Representation Of Auditory Space Research Articles

Population coding of auditory space in the dorsal inferior colliculus persists with altered binaural cues.

Sound localization is critical for real-world hearing, such as segregating overlapping sound streams. For optimal flexibility, central representations of auditory space must adapt to peripheral changes in binaural cue availability, such as following asymmetric hearing loss in adulthood. However, whether the mature auditory system can reliably encode spatial auditory representations upon abrupt changes in binaural input is unclear. Here we use 2-photon Ca2+ imaging in awake head-fixed mice to determine how the higher-order "shell" layers of the inferior colliculus (IC) encode sound source location in the frontal azimuth, under binaural conditions and after acute monaural hearing loss induced by an ear plug ipsilateral to the imaged hemisphere. Spatial receptive fields were typically broad and not exclusively contralateral: Neurons responded reliably to multiple positions in the contra- and ipsi-lateral hemifields, with preferred positions tiling the entire frontal azimuth. Ear plugging broadened receptive fields and reduced spatial selectivity in a subset of neurons, in agreement with an inhibitory influence of ipsilateral sounds. However ear plugging also enhanced spatial tuning and/or unmasked receptive fields in other neurons, shifting the distribution of preferred angles ipsilaterally with minimal impact on the neuronal population's overall spatial resolution; these effects occurred within 2 hours of ear plugging. Consequently, linear classifiers trained on fluorescence data from control and ear-plugged conditions had similar classification accuracy when tested on held out data from within, but not across hearing conditions. Spatially informative neuronal population codes therefore arise rapidly following monaural hearing loss, in absence of overt experience.

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.

Two Types of Auditory Spatial Receptive Fields in Different Parts of the Chicken's Midbrain.

The optic tectum (OT) is an avian midbrain structure involved in the integration of visual and auditory stimuli. Studies in the barn owl, an auditory specialist, have shown that spatial auditory information is topographically represented in the OT. Little is known about how auditory space is represented in the midbrain of birds with generalist hearing, i.e., most of avian species lacking peripheral adaptations such as facial ruffs or asymmetric ears. Thus, we conducted in vivo extracellular recordings of single neurons in the OT and in the external portion of the formatio reticularis lateralis (FRLx), a brain structure located between the inferior colliculus (IC) and the OT, in anaesthetized chickens of either sex. We found that most of the auditory spatial receptive fields (aSRFs) were spatially confined both in azimuth and elevation, divided into two main classes: round aSRFs, mainly present in the OT, and annular aSRFs, with a ring-like shape around the interaural axis, mainly present in the FRLx. Our data further indicate that interaural time difference (ITD) and interaural level difference (ILD) play a role in the formation of both aSRF classes. These results suggest that, unlike mammals and owls which have a congruent representation of visual and auditory space in the OT, generalist birds separate the computation of auditory space in two different midbrain structures. We hypothesize that the FRLx-annular aSRFs define the distance of a sound source from the axis of the lateral visual fovea, whereas the OT-round aSRFs are involved in multimodal integration of the stimulus around the lateral fovea.SIGNIFICANCE STATEMENT Previous studies implied that auditory spatial receptive fields (aSRFs) in the midbrain of generalist birds are only confined along azimuth. Interestingly, we found SRFs s in the chicken to be confined along both azimuth and elevation. Moreover, the auditory receptive fields are arranged in a concentric manner around the overlapping interaural and visual axes. These data suggest that in generalist birds, which mainly rely on vision, the auditory system mainly serves to align auditory stimuli with the visual axis, while auditory specialized birds like the barn owl compute sound sources more precisely and integrate sound positions in the multimodal space map of the optic tectum (OT).

High-Frequency Hearing Is Required to Compute a Topographic Map of Auditory Space in the Mouse Superior Colliculus.

