Visual influences on auditory spatial learning

The visual and auditory systems frequently work together to facilitate the identification and localization of objects and events in the external world. Experience plays a critical role in establishing and maintaining congruent visual-auditory associations, so that the different sensory cues associated with targets that can be both seen and heard are synthesized appropriately. For stimulus location, visual information is normally more accurate and reliable and provides a reference for calibrating the perception of auditory space. During development, vision plays a key role in aligning neural representations of space in the brain, as revealed by the dramatic changes produced in auditory responses when visual inputs are altered, and is used throughout life to resolve short-term spatial conflicts between these modalities. However, accurate, and even supra-normal, auditory localization abilities can be achieved in the absence of vision, and the capacity of the mature brain to relearn to localize sound in the presence of substantially altered auditory spatial cues does not require visuomotor feedback. Thus, while vision is normally used to coordinate information across the senses, the neural circuits responsible for spatial hearing can be recalibrated in a vision-independent fashion. Nevertheless, early multisensory experience appears to be crucial for the emergence of an ability to match signals from different sensory modalities and therefore for the outcome of audiovisual-based rehabilitation of deaf patients in whom hearing has been restored by cochlear implantation.     

An ideal-observer model of human sound localization

In recent years, a great deal of research within the field of sound localization has been aimed at finding the acoustic cues that human listeners use to localize sounds and understanding the mechanisms by which they process these cues. In this paper, we propose a complementary approach by constructing an ideal-observer model, by which we mean a model that performs optimal information processing within a Bayesian context. The model considers all available spatial information contained within the acoustic signals encoded by each ear. Parameters for the optimal Bayesian model are determined based on psychoacoustic discrimination experiments on interaural time difference and sound intensity. Without regard as to how the human auditory system actually processes information, we examine the best possible localization performance that could be achieved based only on analysis of the input information, given the constraints of the normal auditory system. We show that the model performance is generally in good agreement with the actual human localization performance, as assessed in a meta-analysis of many localization experiments (Best et al. in Principles and applications of spatial hearing, pp 14–23. World Scientific Publishing, Singapore, 2011). We believe this approach can shed new light on the optimality (or otherwise) of human sound localization, especially with regard to the level of uncertainty in the input information. Moreover, the proposed model allows one to study the relative importance of various (combinations of) acoustic cues for spatial localization and enables a prediction of which cues are most informative and therefore likely to be used by humans in various circumstances.     

Development of Sound Localization Strategies in Children with Bilateral Cochlear Implants

Localizing sounds in our environment is one of the fundamental perceptual abilities that enable humans to communicate, and to remain safe. Because the acoustic cues necessary for computing source locations consist of differences between the two ears in signal intensity and arrival time, sound localization is fairly poor when a single ear is available. In adults who become deaf and are fitted with cochlear implants (CIs) sound localization is known to improve when bilateral CIs (BiCIs) are used compared to when a single CI is used. The aim of the present study was to investigate the emergence of spatial hearing sensitivity in children who use BiCIs, with a particular focus on the development of behavioral localization patterns when stimuli are presented in free-field horizontal acoustic space. A new analysis was implemented to quantify patterns observed in children for mapping acoustic space to a spatially relevant perceptual representation. Children with normal hearing were found to distribute their responses in a manner that demonstrated high spatial sensitivity. In contrast, children with BiCIs tended to classify sound source locations to the left and right; with increased bilateral hearing experience, they developed a perceptual map of space that was better aligned with the acoustic space. The results indicate experience-dependent refinement of spatial hearing skills in children with CIs. Localization strategies appear to undergo transitions from sound source categorization strategies to more fine-grained location identification strategies. This may provide evidence for neural plasticity, with implications for training of spatial hearing ability in CI users.     

Experience Changes How Emotion in Music Is Judged: Evidence from Children Listening with Bilateral Cochlear Implants,Bimodal Devices,and Normal Hearing

