Binaural Cues For Sound Localization Research Articles

The Neural Representation of Binaural Sound Localization Cues Across Different Subregions of the Chicken's Inferior Colliculus.

The sound localization behavior of the nocturnally hunting barn owl and its underlying neural computations is a textbook example of neuroethology. Differences in sound timing and level at the two ears are integrated in a series of well-characterized steps, from brainstem to inferior colliculus (IC), resulting in a topographical neural representation of auditory space. It remains an important question of brain evolution: How is this specialized case derived from a more plesiomorphic pattern? The present study is the first to match physiology and anatomical subregions in the non-owl avian IC. Single-unit responses in the chicken IC were tested for selectivity to different frequencies and to the binaural difference cues. Their anatomical origin was reconstructed with the help of electrolytic lesions and immunohistochemical identification of different subregions of the IC, based on previous characterizations in owl and chicken. In contrast to barn owl, there was no distinct differentiation of responses in the different subregions. We found neural topographies for both binaural cues but no evidence for a coherent representation of auditory space. The results are consistent with previous work in pigeon IC and chicken higher-order midbrain and suggest a plesiomorphic condition of multisensory integration in the midbrain that is dominated by lateral panoramic vision.

Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs.

Sound localization relies on minute differences in the timing and intensity of sound arriving at both ears. Neurons of the lateral superior olive (LSO) in the brainstem process these interaural disparities by precisely detecting excitatory and inhibitory synaptic inputs. Aging generally induces selective loss of inhibitory synaptic transmission along the entire auditory pathways, including the reduction of inhibitory afferents to LSO. Electrophysiological recordings in animals, however, reported only minor functional changes in aged LSO. The perplexing discrepancy between anatomical and physiological observations suggests a role for activity-dependent plasticity that would help neurons retain their binaural tuning function despite loss of inhibitory inputs. To explore this hypothesis, we use a computational model of LSO to investigate mechanisms underlying the observed functional robustness against age-related loss of inhibitory inputs. The LSO model is an integrate-and-fire type enhanced with a small amount of low-voltage activated potassium conductance and driven with (in)homogeneous Poissonian inputs. Without synaptic input loss, model spike rates varied smoothly with interaural time and level differences, replicating empirical tuning properties of LSO. By reducing the number of inhibitory afferents to mimic age-related loss of inhibition, overall spike rates increased, which negatively impacted binaural tuning performance, measured as modulation depth and neuronal discriminability. To simulate a recovery process compensating for the loss of inhibitory fibers, the strength of remaining inhibitory inputs was increased. By this modification, effects of inhibition loss on binaural tuning were considerably weakened, leading to an improvement of functional performance. These neuron-level observations were further confirmed by population modeling, in which binaural tuning properties of multiple LSO neurons were varied according to empirical measurements. These results demonstrate the plausibility that homeostatic plasticity could effectively counteract known age-dependent loss of inhibitory fibers in LSO and suggest that behavioral degradation of sound localization might originate from changes occurring more centrally.

Enhanced Excitatory Connectivity and Disturbed Sound Processing in the Auditory Brainstem of Fragile X Mice.

