associated with attributing functional consequences to response features and then consider whether the transformations found in some mammals are species-specific or are universal features of all mammals.

Reversible Inactivation of the Dorsal Nucleus of the Lateral Lemniscus Reveals Its Role in the Processing of Multiple Sound Sources in the Inferior Colliculus of Bats

Neurons in the inferior colliculus (IC) that are excited by one ear and inhibited by the other [excitatory-inhibitory (EI) neurons] can code interaural intensity disparities (IIDs), the cues animals use to localize high frequencies. Although EI properties are first formed in a lower nucleus and imposed on some IC cells via an excitatory projection, many other EI neurons are formed de novo in the IC. By reversibly inactivating the dorsal nucleus of the lateral lemniscus (DNLL) in Mexican free-tailed bats with kynurenic acid, we show that the EI properties of many IC cells are formed de novo via an inhibitory projection from the DNLL on the opposite side. We also show that signals excitatory to the IC evoke an inhibition in the opposite DNLL that persists for tens of milliseconds after the signal has ended. During that period, strongly suppressed EI cells in the IC are deprived of inhibition from the DNLL and respond to binaural signals as weakly inhibited or monaural cells. By relieving inhibition at the IC, we show that an initial binaural signal essentially reconfigures the circuit and thereby allows IC cells to respond to trailing binaural signals that were inhibitory when presented alone. Thus, DNLL innervation creates a property in the IC that is not possessed by lower neurons or by collicular EI neurons that are not innervated by the DNLL. That property is a change in responsiveness to binaural signals, a change dependent on the reception of an earlier sound. These features suggest that the circuitry linking the DNLL with the opposite central nucleus of the IC is important for the processing of IIDs that change over time, such as the IIDs generated by moving stimuli or by multiple sound sources that emanate from different regions of space.

Auditory cortical responses to the interactive effects of interaural intensity disparities and frequency.

Under natural conditions, stimuli reaching the two ears contain multiple acoustic components. Rarely does a stimulus containing only one component (e.g. pure tone burst) exist outside the realm of the laboratory. For example, in sound localization the simultaneous presence of multiple cues (spectral content, level, phase, etc.) serves to increase the number of available cues and provide the listener with more information, thereby helping to reduce errors in locating the sound source. The present study was designed to explore the relationship between two acoustic parameters: stimulus frequency and interaural intensity disparities (IIDs). By varying both stimulus frequency and IIDs for each cell, we hoped to gain insight into how multiple cues are processed. To this end, we examined the responses of neurons in cat primary auditory cortex (AI) to determine if their sensitivity to IIDs changed as a function of stimulus frequency. IIDs ranging from +30 to -30 dB were presented at different frequencies (frequency was always the same in the two ears). We found that approximately half of the units examined exhibited responses to IIDs that varied as a function of stimulus frequency (i.e. displayed some form of IID x Freq dependency). The remaining units displayed IID responses that were not clearly related to stimulus frequency.

Evidence for separate processing in the human brainstem of interaural intensity and temporal disparities for sound lateralization

Sound lateralization can be induced by interaural intensity disparities (IIDs) or by interaural temporal disparities (ITDs). The purpose of this study was to indicate whether IIDs and ITDs are processed by the same central units that detect interaural disparity in timing of afferent activity. If sound lateralization to intensity and time cues was determined by the same afferent latency disparity detectors in the brainstem, lateralization would be the same, regardless of whether latency disparity was induced by IIDs or ITDs. Moreover, the disparity detectors, and thus their dipole equivalents, would be the same for equal lateralizations, whether induced by IIDs or ITDs. Auditory brainstem evoked potentials (ABEPs) were recorded in response to monaural and binaural clicks, with a variety of IIDs and ITDs. Peak II (proximal auditory nerve activity), peak III (input to the superior olivary complex), and binaural interaction components (BICs) Be I and Be II (binaurally activated upper pons) were identified and their latencies measured. The psychophysical lateralization of the clicks (in cm from vertex) was also measured in response to the same binaural stimuli. The correlations between interaural afferent latency disparities (difference in corresponding peak latencies originating in each ear) and psychophysical click lateralization were calculated. Similarly, the correlations with click lateralization of the BICs equivalent dipole latency as well as orientation change (relative to symmetrical clicks) were determined. A strong correlation with lateralization was found for peaks II and III latency disparities, with steeper slopes for IIDs than for ITDs. Moreover, binaural activity across the same lateralizations differed between IIDs and ITDs. These results, therefore, indicate that interaural time and intensity cues are processed by separate systems in the brainstem, both at the afferent convergence level and after interaural disparities are determined.