Children using unilateral cochlear implants abnormally rely on tempo rather than mode cues to distinguish whether a musical piece is happy or sad. This led us to question how this judgment is affected by the type of experience in early auditory development. We hypothesized that judgments of the emotional content of music would vary by the type and duration of access to sound in early life due to deafness, altered perception of musical cues through new ways of using auditory prostheses bilaterally, and formal music training during childhood. Seventy-five participants completed the Montreal Emotion Identification Test. Thirty-three had normal hearing (aged 6.6 to 40.0 years) and 42 children had hearing loss and used bilateral auditory prostheses (31 bilaterally implanted and 11 unilaterally implanted with contralateral hearing aid use). Reaction time and accuracy were measured. Accurate judgment of emotion in music was achieved across ages and musical experience. Musical training accentuated the reliance on mode cues which developed with age in the normal hearing group. Degrading pitch cues through cochlear implant-mediated hearing induced greater reliance on tempo cues, but mode cues grew in salience when at least partial acoustic information was available through some residual hearing in the contralateral ear. Finally, when pitch cues were experimentally distorted to represent cochlear implant hearing, individuals with normal hearing (including those with musical training) switched to an abnormal dependence on tempo cues. The data indicate that, in a western culture, access to acoustic hearing in early life promotes a preference for mode rather than tempo cues which is enhanced by musical training. The challenge to these preferred strategies during cochlear implant hearing (simulated and real), regardless of musical training, suggests that access to pitch cues for children with hearing loss must be improved by preservation of residual hearing and improvements in cochlear implant technology.     

A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals

Blind individuals often demonstrate enhanced nonvisual perceptual abilities. However, the neural substrate that underlies this improved performance remains to be fully understood. An earlier behavioral study demonstrated that some early-blind people localize sounds more accurately than sighted controls using monaural cues. In order to investigate the neural basis of these behavioral differences in humans, we carried out functional imaging studies using positron emission tomography and a speaker array that permitted pseudo-free-field presentations within the scanner. During binaural sound localization, a sighted control group showed decreased cerebral blood flow in the occipital lobe, which was not seen in early-blind individuals. During monaural sound localization (one ear plugged), the subgroup of early-blind subjects who were behaviorally superior at sound localization displayed two activation foci in the occipital cortex. This effect was not seen in blind persons who did not have superior monaural sound localization abilities, nor in sighted individuals. The degree of activation of one of these foci was strongly correlated with sound localization accuracy across the entire group of blind subjects. The results show that those blind persons who perform better than sighted persons recruit occipital areas to carry out auditory localization under monaural conditions. We therefore conclude that computations carried out in the occipital cortex specifically underlie the enhanced capacity to use monaural cues. Our findings shed light not only on intermodal compensatory mechanisms, but also on individual differences in these mechanisms and on inhibitory patterns that differ between sighted individuals and those deprived of vision early in life.     

Effect of audiovisual training on monaural spatial hearing in horizontal plane

The article aims to test the hypothesis that audiovisual integration can improve spatial hearing in monaural conditions when interaural difference cues are not available. We trained one group of subjects with an audiovisual task, where a flash was presented in parallel with the sound and another group in an auditory task, where only sound from different spatial locations was presented. To check whether the observed audiovisual effect was similar to feedback, the third group was trained using the visual feedback paradigm. Training sessions were administered once per day, for 5 days. The performance level in each group was compared for auditory only stimulation on the first and the last day of practice. Improvement after audiovisual training was several times higher than after auditory practice. The group trained with visual feedback demonstrated a different effect of training with the improvement smaller than the group with audiovisual training. We conclude that cross-modal facilitation is highly important to improve spatial hearing in monaural conditions and may be applied to the rehabilitation of patients with unilateral deafness and after unilateral cochlear implantation.     

Mechanisms of experience-dependent plasticity in the auditory localization pathway of the barn owl

Sound localization is a computational process that requires the central nervous system to measure various auditory cues and then associate particular cue values with appropriate locations in space. Behavioral experiments show that barn owls learn to associate values of cues with locations in space based on experience. The capacity for experience-driven changes in sound localization behavior is particularly great during a sensitive period that lasts until the approach of adulthood. Neurophysiological techniques have been used to determine underlying sites of plasticity in the auditory space-processing pathway. The external nucleus of the inferior colliculus (ICX), where a map of auditory space is synthesized, is a major site of plasticity. Experience during the sensitive period can cause large-scale, adaptive changes in the tuning of ICX neurons for sound localization cues. Large-scale physiological changes are accompanied by anatomical remodeling of afferent axons to the ICX. Changes in the tuning of ICX neurons for cue values involve two stages: (1) the instructed acquisition of neuronal responses to novel cue values and (2) the elimination of responses to inappropriate cue values. Newly acquired neuronal responses depend differentially on NMDA receptor currents for their expression. A model is presented that can account for this adaptive plasticity in terms of plausible cellular mechanisms. Accepted: 17 April 1999     