Hypersensitivity to sounds is one of the prevalent symptoms in individuals with Fragile X syndrome (FXS). It manifests behaviorally early during development and is often used as a landmark for treatment efficacy. However, the physiological mechanisms and circuit-level alterations underlying this aberrant behavior remain poorly understood. Using the mouse model of FXS (Fmr1 KO), we demonstrate that functional maturation of auditory brainstem synapses is impaired in FXS. Fmr1 KO mice showed a greatly enhanced excitatory synaptic input strength in neurons of the lateral superior olive (LSO), a prominent auditory brainstem nucleus, which integrates ipsilateral excitation and contralateral inhibition to compute interaural level differences. Conversely, the glycinergic, inhibitory input properties remained unaffected. The enhanced excitation was the result of an increased number of cochlear nucleus fibers converging onto one LSO neuron, without changing individual synapse properties. Concomitantly, immunolabeling of excitatory ending markers revealed an increase in the immunolabeled area, supporting abnormally elevated excitatory input numbers. Intrinsic firing properties were only slightly enhanced. In line with the disturbed development of LSO circuitry, auditory processing was also affected in adult Fmr1 KO mice as shown with single-unit recordings of LSO neurons. These processing deficits manifested as an increase in firing rate, a broadening of the frequency response area, and a shift in the interaural level difference function of LSO neurons. Our results suggest that this aberrant synaptic development of auditory brainstem circuits might be a major underlying cause of the auditory processing deficits in FXS.SIGNIFICANCE STATEMENT Fragile X Syndrome (FXS) is the most common inheritable form of intellectual impairment, including autism. A core symptom of FXS is extreme sensitivity to loud sounds. This is one reason why individuals with FXS tend to avoid social interactions, contributing to their isolation. Here, a mouse model of FXS was used to investigate the auditory brainstem where basic sound information is first processed. Loss of the Fragile X mental retardation protein leads to excessive excitatory compared with inhibitory inputs in neurons extracting information about sound levels. Functionally, this elevated excitation results in increased firing rates, and abnormal coding of frequency and binaural sound localization cues. Imbalanced early-stage sound level processing could partially explain the auditory processing deficits in FXS.

Structural Changes and Lack of HCN1 Channels in the Binaural Auditory Brainstem of the Naked Mole-Rat (Heterocephalus glaber).

Naked mole-rats (Heterocephalus glaber) live in large eu-social, underground colonies in narrow burrows and are exposed to a large repertoire of communication signals but negligible binaural sound localization cues, such as interaural time and intensity differences. We therefore asked whether monaural and binaural auditory brainstem nuclei in the naked mole-rat are differentially adjusted to this acoustic environment. Using antibody stainings against excitatory and inhibitory presynaptic structures, namely the vesicular glutamate transporter VGluT1 and the glycine transporter GlyT2 we identified all major auditory brainstem nuclei except the superior paraolivary nucleus in these animals. Naked mole-rats possess a well structured medial superior olive, with a similar synaptic arrangement to interaural-time-difference encoding animals. The neighboring lateral superior olive, which analyzes interaural intensity differences, is large and elongated, whereas the medial nucleus of the trapezoid body, which provides the contralateral inhibitory input to these binaural nuclei, is reduced in size. In contrast, the cochlear nucleus, the nuclei of the lateral lemniscus and the inferior colliculus are not considerably different when compared to other rodent species. Most interestingly, binaural auditory brainstem nuclei lack the membrane-bound hyperpolarization-activated channel HCN1, a voltage-gated ion channel that greatly contributes to the fast integration times in binaural nuclei of the superior olivary complex in other species. This suggests substantially lengthened membrane time constants and thus prolonged temporal integration of inputs in binaural auditory brainstem neurons and might be linked to the severely degenerated sound localization abilities in these animals.

Tuning to Binaural Cues in Human Auditory Cortex

Interaural level and time differences (ILD and ITD), the primary binaural cues for sound localization in azimuth, are known to modulate the tuned responses of neurons in mammalian auditory cortex (AC). The majority of these neurons respond best to cue values that favor the contralateral ear, such that contralateral bias is evident in the overall population response and thereby expected in population-level functional imaging data. Human neuroimaging studies, however, have not consistently found contralaterally biased binaural response patterns. Here, we used functional magnetic resonance imaging (fMRI) to parametrically measure ILD and ITD tuning in human AC. For ILD, contralateral tuning was observed, using both univariate and multivoxel analyses, in posterior superior temporal gyrus (pSTG) in both hemispheres. Response-ILD functions were U-shaped, revealing responsiveness to both contralateral and—to a lesser degree—ipsilateral ILD values, consistent with rate coding by unequal populations of contralaterally and ipsilaterally tuned neurons. In contrast, for ITD, univariate analyses showed modest contralateral tuning only in left pSTG, characterized by a monotonic response-ITD function. A multivoxel classifier, however, revealed ITD coding in both hemispheres. Although sensitivity to ILD and ITD was distributed in similar AC regions, the differently shaped response functions and different response patterns across hemispheres suggest that basic ILD and ITD processes are not fully integrated in human AC. The results support opponent-channel theories of ILD but not necessarily ITD coding, the latter of which may involve multiple types of representation that differ across hemispheres.