Investigating acoustic localization using artificial ears

Physical modeling is a technique wherein sensorimotor mechanisms believed to underlie animal behavior are mimicked using functionally analogous transducers and electromechanical circuitry. Because physical models inhabit the same environment as animals, they allow biologists to examine more realistic environmental interactions. In turn, physical modeling can enable engineers to discover the general principles underlying robust, adaptive sensorimotor control of robots. Two acoustic localization mechanisms are being physically modeled: cricket phonotaxis and echolocation by constant frequency emitting bats. (1) The function of the cricket trachea was modeled by connecting the output of two miniature microphones to a circuit measuring the relative intensity and binaural phase shift of a received call. Using only tracheal phase cancellation and latency comparison, a robot bearing this sensor obtains directional information enabling it to approach only those sounds with the right (frequency and envelope) structure. (2) An artificial echolocation system was built using a continuous, pure-tone-emitting transducer and a pair of receivers mounted on the pan/tilt head of a robot. Directional cues contained in echoes reflected from moving targets—interaural intensity disparities and temporal differences in the echo modulating waveforms—are used to orient the robot toward these targets.

Azimuthal receptive fields are shaped by GABAergic inhibition in the inferior colliculus of the mustache bat.

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

The roles of GABAergic and glycinergic inhibition on binaural processing in the dorsal nucleus of the lateral lemniscus of the mustache bat.

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)

Binaural processing in the dorsal nucleus of the lateral lemniscus

We studied the binaural properties of 72 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat. There are six main findings: 1) Conventional EI neurons that were excited by stimulation of the contralateral ear and inhibited by ipsilateral stimulation, comprise the majority (80%) of binaural DNLL cells. 2) For most EI neurons the quantitative features of their interaural intensity disparity (IID) functions, maximum inhibition, dynamic range and 50% point IIDs, were largely unaffected by the absolute intensity at the contralateral ear. 3) Although the net effect of the inhibition evoked by ipsilateral stimulation was to suppress discharges evoked by contralateral stimulation, our results indicate that the inhibitory inputs can act in three different ways. The first was a time-intensity trade, where increasing the intensity at the ipsilateral ear evoked inhibitory effects with progressively shorter latencies. The second way was that the latency of inhibition did not appear to decrease with ipsilateral intensity, but rather increasing ipsilateral intensity appeared only to increase the strength of the inhibition. The third way was that the lowest effective ipsilateral intensity suppressed the first spikes evoked by the contralateral stimulus and higher ipsilateral intensities then suppressed the later discharges of the train. Each of these inhibitory patterns was seen in about a third of the cells. 4) Neurons that had more complex binaural properties, such as the facilitated EI neurons (EI/F) and neurons that were driven by sound to either ear (EE neurons), represented about 20% of the binaural population. There were two types of EE neurons; those in which there was a simple summation of discharges evoked with certain IIDs, and those in which the spike-counts to binaural stimulation at certain IIDs were greater than a summation of the monaural counts and thus were facilitated. 5) All binaural neurons were strongly inhibited with IIDs that favored the ipsilateral ear. Our findings indicate that the more complex binaural types, the facilitated EI neurons (EI/F) as well as the two types of EE neurons, may be constructed from conventional EI neurons by adding inputs from several sources that impart the more complex features to these neurons. We propose four circuits that could account for the different binaural response properties that we observed. The circuits are based on the known connections of the DNLL and the neurochemistry of those connections. Finally, we compared the binaural properties of neurons in the mustache bat DNLL with those of neurons in the mustache bat inferior colliculus and lateral superior olive. The comparative features suggest that the processing of the interaural intensity disparities undergoes at least four types of response transformations along the ascending auditory system.

GABA shapes sensitivity to interaural intensity disparities in the mustache bat's inferior colliculus: implications for encoding sound location