Development of the chloride homeostasis in the auditory brainstem

Inhibitory neurotransmission plays a substantial role in encoding of auditory cues relevant for sound localization in vertebrates. While the anatomical organization of the respective afferent auditory brainstem circuits shows remarkable similarities between mammals and birds, the properties of inhibitory neurotransmission in these neural circuits are strikingly different. In mammals, inhibition is predominantly glycinergic and endowed with fast kinetics. In birds, inhibition is mediated by gamma-Aminobutiric acid (GABA) and too slow to convey temporal information. A further prominent difference lies in the mechanism of inhibition in the respective systems. In auditory brainstem neurons of mammals, [Cl(-)](i) undergoes a developmental shift causing the actions of GABA and glycine to gradually change from depolarization to the 'classic' hyperpolarizing-inhibition before hearing onset. Contrary to this, in the mature avian auditory brainstem Cl(-) homeostasis mechanisms accurately adjust the Cl(-) gradient to enable depolarizing, but still very efficient, shunting inhibition. The present review considers the mechanisms underlying development of the Cl(-) homeostasis in the auditory system of mammals and birds and discusses some open issues that require closer attention in future studies.     

Mutation in the Kv3.3 Voltage-Gated Potassium Channel Causing Spinocerebellar Ataxia 13 Disrupts Sound-Localization Mechanisms

Normal sound localization requires precise comparisons of sound timing and pressure levels between the two ears. The primary localization cues are interaural time differences, ITD, and interaural level differences, ILD. Voltage-gated potassium channels, including Kv3.3, are highly expressed in the auditory brainstem and are thought to underlie the exquisite temporal precision and rapid spike rates that characterize brainstem binaural pathways. An autosomal dominant mutation in the gene encoding Kv3.3 has been demonstrated in a large Filipino kindred manifesting as spinocerebellar ataxia type 13 (SCA13). This kindred provides a rare opportunity to test in vivo the importance of a specific channel subunit for human hearing. Here, we demonstrate psychophysically that individuals with the mutant allele exhibit profound deficits in both ITD and ILD sensitivity, despite showing no obvious impairment in pure-tone sensitivity with either ear. Surprisingly, several individuals exhibited the auditory deficits even though they were pre-symptomatic for SCA13. We would expect that impairments of binaural processing as great as those observed in this family would result in prominent deficits in localization of sound sources and in loss of the "spatial release from masking" that aids in understanding speech in the presence of competing sounds.     

Identification of sound-localization cues in the HRTF of the bat-head model

Animals such as bats and dolphins exhibit impressive echolocation abilities in terms of ranging, resolution and imaging and therefore represent a valuable learning model for the study of spatial hearing and sound source localization leading to a better understanding of the hearing mechanism and further improvement of the existing localization strategies. This study aims to examine and understand the directional characteristics of a sonar receiver modeled upon the bat auditory system via measurements of the head-related transfer function (HRTF) in the horizontal plane. Four different models of the bat head were considered here and used to evaluate acoustic spectral characteristics of the sound received by the bat's ears – a sphere model, a sphere model with a pinna attached (two pinnae of different size were used in this study) and a bat-head cast. The performed HRTF measurements of the bat-head models were further analyzed and compared to identify monaural spectral localization cues in the horizontal plane defined by the bat's head and pinna shape and size. Our study suggests that the acoustical characteristics of a bio-inspired sonar head measured and specified in advance can potentially improve the performance of a receiver. Moreover, the generated auditory models may hold clues for the design of receiver characteristics in ultrasound imaging and navigation systems.     

Reversible induction of phantom auditory sensations through simulated unilateral hearing loss

Tinnitus, a phantom auditory sensation, is associated with hearing loss in most cases, but it is unclear if hearing loss causes tinnitus. Phantom auditory sensations can be induced in normal hearing listeners when they experience severe auditory deprivation such as confinement in an anechoic chamber, which can be regarded as somewhat analogous to a profound bilateral hearing loss. As this condition is relatively uncommon among tinnitus patients, induction of phantom sounds by a lesser degree of auditory deprivation could advance our understanding of the mechanisms of tinnitus. In this study, we therefore investigated the reporting of phantom sounds after continuous use of an earplug. 18 healthy volunteers with normal hearing wore a silicone earplug continuously in one ear for 7 days. The attenuation provided by the earplugs simulated a mild high-frequency hearing loss, mean attenuation increased from <10 dB at 0.25 kHz to >30 dB at 3 and 4 kHz. 14 out of 18 participants reported phantom sounds during earplug use. 11 participants presented with stable phantom sounds on day 7 and underwent tinnitus spectrum characterization with the earplug still in place. The spectra showed that the phantom sounds were perceived predominantly as high-pitched, corresponding to the frequency range most affected by the earplug. In all cases, the auditory phantom disappeared when the earplug was removed, indicating a causal relation between auditory deprivation and phantom sounds. This relation matches the predictions of our computational model of tinnitus development, which proposes a possible mechanism by which a stabilization of neuronal activity through homeostatic plasticity in the central auditory system could lead to the development of a neuronal correlate of tinnitus when auditory nerve activity is reduced due to the earplug.     