A topographic map of auditory space is a feature found in the superior colliculus (SC) of many species, including CBA/CaJ mice. In this genetic background, high-frequency monaural spectral cues and interaural level differences (ILDs) are used to compute spatial receptive fields (RFs) that form a topographic map along the azimuth. Unfortunately, C57BL/6 mice, a strain widely used for transgenic manipulation, display age-related hearing loss (AHL) because of an inbred mutation in the Cadherin 23 gene (Cdh23) that affects hair cell mechanotransduction. To overcome this problem, researchers have used young C57BL/6 mice in their studies, as they have been shown to have normal hearing thresholds. However, important details of the auditory response characteristics of the SC such as spectral responses and spatial localization, have not been characterized in young C57BL/6 mice. Here, we show that two- to four-month C57BL/6 mice lack neurons with frontal auditory RFs and therefore lack a topographic representation of auditory space in the SC. Analysis of the spectrotemporal RFs (STRFs) of the SC auditory neurons shows that C57BL/6 mouse SC neurons lack the ability to detect the high-frequency (>40 kHz) spectral cues that are needed to compute frontal RFs. We also show that crossing C57BL/6 mice with CBA/CaJ mice or introducing one copy of the wild-type Cdh23 to C57BL/6 mice rescues the high-frequency hearing deficit and improves the topographic map of auditory space. Taken together, these results demonstrate the importance of high-frequency hearing in computing a topographic map of auditory space.

No effect of 10-week training in click-based echolocation on auditory localization in people who are blind

What factors are important in the calibration of mental representations of auditory space? A substantial body of research investigating the audiospatial abilities of people who are blind has shown that visual experience might be an important factor for accurate performance in some audiospatial tasks. Yet, it has also been shown that long-term experience using click-based echolocation might play a similar role, with blind expert echolocators demonstrating auditory localization abilities that are superior to those of people who are blind and who do not use click-based echolocation by Vercillo et al. (Neuropsychologia 67: 35–40, 2015). Based on this hypothesis we might predict that training in click-based echolocation may lead to improvement in performance in auditory localization tasks in people who are blind. Here we investigated this hypothesis in a sample of 12 adult people who have been blind from birth. We did not find evidence for an improvement in performance in auditory localization after 10 weeks of training despite significant improvement in echolocation ability. It is possible that longer-term experience with click-based echolocation is required for effects to develop, or that other factors can explain the association between echolocation expertise and superior auditory localization. Considering the practical relevance of click-based echolocation for people who are visually impaired, future research should address these questions.

Time attracts auditory space representation during development

Vision is the most accurate sense for spatial representation, whereas audition is for temporal representation. However, how different sensory modalities shape the development of spatial and temporal representations is still unclear. Here, 45 children aged 11–13 years were tested to investigate the abilities to evaluate spatial features of auditory stimuli during bisection tasks, while conflicting or non-conflicting spatial and temporal information was delivered. Since audition is fundamental for temporal representation, the hypothesis was that temporal information could influence auditory spatial representation development. Results show a strong interaction between the temporal and the spatial domain. Younger children are not able to build complex spatial representations when the temporal domain is uninformative about space. However, when the spatial information is coherent with the temporal information children of all age are able to decode complex spatial relationships. When spatial and temporal cues are conflicting, younger children are strongly attracted by the temporal instead of spatial information, while older participants result unaffected by the cross-domain conflict. These findings suggest that during development temporal representation of events is used to infer spatial coordinates of the environment, offering important opportunities for new teaching and rehabilitation strategies.

Neurons in primary auditory cortex represent sound source location in a cue-invariant manner

Auditory cortex is required for sound localisation, but how neural firing in auditory cortex underlies our perception of sound sources in space remains unclear. Specifically, whether neurons in auditory cortex represent spatial cues or an integrated representation of auditory space across cues is not known. Here, we measured the spatial receptive fields of neurons in primary auditory cortex (A1) while ferrets performed a relative localisation task. Manipulating the availability of binaural and spectral localisation cues had little impact on ferrets’ performance, or on neural spatial tuning. A subpopulation of neurons encoded spatial position consistently across localisation cue type. Furthermore, neural firing pattern decoders outperformed two-channel model decoders using population activity. Together, these observations suggest that A1 encodes the location of sound sources, as opposed to spatial cue values.

Where did that noise come from? Memory for sound locations is exceedingly eccentric both in front and in rear space.

Few studies have examined the stability of the representation of the position of sound sources in spatial working memory. The goal of this study was to verify whether the memory of sound position declines as maintenance time increases. In two experiments, we tested the influence of the delay between stimulus and response in a sound localization task. In Experiment 1, blindfolded participants listened to bursts of white noise originating from 16 loudspeakers equally spaced in a 360-degree circular space around the listener in such a way that the nose was aligned to the zero-degree coordinate. Their task was to indicate sounds' position using a digital pointer when prompted at varying delays: 0, 3, and 6s after stimulus offset. In Experiment 2, the task was analogous to Exp. 1 with stimulus-response delays of 0 or 10s. Results of the two experiments show that increasing stimulus-response delays up to 10s do not impair sound localization. Participants systematically overestimated the eccentricity of the auditory stimulus by shifting their responses either toward the 90-degree coordinate, in alignment with the right ear, or toward the 270-degree coordinate, in alignment with the left ear. Such bias was analogous in the front and in the rear azimuthal space and was only marginally influenced by the delay conditions. We conclude that the representation of auditory space in working memory is stable, but directionally biased with systematic overestimation of eccentricity.