This study examined how GABAergic inhibition affected binaural properties of neurons in the mustache bat's inferior colliculus. Evaluations were made by documenting changes in acoustically evoked inhibition that occurred when GABAergic inputs were reversibly blocked by iontophoretic application of the GABAA antagonist bicuculline. We studied neurons sensitive to interaural intensity disparities (IIDs), since these are the principal cues animals use to localize high-frequency sounds. Neurons sensitive to these cues receive excitation from one ear and inhibition from the other ear, and are called EI neurons. Recordings focused on the EI region in the hypertrophied 60 kHz isofrequency contour, where the sensitivities of the EI cells to IIDs are systematically ordered, thereby creating a map of IID sensitivity. EI neurons were classified on the basis of their IID functions, of which there were two principal types. Seventy percent of the cells had conventional IID functions where the firing rate evoked by a fixed intensity at the contralateral (excitatory) ear remained constant with low intensities at the ipsilateral (inhibitory) ear and then declined progressively as the intensity at the ipsilateral ear increased. We refer to cells that had this type of IID function simply as EI neurons. The IID functions in the remaining 30% of the cells showed binaural facilitation and were classified as EI/f neurons. In these cells, increasing sound intensity at the ipsilateral (inhibitory) ear when the intensity at the contralateral (excitatory) ear was fixed, initially caused the firing rate to increase by at least 25% above the rate evoked by the sound at the contralateral ear alone. Additional intensity increases at the ipsilateral ear then resulted in a marked decline in response rate. We examined the effects of bicuculline on three binaural properties: (1) the degree of inhibition evoked by the ipsilateral ear (the maximum inhibition), (2) the IID at which the unit's discharge rate declined by 50% (the 50% point), and (3) binaural facilitation. There are three main findings. First, bicuculline substantially reduced or eliminated the inhibition evoked by the ipsilateral ear in about 40% of the cells. In the other 60% of the cells, bicuculline had little or no effect on the magnitude of the ipsilaterally evoked inhibition. The second finding is that in more than half of the cells in which there was little or no reduction in the magnitude of the ipsilaterally evoked inhibition, bicuculline changed the IID at which the ipsilaterally evoked inhibition caused the discharge rate to decline by 50%.(ABSTRACT TRUNCATED AT 400 WORDS)

Time is traded for intensity in the bat's auditory system

Disparities in time and intensity are the two chief cues animals use for localizing a sound source in space. Echolocating bats belonging to the family Molossidae emit brief, ultrasonic signals for orientation that sweep downward about an octave over the duration of the pulse. Due to acoustic shadowing and the directional properties of the ears, pronounced interaural intensity disparities are created that vary as a function of azimuth. However, due to the small headwidth of these animals, azimuthal changes create small interaural time disparities that are at most 30 μs. The experiments in this report are concerned with the binaural processing of time and intensity disparities using brief FM signals that simulate the animal's natural echolocation calls. Binaural neurons receiving excitation from one ear and inhibition from the other (E-I neurons) were recorded from the inferior colliculus of Mexican free-tailed bats. The majority of units sampled were highly sensitive for temporal disparities of 100–300 μs, and a few had significant changes in discharge probability when interaural time was changed by 10–20 μs. However, all E-I neurons were also sensitive to intensity disparities. With only one exception, all E-I neurons traded time for intensity. On the average, each decibel difference in intensity could be compensated for by advancing or delaying the inhibitory sound by 47 μs. The main conclusion is that the auditory system processes interaural disparities by transforming level differences at the two ears into latency differences. Thus the discharge probability of each binaural neuron is determined largely by the arrival times of the discharges from the excitatory and inhibitory ears. In view of the substantial time-intensity trading ratios, the small interaural time disparities produced by azimuthal locations off the midline play no role in shaping the response properties of these neurons. Specific examples of how time-intensity trades can translate into a high spatial selectivity are presented.

Binaural response organization within a frequency-band representation of the inferior colliculus: implications for sound localization

The auditory system of the mustache bat (Pteronotus parnellii) contains a disproportionately large representation of a narrow frequency band, corresponding to the dominant, 60 kHz component of its echolocation signal. In the inferior colliculus (IC), the 60 kHz representation comprises an architectonically distinct region called the dorsoposterior division (DPD), which is accessible for detailed physiological study. We examined the topographic distribution of binaural responses within this one frequency-band representation of the inferior colliculus. We describe two primary results. First, neurons with different binaural response properties are spatially segregated into one of four binaural response-specific regions of the DPD: a large region of monaural (EO) responses; two regions containing neurons excited by sound from both ears (EE); and a region containing neurons excited by one ear and inhibited by the other (EI). Regions dominated by 60 kHz EI responses are also found in the lateral extremity of the IC, probably within the external nucleus. These results demonstrate functionally defined subdivisions in a single frequency-band representation of the IC. Moreover, they suggest that brain stem auditory projections to the DPD and/or intrinsic connections within the DPD are highly organized. Second, within the EI region of the DPD, there is a systematic shift in the sensitivity of EI multiunit responses to interaural intensity disparities (IIDs). Dorsally, EI neurons are suppressed only by relatively loud ipsilateral sounds, and there is a systematic decrease in the relative ipsilateral intensity required for suppression at more ventral recording sites. This result demonstrates that neurons sensitive to a sound localization cue are systematically organized within a frequency-band representation of the inferior colliculus. It has implications for the manner in which the location of a sound source is encoded within the primary auditory pathway.