Updating and orientation in auditory space

For stable sound localization in space, a listener has to account for self-motion. This requires a head-to-world coordinate transformation by combining proprioceptive and vestibular inputs with the binaural cues for sound localization. Proprioceptive and vestibular information influence the evaluation of spatial auditory cues as indicated by the numerous proprioceptive and vestibular neural inputs into the auditory brainstem. First, we evaluate the relative influence of vestibular and proprioceptive cues on updating the world-centered position of auditory targets during active and passive head and/or body rotations in azimuth. Our results show that both vestibular and proprioceptive signals are used to update the spatial representations of auditory targets, but that vestibular inputs contribute more than proprioceptive inputs. Second, we explore the interplay of spatial audition and self-motion in subjects for which auditory space evaluation is of utmost importance, namely, for blind humans relying on ech...

Directional hearing: from biophysical binaural cues to directional hearing outdoors.

When insects communicate by sound, or use acoustic cues to escape predators or detect prey or hosts they have to localize the sound in most cases, to perform adaptive behavioral responses. In the case of particle velocity receivers such as the antennae of mosquitoes, directionality is no problem because such receivers are inherently directional. Insects equipped with bilateral pairs of tympanate ears could principally make use of binaural cues for sound localization, like all other animals with two ears. However, their small size is a major problem to create sufficiently large binaural cues, with respect to both interaural time differences (ITDs, because interaural distances are so small), but also with respect to interaural intensity differences (IIDs), since the ratio of body size to the wavelength of sound is rather unfavorable for diffractive effects. In my review, I will only shortly cover these biophysical aspects of directional hearing. Instead, I will focus on aspects of directional hearing which received relatively little attention previously, the evolution of a pressure difference receiver, 3D-hearing, directional hearing outdoors, and directional hearing for auditory scene analysis.

Single-sided deafness and directional hearing: contribution of spectral cues and high-frequency hearing loss in the hearing ear.

Direction-specific interactions of sound waves with the head, torso, and pinna provide unique spectral-shape cues that are used for the localization of sounds in the vertical plane, whereas horizontal sound localization is based primarily on the processing of binaural acoustic differences in arrival time (interaural time differences, or ITDs) and sound level (interaural level differences, or ILDs). Because the binaural sound-localization cues are absent in listeners with total single-sided deafness (SSD), their ability to localize sound is heavily impaired. However, some studies have reported that SSD listeners are able, to some extent, to localize sound sources in azimuth, although the underlying mechanisms used for localization are unclear. To investigate whether SSD listeners rely on monaural pinna-induced spectral-shape cues of their hearing ear for directional hearing, we investigated localization performance for low-pass filtered (LP, <1.5 kHz), high-pass filtered (HP, >3kHz), and broadband (BB, 0.5–20 kHz) noises in the two-dimensional frontal hemifield. We tested whether localization performance of SSD listeners further deteriorated when the pinna cavities of their hearing ear were filled with a mold that disrupted their spectral-shape cues. To remove the potential use of perceived sound level as an invalid azimuth cue, we randomly varied stimulus presentation levels over a broad range (45–65 dB SPL). Several listeners with SSD could localize HP and BB sound sources in the horizontal plane, but inter-subject variability was considerable. Localization performance of these listeners strongly reduced after diminishing of their spectral pinna-cues. We further show that inter-subject variability of SSD can be explained to a large extent by the severity of high-frequency hearing loss in their hearing ear.