Distinct mechanisms govern recalibration to audio-visual discrepancies in remote and recent history

To maintain perceptual coherence, the brain corrects for discrepancies between the senses. If, for example, lights are consistently offset from sounds, representations of auditory space are remapped to reduce this error (spatial recalibration). While recalibration effects have been observed following both brief and prolonged periods of adaptation, the relative contribution of discrepancies occurring over these timescales is unknown. Here we show that distinct multisensory recalibration mechanisms operate in remote and recent history. To characterise the dynamics of this spatial recalibration, we adapted human participants to audio-visual discrepancies for different durations, from 32 to 256 seconds, and measured the aftereffects on perceived auditory location. Recalibration effects saturated rapidly but decayed slowly, suggesting a combination of transient and sustained adaptation mechanisms. When long-term adaptation to an audio-visual discrepancy was immediately followed by a brief period of de-adaptation to an opposing discrepancy, recalibration was initially cancelled but subsequently reappeared with further testing. These dynamics were best fit by a multiple-exponential model that monitored audio-visual discrepancies over distinct timescales. Recent and remote recalibration mechanisms enable the brain to balance rapid adaptive changes to transient discrepancies that should be quickly forgotten against slower adaptive changes to persistent discrepancies likely to be more permanent.

Stronger responses in the visual cortex of sighted compared to blind individuals during auditory space representation

It has been previously shown that the interaction between vision and audition involves early sensory cortices. However, the functional role of these interactions and their modulation due to sensory impairment is not yet understood. To shed light on the impact of vision on auditory spatial processing, we recorded ERPs and collected psychophysical responses during space and time bisection tasks in sighted and blind participants. They listened to three consecutive sounds and judged whether the second sound was either spatially or temporally further from the first or the third sound. We demonstrate that spatial metric representation of sounds elicits an early response of the visual cortex (P70) which is different between sighted and visually deprived individuals. Indeed, only in sighted and not in blind people P70 is strongly selective for the spatial position of sounds, mimicking many aspects of the visual-evoked C1. These results suggest that early auditory processing associated with the construction of spatial maps is mediated by visual experience. The lack of vision might impair the projection of multi-sensory maps on the retinotopic maps used by the visual cortex.

Behavioral and neural spatial acuity can be persistently reduced by early temporary hearing loss

Children experiencing asymmetrical hearing early in life, typically due to conductive hearing loss (CHL) associated with ear infection, often display reduced behavioral spatial acuity that persists long after hearing is restored, suggesting abnormal central auditory development. We hypothesized that persistent CHL disrupts the experience-dependent fine-tuning of binaural hearing necessary in the developing auditory system to support normal behavioral spatial acuity. Using an animal model (the guinea pig), we found that chronic unilateral CHL during development (induced by an earplug) caused the brain to generate a less precise representation of auditory space. When the hearing loss was reversed by simply removing the earplug, both the spatial acuity of single neurons in the inferior colliculus and behavioral performance in a simple sound location acuity task were ~threefold worse than animals that had not worn earplugs, as if the sense of auditory space had been blurred. Overall, the results suggest that experiencing even temporary hearing loss during early development can persistently alter the normal maturation of the auditory brain circuits that are necessary to support good spatial acuity. Thus, the maladaptive plasticity in these circuits due to temporary hearing loss during development can place limitations on spatial acuity in adulthood. [Support: R01-DC011555, T32-DC012280, F31-DC014219.]