Localization dominance and the effect of frequency in the Mongolian Gerbil, Meriones unguiculatus

Due to its good low-frequency hearing, the Mongolian Gerbil (Meriones unguiculatus) has become a well-established animal model for human hearing. In humans, sound localization in reverberant environments is facilitated by the precedence effect, i.e., the perceptual suppression of spatial information carried by echoes. The current study addresses the question whether gerbils are a valid animal model for such complex spatial processing. Specifically, we quantify localization dominance, i.e., the fact that in the context of precedence, only the directional information of the sound which reaches the ear first dominates the perceived position of a sound source whereas directional information of the delayed echoes is suppressed. As localization dominance is known to be stimulus-dependent, we quantified the extent to which the spectral content of transient sounds affects localization dominance in the gerbil. The results reveal that gerbils show stable localization dominance across echo delays, well comparable to humans. Moreover, localization dominance systematically decreased with increasing center frequency, which has not been demonstrated in an animal before. These findings are consistent with an important contribution of peripheral-auditory processing to perceptual localization dominance. The data show that the gerbil is an excellent model to study the neural basis of complex spatial-auditory processing.     

A Dominance Hierarchy of Auditory Spatial Cues in Barn Owls

Background

Barn owls integrate spatial information across frequency channels to localize sounds in space.

Methodology/Principal Findings

We presented barn owls with synchronous sounds that contained different bands of frequencies (3–5 kHz and 7–9 kHz) from different locations in space. When the owls were confronted with the conflicting localization cues from two synchronous sounds of equal level, their orienting responses were dominated by one of the sounds: they oriented toward the location of the low frequency sound when the sources were separated in azimuth; in contrast, they oriented toward the location of the high frequency sound when the sources were separated in elevation. We identified neural correlates of this behavioral effect in the optic tectum (OT, superior colliculus in mammals), which contains a map of auditory space and is involved in generating orienting movements to sounds. We found that low frequency cues dominate the representation of sound azimuth in the OT space map, whereas high frequency cues dominate the representation of sound elevation.

Conclusions/Significance

We argue that the dominance hierarchy of localization cues reflects several factors: 1) the relative amplitude of the sound providing the cue, 2) the resolution with which the auditory system measures the value of a cue, and 3) the spatial ambiguity in interpreting the cue. These same factors may contribute to the relative weighting of sound localization cues in other species, including humans.     

Hearing Loss in a Mouse Model of 22q11.2 Deletion Syndrome

22q11.2 Deletion Syndrome (22q11DS) arises from an interstitial chromosomal microdeletion encompassing at least 30 genes. This disorder is one of the most significant known cytogenetic risk factors for schizophrenia, and can also cause heart abnormalities, cognitive deficits, hearing difficulties, and a variety of other medical problems. The Df1/+ hemizygous knockout mouse, a model for human 22q11DS, recapitulates many of the deficits observed in the human syndrome including heart defects, impaired memory, and abnormal auditory sensorimotor gating. Here we show that Df1/+ mice, like human 22q11DS patients, have substantial rates of hearing loss arising from chronic middle ear infection. Auditory brainstem response (ABR) measurements revealed significant elevation of click-response thresholds in 48% of Df1/+ mice, often in only one ear. Anatomical and histological analysis of the middle ear demonstrated no gross structural abnormalities, but frequent signs of otitis media (OM, chronic inflammation of the middle ear), including excessive effusion and thickened mucosa. In mice for which both in vivo ABR thresholds and post mortem middle-ear histology were obtained, the severity of signs of OM correlated directly with the level of hearing impairment. These results suggest that abnormal auditory sensorimotor gating previously reported in mouse models of 22q11DS could arise from abnormalities in auditory processing. Furthermore, the findings indicate that Df1/+ mice are an excellent model for increased risk of OM in human 22q11DS patients. Given the frequently monaural nature of OM in Df1/+ mice, these animals could also be a powerful tool for investigating the interplay between genetic and environmental causes of OM.     