Azimuthal representation within a population of interaural intensity‐sensitive neurons

One‐third of the central nucleus of the inferior colliculus (ICC) in the mustache bat is devoted to processing information at 60 kHz, a dominant component of the echolocation pulse. Within this 60‐kHz region, E‐I type neurons sensitive to interaural intensity disparities (IIDs) are grouped together. Their IID sensitivity changes in orderly fashion along the vertical axis of the ICC. Dorsal‐most neurons require the highest relative inhibitory intensity to suppress activity, the most ventral require the lowest. Regardless of their IID sensitivity, all neurons had lowest excitatory thresholds for the same azimuthal sound location. IID sensitivity did, however, influence their overall responsiveness to azimuthal locations across the frontal sound field. E‐I neurons with the highest inhibitory thresholds responded to sounds throughout the frontal field. As inhibitory thresholds dropped, their medial receptive field borders shifted systematically across the azimuth toward the area of lowest excitatory thresholds. The percentage of excited neurons within this population will therefore shift systematically along the vertical axis of the ICC as a function of azimuthal location. [Work supported by NIH, NSF.]

A functional organization of binaural responses in the inferior colliculus

Binaural responses are segregated within an enlarged isofrequency region of the mustache bat's inferior colliculus. In the part of this region containing E-I responses, there is an orderly shift in the sensitivity of unit clusters to interaural intensity disparities, having implications for the representation of auditory space within isofrequency regions of the inferior colliculus.

A representation of horizontal sound location in the inferior colliculus of the mustache bat (Pteronotus p. parnellii).

Binaurally sensitive E-I neurons in the inferior colliculus are topographically organized with respect to their sensitivity to interaural intensity disparities (IIDs). IID sensitivity dictates the azimuthal position of the medial border of a neuron's spatial receptive field. A sound moving along the azimuth will result in a change in the percentage of excited neurons as receptive field borders are crossed. Percent excitation within this population may provide a neural code for horizontal sound location.

Binaural interactions of single neurons in posterior field of cat auditory cortex.

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.

Coding of tonal stimuli by neurons in anterior auditory field of cat cerebral cortex

In the cortex of barbiturate‐anesthetized cats, the anterior auditory field (AAF) was defined by microelectrode maps of its frequency organization, and the responses of single neurons in that field to monaural and binaural tone‐burst stimuli were examined quantitatively. AAF neurons generally had narrow, V‐shaped threshold frequency tuning curves centered on a clearly defined best frequency (BF). Intensity functions at BF were commonly monotonic in shape with dynamic ranges of 15 to 40 dB. Cells with nonmonotonic intensity functions had optimal sound pressure levels in the range 15 to 70 dB. Minimum response latencies at BF were in the range 10 to 15 ms. Binaural interactions were diverse, and a number of neurons demonstrated sensitivity to interaural intensity disparities. These properties are similar to those of cells in the primary auditory cortex, A1 [D. P. Phillips and D. R. F. Irvine, J. Neurophysiol. 45, 48–58 (1981)], and the data are consistent with the view that AAF and A1 function in some sense as parallel processors. It remains, however, to determine whether their thalamic afferents are independent, collateral, or overlapping, and to establish their specific functional roles in acoustic behavior.

Time-intensity trades revisited.

Two experiments were accomplished which involved time-intensity trades on a lateralization task. In the first experiment, subjects adjusted interaural time differences between binaural stimuli to compensate for interaural intensity disparities. In the second, the same listeners adjusted the interaural intensity relationship to offset interaural time differences. Three pure tones (250, 500, and 1000 Hz) were employed as binaural stimuli. The two experiments yielded substantially different time-intensity trading ratios for large values of interaural time differences and intensity disparities. This finding supplies evidence of a new type that the time-intensity trading ratio does not accurately reflect the central auditory processes that are involved with interaural time and intensity on a lateralization task.

Binaural intensity JNDs for transients

Difference thresholds for interaural intensity (ΔI) were measured as a function of overall interaural intensity disparity (I) using a same‐different lateralization paradigm. The signals tested were high (3–4 kHz) or low (0.1–2 kHz) frequency bandpass clicks. Values of I ranged from 0 to 32 dB, while the average overall level for each binaural click was maintained at 48 dB SPL by symmetrically dividing the values of I and ΔI between the two ears. Controls were included to account for information contained in monaural loudness increments, and differences between binaural and monaural thresholds were taken as measures of subjects' intensity‐based lateralization abilities. Hafter and DeMaio [J. Acoust. Soc. Am. 57, 181–186 (1975)], also using clicks, reported that sensitivity to interaural time (Δt) falls off gradually as the overall difference (t) increases. Within the framework of a model which equates intensity differences to time differences, use of these earlier data may permit extraction of “true” intensity‐based lateralization, independent of both monaural and temporal cues. Our results verify that, at least for the high‐frequency range, such interaural intensity differences are indeed useable cues for lateralization. Acuity for the interaural intensity cue declines slowly for images lateralized away from the midline; use of the cue deteriorates completely as I reaches values near 24 dB. [Supported in part by grants from the NIH and HIMH.]