Neural tracking of auditory motion is reflected by delta phase and alpha power of EEG

It is of increasing practical interest to be able to decode the spatial characteristics of an auditory scene from electrophysiological signals. However, the cortical representation of auditory space is not well characterized, and it is unclear how cortical activity reflects the time-varying location of a moving sound. Recently, we demonstrated that cortical response measures to discrete noise bursts can be decoded to determine their origin in space. Here we build on these findings to investigate the cortical representation of a continuously moving auditory stimulus using scalp recorded electroencephalography (EEG).In a first experiment, subjects listened to pink noise over headphones which was spectro-temporally modified to be perceived as randomly moving on a semi-circular trajectory in the horizontal plane. While subjects listened to the stimuli, we recorded their EEG using a 128-channel acquisition system. The data were analysed by 1) building a linear regression model (decoder) mapping the relationship between the stimulus location and a training set of EEG data, and 2) using the decoder to reconstruct an estimate of the time-varying sound source azimuth from the EEG data. The results showed that we can decode sound trajectory with a reconstruction accuracy significantly above chance level. Specifically, we found that the phase of delta (<2 Hz) and power of alpha (8–12 Hz) EEG track the dynamics of a moving auditory object.In a follow-up experiment, we replaced the noise with pulse train stimuli containing only interaural level and time differences (ILDs and ITDs respectively). This allowed us to investigate whether our trajectory decoding is sensitive to both acoustic cues. We found that the sound trajectory can be decoded for both ILD and ITD stimuli. Moreover, their neural signatures were similar and even allowed successful cross-cue classification. This supports the notion of integrated processing of ILD and ITD at the cortical level. These results are particularly relevant for application in devices such as cognitively controlled hearing aids and for the evaluation of virtual acoustic environments.

Emergence of an Adaptive Command for Orienting Behavior in Premotor Brainstem Neurons of Barn Owls

The midbrain map of auditory space commands sound-orienting responses in barn owls. Owls precisely localize sounds in frontal space but underestimate the direction of peripheral sound sources. This bias for central locations was proposed to be adaptive to the decreased reliability in the periphery of sensory cues used for sound localization by the owl. Understanding the neural pathway supporting this biased behavior provides a means to address how adaptive motor commands are implemented by neurons. Here we find that the sensory input for sound direction is weighted by its reliability in premotor neurons of the midbrain tegmentum of owls (male and female), such that the mean population firing rate approximates the head-orienting behavior. We provide evidence that this coding may emerge through convergence of upstream projections from the midbrain map of auditory space. We further show that manipulating the sensory input yields changes predicted by the convergent network in both premotor neural responses and behavior. This work demonstrates how a topographic sensory representation can be linearly read out to adjust behavioral responses by the reliability of the sensory input.SIGNIFICANCE STATEMENT This research shows how statistics of the sensory input can be integrated into a behavioral command by readout of a sensory representation. The firing rate of midbrain premotor neurons receiving sensory information from a topographic representation of auditory space is weighted by the reliability of sensory cues. We show that these premotor responses are consistent with a weighted convergence from the topographic sensory representation. This convergence was also tested behaviorally, where manipulation of stimulus properties led to bidirectional changes in sound localization errors. Thus a topographic representation of auditory space is translated into a premotor command for sound localization that is modulated by sensory reliability.

Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat.

Essential to spatial orientation in the natural environment is a dynamic representation of direction and distance to objects. Despite the importance of 3D spatial localization to parse objects in the environment and to guide movement, most neurophysiological investigations of sensory mapping have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here, we show for the first time that sensory neurons in the midbrain superior colliculus (SC) of the free-flying echolocating bat encode 3D egocentric space, and that the bat's inspection of objects in the physical environment sharpens tuning of single neurons, and shifts peak responses to represent closer distances. These findings emerged from wireless neural recordings in free-flying bats, in combination with an echo model that computes the animal's instantaneous stimulus space. Our research reveals dynamic 3D space coding in a freely moving mammal engaged in a real-world navigation task.

Binaural responses in the auditory midbrain of chicken (Gallus gallus).

The auditory midbrain is the location in which neurons represent binaural acoustic information necessary for sound localization. The external nucleus of the midbrain inferior colliculus (IC) of the barn owl is a classic example of an auditory space map, but it is unknown to what extent the principles underlying its formation generalize to other, less specialized animals. We characterized the spiking responses of 139 auditory neurons in the IC of the chicken (Gallus gallus) invivo, focusing on their sensitivities to the binaural localization cues of interaural time (ITD) and level (ILD) differences. Most units were frequency-selective, with best frequencies distributed unevenly into low-frequency and high-frequency (>2kHz) clusters. Many units showed sensitivity to either ITD (65%) or ILD (66%) and nearly half to both (47%). ITD selectivity was disproportionately more common among low-frequency units, while ILD-only selective units were predominantly tuned to high frequencies. ILD sensitivities were diverse, and we thus developed a decision tree defining five types. One rare type with a bell-like ILD tuning was also selective for ITD but typically not frequency-selective, and thus matched the characteristics of neurons in the auditory space map of the barn owl. Our results suggest that generalist birds such as the chicken show a prominent representation of ITD and ILD cues in the IC, providing complementary information for sound localization, according to the duplex theory. A broadband response type narrowly selective for both ITD and ILD may form the basis for a representation of auditory space.

