Auditory Spatial Tuning Research Articles

The auditory space in the motor system

Sensory events in the space around us trigger specific motor patterns directed toward or away from the spatial location of the sensory source. Spatially-defined sensorimotor associations are well-known in the visual domain but less so for the auditory modality. In particular no spatially-directed audio-motor association has been described for the upper limb. We tested the instantaneous directional tuning of the corticospinal system by means of single-pulse transcranial magnetic stimulation (TMS) over the left motor cortex in 16 healthy volunteers while at rest. We recorded the lateral accelerations of the TMS-evoked movement by means of an accelerometer placed on the forearm. Acoustic stimuli (pure tone frequency=1000Hz, duration=50ms) coming from 25 different directions lying in the axial anterior half-plane at the height of the participant’s ears were played on earphones. The entire set of sound directions covered a span of 160° (±80° where 0° is the frontal direction) at a fixed azimuth angle. Six different intervals between sound onset and TMS (0, 25, 50, 100, 150 and 200ms) were tested for each sound direction. Significant correlations were found between sound origin and TMS-evoked arm accelerations only when TMS was delivered 50ms prior to sound onset. We show the presence in the upper limb motor system of auditory spatial tuning. Sound information accesses the motor system at very short latency, potentially compatible with both a subcortical and a cortical origin of the response. The use of TMS-evoked accelerations allowed us to disclose a strict directional tuning in audio-motor associations.

Linear Processing of Interaural Level Difference Underlies Spatial Tuning in the Nucleus of the Brachium of the Inferior Colliculus

The spatial location of sounds is an important aspect of auditory perception, but the ways in which space is represented are not fully understood. No space map has been found within the primary auditory pathway. However, a space map has been found in the nucleus of the brachium of the inferior colliculus (BIN), which provides a major auditory projection to the superior colliculus. We measured the spectral processing underlying auditory spatial tuning in the BIN of unanesthetized marmoset monkeys. Because neurons in the BIN respond poorly to tones and are broadly tuned, we used a broadband stimulus with random spectral shapes (RSSs) from which both spatial receptive fields and frequency sensitivity can be derived. Responses to virtual space (VS) stimuli, based on the animal's own ear acoustics, were compared with the predictions of a weight-function model of responses to the RSS stimuli. First-order (linear) weight functions had broad spectral tuning (approximately three octaves) and were excitatory in the contralateral ear, inhibitory in the ipsilateral ear, and biased toward high frequencies. Responses to interaural time differences and spectral cues were relatively weak. In cross-validation tests, the first-order RSS model accurately predicted the measured VS tuning curves in the majority of neurons, but was inaccurate in 25% of neurons. In some cases, second-order weighting functions led to significant improvements. Finally, we found a significant correlation between the degree of binaural weight asymmetry and the best azimuth. Overall, the results suggest that linear processing of interaural level difference underlies spatial tuning in the BIN.

Auditory Spatial Tuning at the Crossroads of the Midbrain and Forebrain

The barn owl's midbrain and forebrain contain neurons tuned to sound direction. The spatial receptive fields of these neurons result from sensitivity to combinations of interaural time (ITD) and level (ILD) differences over a broad frequency range. While a map of auditory space has been described in the midbrain, no similar topographic representation has been found in the forebrain. The first nuclei that belong exclusively to the forebrain and midbrain pathways are the thalamic nucleus ovoidalis (Ov) and the external nucleus of the inferior colliculus (ICx), respectively. The midbrain projects to the auditory thalamus before sharp spatial receptive fields emerge; although Ov and ICx receive projections from the same midbrain nuclei, they are not directly connected. We compared the spatial tuning in Ov and ICx. Thalamic neurons respond to a broader frequency range and their ITD and ILD tuning varied more across frequency. However, neurons in Ov showed spatial receptive fields as selective as neurons in ICx. Thalamic spatial receptive fields were tuned to frontal and contralateral space and correlated with their tuning to ITD and ILD. Our results indicate that spatial tuning emerges in both pathways by similar combination selectivity to ITD and ILD. However, the midbrain and the thalamus do not appear to repeat exactly the same processing, as indicated by the difference in frequency range and the broader tuning to binaural cues. The differences observed at the initial stages of these sound-localization pathways may reflect diverse functions and coding schemes of midbrain and forebrain.