Directional properties of bat ears for target localization

Among several bat acoustic capabilities, it is reported that the error they show in discriminating the direction of a target in the elevation plane is within a few degrees. Many researchers have investigated bat echolocation and attempted to explain which features their accuracy relies on. Some works have pointed out the importance of beam patterns associated to the ears of the bats: indeed, ear shapes are very complex and different across species. This allows bats to significantly discriminate among the directions the echoes of their calls come from. Also, binaural cues for sound localization have been found to be determinant for some bat species. A method to estimate target orientation based on the beam patterns of the receivers and their binaural geometric relationship is developed for a sonar system emulating bats echolocation: a broadband signal is produced in the ultrasonic range and the echoes are collected by two receivers. The location of the target with respect to the bat is given by spherical coordinates including the distance from the bat and the orientation (defined by azimuth and elevation angles). While distance of the target from the sonar system is recovered through the time from the emission to the reception of the signal, the orientation is estimated from knowledge of the beam profiles of the receivers. The ratios between received and original signals’ spectra are calculated for the left and the right receiver across frequencies after compensating for distance effects. Orientations ensuring attenuation values in the beam patterns closest to the ratios are selected. Among these, one orientation for the left receiver and one for the right, fulfilling appropriate mutual geometric relations given by the geometry of the situation, are selected, these two defining the direction of the signal echo. The beam patterns associated to the left and the right ear of the Phyllostomus discolor bat are used within a limited range of orientations. A model of the emission of the signal and its reception is simulated for a set of target orientations spanning the beam pattern domain. Additionally, several noise levels are considered. Estimates of directions of the echoes are performed and the error for each of them with respect to the true orientation is calculated. Most error values are comparable to those reported in the literature and associated to some bat species. The beam patterns have very irregular shapes over the set of orientations that change with the frequency range: indeed, the accuracy of the method in estimating the true orientation depends on the choice of the frequency range and on the area of orientations over which the beam pattern is defined. This approach makes it possible to investigate which acoustic features ensure good orientation estimates in order to explain why bats have such complex beam patterns filtering the echoes. As this method relies only on knowledge of the receivers’ beam patterns and geometric relations based on the binaural configuration, it appears feasible that bats utilise this effect.

Sound Rhythms Are Encoded by Postinhibitory Rebound Spiking in the Superior Paraolivary Nucleus

The superior paraolivary nucleus (SPON) is a prominent structure in the auditory brainstem. In contrast to the principal superior olivary nuclei with identified roles in processing binaural sound localization cues, the role of the SPON in hearing is not well understood. A combined in vitro and in vivo approach was used to investigate the cellular properties of SPON neurons in the mouse. Patch-clamp recordings in brain slices revealed that brief and well timed postinhibitory rebound spiking, generated by the interaction of two subthreshold-activated ion currents, is a hallmark of SPON neurons. The I(h) current determines the timing of the rebound, whereas the T-type Ca(2+) current boosts the rebound to spike threshold. This precisely timed rebound spiking provides a physiological explanation for the sensitivity of SPON neurons to sinusoidally amplitude-modulated (SAM) tones in vivo, where peaks in the sound envelope drive inhibitory inputs and SPON neurons fire action potentials during the waveform troughs. Consistent with this notion, SPON neurons display intrinsic tuning to frequency-modulated sinusoidal currents (1-15Hz) in vitro and discharge with strong synchrony to SAMs with modulation frequencies between 1 and 20 Hz in vivo. The results of this study suggest that the SPON is particularly well suited to encode rhythmic sound patterns. Such temporal periodicity information is likely important for detection of communication cues, such as the acoustic envelopes of animal vocalizations and speech signals.

Effects of Reverberation on the Directional Sensitivity of Auditory Neurons across the Tonotopic Axis: Influences of Interaural Time and Level Differences

In reverberant environments, acoustic reflections interfere with the direct sound arriving at a listener's ears, distorting the binaural cues for sound localization. We investigated the effects of reverberation on the directional sensitivity of single neurons in the inferior colliculus (IC) of unanesthetized rabbits. We find that reverberation degrades the directional sensitivity of single neurons, although the amount of degradation depends on the characteristic frequency (CF) and the type of binaural cues available. When interaural time differences (ITDs) are the only available directional cue, low-CF cells sensitive to ITDs in the waveform fine time structure maintain better directional sensitivity in reverberation than high-CF cells sensitive to ITDs in the envelope induced by cochlear filtering. Conversely, when both ITD and interaural level difference (ILD) cues are available, directional sensitivity in reverberation is comparable throughout the tonotopic axis of the IC. This result suggests that, at high frequencies, ILDs provide better directional information than envelope ITDs, emphasizing the importance of the ILD-processing pathway for sound localization in reverberation.