How the Barn Owl Computes Auditory Space

In a series of seminal behavioral and electrophysiological experiments, Knudsen and Konishi studied the mechanisms of hearing. Their 1979 article showed how the barn owl utilizes unique anatomical features for creating a systematic internal representation of auditory space. This established the barn owl as a prime model for studying sensory systems.

Influence of Visual Prism Adaptation on Auditory Space Representation.

Prisms shifting the visual input sideways produce a mismatch between the visual versus felt position of one’s hand. Prism adaptation eliminates this mismatch, realigning hand proprioception with visual input. Whether this realignment concerns exclusively the visuo-(hand)motor system or it generalizes to acoustic inputs is controversial. We here show that there is indeed a slight influence of visual adaptation on the perceived direction of acoustic sources. However, this shift in perceived auditory direction can be fully explained by a subconscious head rotation during prism exposure and by changes in arm proprioception. Hence, prism adaptation does only indirectly generalize to auditory space perception.

Audio Spatial Representation Around the Body.

Studies have found that portions of space around our body are differently coded by our brain. Numerous works have investigated visual and auditory spatial representation, focusing mostly on the spatial representation of stimuli presented at head level, especially in the frontal space. Only few studies have investigated spatial representation around the entire body and its relationship with motor activity. Moreover, it is still not clear whether the space surrounding us is represented as a unitary dimension or whether it is split up into different portions, differently shaped by our senses and motor activity. To clarify these points, we investigated audio localization of dynamic and static sounds at different body levels. In order to understand the role of a motor action in auditory space representation, we asked subjects to localize sounds by pointing with the hand or the foot, or by giving a verbal answer. We found that the audio sound localization was different depending on the body part considered. Moreover, a different pattern of response was observed when subjects were asked to make actions with respect to the verbal responses. These results suggest that the audio space around our body is split in various spatial portions, which are perceived differently: front, back, around chest, and around foot, suggesting that these four areas could be differently modulated by our senses and our actions.

Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat

Our natural world is three-dimensional. A fundamental requirement of spatial orientating behaviors in the natural environment is the representation of 3D sensory space. Despite the importance of 3D sensory coding of a natural scene to guide movement, most neurophysiological investigations of this problem have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here we show for the first time that auditory neurons in the midbrain superior colliculus of the free-flying echolocating bat encode 3D egocentric sensory space, and that sonar-guided inspection of objects in the environment sharpens spatial tuning of single neurons. Combining wireless multichannel neural recordings from free-flying bats, synchronized with video and audio data, and an echo model that computes the flying animal’s instantaneous, stimulus space, we demonstrate 3D echo-evoked receptive fields of single auditory midbrain neurons in animals orienting in a complex environment. We discovered that the bat’s ac...

Evidence for cue-independent spatial representation in the human auditory cortex during active listening

Few auditory functions are as important or as universal as the capacity for auditory spatial awareness (e.g., sound localization). That ability relies on sensitivity to acoustical cues-particularly interaural time and level differences (ITD and ILD)-that correlate with sound-source locations. Under nonspatial listening conditions, cortical sensitivity to ITD and ILD takes the form of broad contralaterally dominated response functions. It is unknown, however, whether that sensitivity reflects representations of the specific physical cues or a higher-order representation of auditory space (i.e., integrated cue processing), nor is it known whether responses to spatial cues are modulated by active spatial listening. To investigate, sensitivity to parametrically varied ITD or ILD cues was measured using fMRI during spatial and nonspatial listening tasks. Task type varied across blocks where targets were presented in one of three dimensions: auditory location, pitch, or visual brightness. Task effects were localized primarily to lateral posterior superior temporal gyrus (pSTG) and modulated binaural-cue response functions differently in the two hemispheres. Active spatial listening (location tasks) enhanced both contralateral and ipsilateral responses in the right hemisphere but maintained or enhanced contralateral dominance in the left hemisphere. Two observations suggest integrated processing of ITD and ILD. First, overlapping regions in medial pSTG exhibited significant sensitivity to both cues. Second, successful classification of multivoxel patterns was observed for both cue types and-critically-for cross-cue classification. Together, these results suggest a higher-order representation of auditory space in the human auditory cortex that at least partly integrates the specific underlying cues.