Auditory rehabilitation

Auditory rehabilitation depends of the cause and the severity of the hearing loss (or deafness). Hearing losses dues to middle ear pathologies can beneficiate of medical or surgical treatments, by ossicular prostheses, if it is necessary to restore the function of the ossicles chain. In the sensorineural hearing losses, with inner ear pathology, the use of auditory aid is immediately considered. In the cases for which they are insufficient because of severity of the hearing loss or not suitable because of local non-tolerance, it is possible to use middle ear implant or cochlear implant. The indications of the auditory brainstern implants remain at this day limited to the total bilateral hearing losses due to a complete destruction of cochleae and auditory nerves. These therapeutic orientations are selected after a multidisciplinary evaluation of the deaf person, evaluation that allows the characterization of the hearing loss and its repercussion. In all the cases, the restoration of a bilateral hearing has to be done if possible, making an improvement of the speech comprehension, mainly in the noisy situations, as well as the localization of the sound sources.     

High binaural coherence determines successful sound localization and increased activity in posterior auditory areas

Our brain continuously receives complex combinations of sounds originating from different sources and relating to different events in the external world. Timing differences between the two ears can be used to localize sounds in space, but only when the inputs to the two ears have similar spectrotemporal profiles (high binaural coherence). We used fMRI to investigate any modulation of auditory responses by binaural coherence. We assessed how processing of these cues depends on whether spatial information is task relevant and whether brain activity correlates with subjects' localization performance. We found that activity in Heschl's gyrus increased with increasing coherence, irrespective of whether localization was task relevant. Posterior auditory regions also showed increased activity for high coherence, primarily when sound localization was required and subjects successfully localized sounds. We conclude that binaural coherence cues are processed throughout the auditory cortex and that these cues are used in posterior regions for successful auditory localization.     

Chronic Conductive Hearing Loss Leads to Cochlear Degeneration

Synapses between cochlear nerve terminals and hair cells are the most vulnerable elements in the inner ear in both noise-induced and age-related hearing loss, and this neuropathy is exacerbated in the absence of efferent feedback from the olivocochlear bundle. If age-related loss is dominated by a lifetime of exposure to environmental sounds, reduction of acoustic drive to the inner ear might improve cochlear preservation throughout life. To test this, we removed the tympanic membrane unilaterally in one group of young adult mice, removed the olivocochlear bundle in another group and compared their cochlear function and innervation to age-matched controls one year later. Results showed that tympanic membrane removal, and the associated threshold elevation, was counterproductive: cochlear efferent innervation was dramatically reduced, especially the lateral olivocochlear terminals to the inner hair cell area, and there was a corresponding reduction in the number of cochlear nerve synapses. This loss led to a decrease in the amplitude of the suprathreshold cochlear neural responses. Similar results were seen in two cases with conductive hearing loss due to chronic otitis media. Outer hair cell death was increased only in ears lacking medial olivocochlear innervation following olivocochlear bundle cuts. Results suggest the novel ideas that 1) the olivocochlear efferent pathway has a dramatic use-dependent plasticity even in the adult ear and 2) a component of the lingering auditory processing disorder seen in humans after persistent middle-ear infections is cochlear in origin.     

Cochlear implants: the view from the brain

The cochlear implant arguably is the most successful neural prosthesis. Studies of the responses of the central auditory system to prosthetic electrical stimulation of the cochlea are revealing the success with which electrical stimulation of a deaf ear can mimic acoustic stimulation of a normal-hearing ear. Understanding of the physiology of central auditory structures can lead to improved restoration of hearing with cochlear implants. In turn, the cochlear implant can be exploited as an experimental tool for examining central hearing mechanisms isolated from the effects of cochlear mechanics and transduction.     

Expression of polysialylated neural cell adhesion molecules on adult stem cells after neuronal differentiation of inner ear spiral ganglion neurons

During brain development, polysialylated (polySia) neural cell adhesion molecules (polySia–NCAMs) modulate cell–cell adhesive interactions involved in synaptogenesis, neural plasticity, myelination, and neural stem cell (NSC) proliferation and differentiation. Our findings show that polySia–NCAM is expressed on NSC isolated from adult guinea pig spiral ganglion (GPSG), and in neurons and Schwann cells after differentiation of the NSC with epidermal, glia, fibroblast growth factors (GFs) and neurotrophins. These differentiated cells were immunoreactive with mAb’s to polySia, NCAM, β-III tubulin, nestin, S-100 and stained with BrdU. NSC could regenerate and be differentiated into neurons and Schwann cells. We conclude: (1) polySia is expressed on NSC isolated from adult GPSG and on neurons and Schwann cells differentiated from these NSC; (2) polySia is expressed on neurons primarily during the early stage of neuronal development and is expressed on Schwann cells at points of cell–cell contact; (3) polySia is a functional biomarker that modulates neuronal differentiation in inner ear stem cells. These new findings suggest that replacement of defective cells in the inner ear of hearing impaired patients using adult spiral ganglion neurons may offer potential hope to improve the quality of life for patients with auditory dysfunction and impaired hearing disorders.