Use of binaural cues for sound localization in two species of Phyllostomidae: The Greater spear-nosed bat (Phyllostomus hastatus) and the Short-tailed fruit bat (Carollia perspicillata).

Unlike humans, not all mammals use both of the binaural cues for sound localization. Whether an animal uses these cues can be determined by testing its ability to localize pure tones; specifically, low frequencies are localized using time-difference cues, and high frequencies are localized using intensity-difference cues. We determined the ability to use binaural cues in 2 New World bats, Phyllostomus hastatus, large omnivores, and Carollia perspicillata, small frugivores, by testing their tone-localization ability using a conditioned avoidance procedure. Both species easily localized high-frequency tones, indicating that they could use the interaural intensity-difference cue. However, neither species was able to use the phase-difference cue to localize either low-frequency pure tones or amplitude-modulated tones (which provided an envelope for additional time analysis). We now know of 3 bat species that cannot use binaural time cues and 2 that can. Further exploration of localization in bats may provide insight into the neural analysis of time cues in species that do not hear low frequencies.

Auditory and Visual Space Maps in the Cholinergic Nucleus Isthmi Pars Parvocellularis of the Barn Owl

The nucleus isthmi pars parvocellularis (Ipc) is a midbrain cholinergic nucleus that shares reciprocal, topographic connections with the optic tectum (OT). Ipc neurons project to spatially restricted columns in the OT, contacting essentially all OT layers in a given column. Previous research characterizes the Ipc as a visual processor. We found that, in the barn owl, the Ipc responds to auditory as well as to visual stimuli. Auditory responses were tuned broadly for frequency, but sharply for spatial cues. We measured the tuning of Ipc units to binaural sound localization cues, including interaural timing differences (ITDs) and interaural level differences (ILDs). Units in the Ipc were tuned to specific values of both ITD and ILD and were organized systematically according to their ITD and ILD tuning, forming a map of space. The auditory space map aligned with the visual space map in the Ipc. These results demonstrate that the Ipc encodes the spatial location of objects, independent of stimulus modality. These findings, combined with the precise pattern of projections from the Ipc to the OT, suggest that the role of the Ipc is to regulate the sensitivity of OT neurons in a space-specific manner.

The bat head-related transfer function reveals binaural cues for sound localization in azimuth and elevation

Directional properties of the sound transformation at the ear of four intact echolocating bats, Eptesicus fuscus, were investigated via measurements of the head-related transfer function (HRTF). Contributions of external ear structures to directional features of the transfer functions were examined by remeasuring the HRTF in the absence of the pinna and tragus. The investigation mainly focused on the interactions between the spatial and the spectral features in the bat HRTF. The pinna provides gain and shapes these features over a large frequency band (20-90 kHz), and the tragus contributes gain and directionality at the high frequencies (60 to 90 kHz). Analysis of the spatial and spectral characteristics of the bat HRTF reveals that both interaural level differences (ILD) and monaural spectral features are subject to changes in sound source azimuth and elevation. Consequently, localization cues for horizontal and vertical components of the sound source location interact. Availability of multiple cues about sound source azimuth and elevation should enhance information to support reliable sound localization. These findings stress the importance of the acoustic information received at the two ears for sound localization of sonar target position in both azimuth and elevation.

A systems and neurobiological model of nucleus angularis and nucleus laminaris in the barn owl

The representation of binaural sound localization cues was investigated in a model of the barn owl’s auditory nerve, nucleus angularis (NA), nucleus magnocellularis (NM), nucleus laminaris (NL), and superior olivary nucleus (SON) using spiking leaky integrate and fire neurons. A phenomenological model of the barn owl’s auditory-nerve spike response was created to reproduce responses to tonal stimuli and exhibit two-tone rate suppression effects. The representation of stimulus level by NA was investigated by decoding the envelope of the input signal from populations of NA model neurons where the envelope was defined as in a previous computational model of sound localization in the barn owl [B.J. Fischer and C.H. Anderson, Adv. NIPS 16 (2004)]. Simulations demonstrated that inclusion of NA neurons with type IV responses increased the accuracy of the representation of the stimulus envelope. The effect of inhibition on the output of the population of NL model neurons was investigated and compared to a cross-correlation model. The output of the model SON provides inhibitory feedback to ipsilateral NA, NM, and NL model neurons. Simulations demonstrated that inclusion of inhibition of NL neurons by SON output increased peak–trough differences in ITD tuning curves.

Encoding of sound localization cues by an identified auditory interneuron: effects of stimulus temporal pattern.

An important cue for sound localization is binaural comparison of stimulus intensity. Two features of neuronal responses, response strength, i.e., spike count and/or rate, and response latency, vary with stimulus intensity, and binaural comparison of either or both might underlie localization. Previous studies at the receptor-neuron level showed that these response features are affected by the stimulus temporal pattern. When sounds are repeated rapidly, as occurs in many natural sounds, response strength decreases and latency increases, resulting in altered coding of localization cues. In this study we analyze binaural cues for sound localization at the level of an identified pair of interneurons (the left and right AN2) in the cricket auditory system, with emphasis on the effects of stimulus temporal pattern on binaural response differences. AN2 spike count decreases with rapidly repeated stimulation and latency increases. Both effects depend on stimulus intensity. Because of the difference in intensity at the two ears, binaural differences in spike count and latency change as stimulation continues. The binaural difference in spike count decreases, whereas the difference in latency increases. The proportional changes in response strength and in latency are greater at the interneuron level than at the receptor level, suggesting that factors in addition to decrement of receptor responses are involved. Intracellular recordings reveal that a slowly building, long-lasting hyperpolarization is established in AN2. At the same time, the level of depolarization reached during the excitatory postsynaptic potential (EPSP) resulting from each sound stimulus decreases. Neither these effects on membrane potential nor the changes in spiking response are accounted for by contralateral inhibition. Based on comparison of our results with earlier behavioral experiments, it is unlikely that crickets use the binaural difference in latency of AN2 responses as the main cue for determining sound direction, leaving the difference in response strength, i.e., spike count and/or rate, as the most likely candidate.

Monaural and binaural processing in the ventral nucleus of the lateral lemniscus: a major source of inhibition to the inferior colliculus

The ventral nucleus of the lateral lemniscus (VNLL) is a major source of input to the inferior colliculus. This paper reviews recent studies of neural responses in the VNLL of the unanesthetized rabbit. The VNLL has generally been viewed as a monaural nucleus, with its neurons responding primarily to stimulation of the contralateral ear. In the rabbit, the VNLL is divided into a medial division (VNLLm) comprising neurons intercalated in the medial limb of the lemniscus, a compact lateral division (VNLLl), and a dorsal division. The VNLLm contains an abundance of neurons sensitive to interaural temporal disparities (ITDs), one of the major binaural cues for sound localization. These neurons respond only at the onset of tones, and therefore appear to encode the ITDs of transients. Even in the VNLLl, many neurons are sensitive to binaural stimulation. The VNLLl contains a variety of neurons with different discharge patterns, the two most common of which are sustained and onset. The discharge patterns, frequency-tuning and dynamic ranges of VNLLl neurons indicate that this division is able to supply the inferior colliculus with a variety of inputs, each serving a different function in the analysis of sound.

Binaural interactions in primary auditory cortex of the awake macaque.

The functional organization of primary auditory cortex in non-primates is generally modeled as a tonotopic gradient with an orthogonal representation of independently mapped binaural interaction columns along the isofrequency contours. Little information is available regarding the validity of this model in the primate brain, despite the importance of binaural cues for sound localization and auditory scene analysis. Binaural and monaural responses of A1 to pure tone stimulation were studied using auditory evoked potentials, current source density and multiunit activity. Key findings include: (i) differential distribution of binaural responses with respect to best frequency, such that 74% of the sites exhibiting binaural summation had best frequencies below 2000 Hz; (ii) the pattern of binaural responses was variable with respect to cortical depth, with binaural summation often observed in the supragranular laminae of sites showing binaural suppression in thalamorecipient laminae; and (iii) dissociation of binaural responses between the initial and sustained action potential firing of neuronal ensembles in A1. These data support earlier findings regarding the temporal and spatial complexity of responses in A1 in the awake state, and are inconsistent with a simple orthogonal arrangement of binaural interaction columns and best frequency in A1 of the awake primate.

Responses of inferior colliculus neurons to time-varying interaural phase disparity: effects of shifting the locus of virtual motion.

1. Motion of sound sources results in temporal variation of the binaural cues for sound localization. We evaluated the influence of virtual motion on neural tuning to one of these cues, interaural phase disparity (IPD). Responses to dichotic stimuli were recorded from single units in the inferior colliculus of the anesthetized cat and gerbil (Meriones unguiculatus). Static IPDs were generated by presenting dichotic tone pairs with a constant phase offset maintained for the duration of the stimulus. Time-varying IPDs were generated by simultaneously presenting a pure tone to one ear and a phase-modulated tone to the other ear. Sets of time-varying stimuli consisted of modulations through partially overlapping ranges of IPD, corresponding to movement of a sound source through partially overlapping arcs in the horizontal plane. 2. In agreement with previous results, neuronal discharge was typically a peaked function of static IPD resulting from both binaural facilitation at favorable IPDs and binaural suppression at unfavorable IPDs. Responses to time-varying IPD stimuli appeared to be shaped by the same facilitative and inhibitory mechanisms that underlie static IPD tuning. Modulation toward the peak of binaural facilitation increased the probability of discharge, and modulation toward the peak of binaural suppression decreased the probability of discharge. However, it was also clear that IPD tuning could be significantly altered by the temporal context of the stimulus. For the vast majority of units in response to modulation through partially overlapping ranges of IPD the discharge rate profiles were generally nonoverlapping. This shift in IPD tuning induced by the virtual motion reflects the fact that the binaural interaction associated with a given IPD depends on the recent history of stimulation. In addition, modulation in opposite directions through the same range of IPDs often elicited asymmetric responses. These nonlinearities imply that most inferior colliculus neurons do not unambiguously encode a specific IPD, but instead may encode small changes of IPD occurring virtually anywhere within their receptive fields. In a few cases modulation through overlapping ranges of IPD elicited contiguous response profiles, indicating that for these units responses were determined entirely by instantaneous IPD. 3. The nonlinearity of responses to time-varying IPD stimuli could not be attributed to monaural entrainment to the phase-modulated signals, did not depend on the phase modulation waveform, and occurred irrespective of which ear received the phase-modulated signal. Responses were similar in cats and gerbils, suggesting that the underlying mechanisms are common to binaural processing in diverse mammalian species.(ABSTRACT TRUNCATED AT 400 WORDS)

Sound localization in a predatory rodent, the northern grasshopper mouse (Onychomys leucogaster).

A comparison of the ability of mammals to localize sound revealed that among the animals examined to date, none of the rodents have been able to localize as accurately as the carnivores. Because all of these rodents are prey animals, the question arises as to whether their poor localization acuity is a phyletic trait of Rodentia or whether it is a trait common to prey species that may be under less selective pressure than predators to localize sound accurately. To answer this question, sound localization acuity was determined in a species that is both predatory and a rodent, the northern grasshopper mouse. Localization thresholds for a single 100-ms noise burst were determined for three grasshopper mice using a conditioned avoidance procedure. Their 50% discrimination threshold of 19 degrees is larger than that of any of the previously tested carnivores and well within the range of other rodents. However, calculations of the binaural sound localization cues available to rodents (based on their head size) suggest that the grasshopper mouse may make more efficient use of the available locus cues than other rodents. Thus, although the grasshopper mouse cannot localize as accurately as carnivores, it appears to be more accurate than predicted for a nonpredatory rodent of its size.