Auditory Spatial Tuning in Late-onset Blindness in Humans

Abstract Blind individuals who lost their sight as older children or adults were compared with normally sighted controls in their ability to focus auditory spatial attention and to localize sounds in a noisy acoustic environment. Event-related potentials (ERPs) were recorded while participants attended to sounds presented in free field from either central or peripheral arrays of speakers with the task of detecting infrequent targets at the attended location. When attending to the central array of speakers, the two groups detected targets equally well, and their spatial tuning curves for both ERPs and target detections were highly similar. By contrast, late blind participants were significantly more accurate than sighted participants at localizing sounds in the periphery. For both groups, the early N1 amplitude to peripheral standard stimuli displayed no significant spatial tuning. In contrast, the amplitude of the later P3 elicited by targets/deviants displayed a more sharply tuned spatial gradient during peripheral attention in the late blind than in the sighted group. These findings were compared with those of a previous study of congenitally blind individuals in the same task [Röder, B., Teder-Sälejärvi, W., Sterr, A., Rösler, F., Hillyard, S. A., & Neville, H. J. Improved auditory spatial tuning in blind humans. Nature, 400, 162–166, 1999]. It was concluded that both late blind and congenitally blind individuals demonstrate an enhanced capability for focusing auditory attention in the periphery, but they do so via different mechanisms: whereas congenitally blind persons demonstrate a more sharply tuned early attentional filtering, manifested in the N1, late blind individuals show superiority in a later stage of target discrimination and recognition, indexed by the P3.

Auditory Spatial Tuning in Late-onset Blindness in Humans

Blind individuals who lost their sight as older children or adults were compared with normally sighted controls in their ability to focus auditory spatial attention and to localize sounds in a noisy acoustic environment. Event-related potentials (ERPs) were recorded while participants attended to sounds presented in free field from either central or peripheral arrays of speakers with the task of detecting infrequent targets at the attended location. When attending to the central array of speakers, the two groups detected targets equally well, and their spatial tuning curves for both ERPs and target detections were highly similar. By contrast, late blind participants were significantly more accurate than sighted participants at localizing sounds in the periphery. For both groups, the early N1 amplitude to peripheral standard stimuli displayed no significant spatial tuning. In contrast, the amplitude of the later P3 elicited by targets/deviants displayed a more sharply tuned spatial gradient during peripheral attention in the late blind than in the sighted group. These findings were compared with those of a previous study of congenitally blind individuals in the same task [Röder, B., Teder-Sälejärvi, W., Sterr, A., Rösler, F., Hillyard, S. A., & Neville, H. J. Improved auditory spatial tuning in blind humans. Nature, 400, 162-166, 1999]. It was concluded that both late blind and congenitally blind individuals demonstrate an enhanced capability for focusing auditory attention in the periphery, but they do so via different mechanisms: whereas congenitally blind persons demonstrate a more sharply tuned early attentional filtering, manifested in the N1, late blind individuals show superiority in a later stage of target discrimination and recognition, indexed by the P3.

Development of the projection from the nucleus of the brachium of the inferior colliculus to the superior colliculus in the ferret

Neurons in the deeper layers of the superior colliculus (SC) have spatially tuned receptive fields that are arranged to form a map of auditory space. The spatial tuning of these neurons emerges gradually in an experience-dependent manner after the onset of hearing, but the relative contributions of peripheral and central factors in this process of maturation are unknown. We have studied the postnatal development of the projection to the ferret SC from the nucleus of the brachium of the inferior colliculus (nBIC), its main source of auditory input, to determine whether the emergence of auditory map topography can be attributed to anatomical rewiring of this projection. The pattern of retrograde labeling produced by injections of fluorescent microspheres in the SC on postnatal day (P) 0 and just after the age of hearing onset (P29), showed that the nBIC-SC projection is topographically organized in the rostrocaudal axis, along which sound azimuth is represented, from birth. Injections of biotinylated dextran amine-fluorescein into the nBIC at different ages (P30, 60, and 90) labeled axons with numerous terminals and en passant boutons throughout the deeper layers of the SC. This labeling covered the entire mediolateral extent of the SC, but, in keeping with the pattern of retrograde labeling following microsphere injections in the SC, was more restricted rostrocaudally. No systematic changes were observed with age. The stability of the nBIC-SC projection over this period suggests that developmental changes in auditory spatial tuning involve other processes, rather than a gross refinement of the projection from the nBIC.

Robustness of multiplicative processes in auditory spatial tuning.

Auditory space-specific neurons in the owl's inferior colliculus selectively respond to the direction of sound propagation, which is defined by combinations of interaural time (ITD) and level (ILD) differences. Mathematical analyses show that the amplitude of postsynaptic potentials in these neurons is a product of two components that vary with either ITD or ILD. Temporal correlation in the fine structure of signals between the ears is essential for detection of ITD. By varying the degree of binaural correlation, we could accurately change the amplitude of the ITD component of postsynaptic potentials in the space-specific neurons. Multiplication worked for the entire range of postsynaptic potentials created by manipulation of ITD.

Adaptive Axonal Remodeling in the Midbrain Auditory Space Map

The auditory space map in the external nucleus of the inferior colliculus (ICX) of barn owls is highly plastic, especially during early life. When juvenile owls are reared with prismatic spectacles (prisms) that displace the visual field laterally, the auditory spatial tuning of neurons in the ICX adjusts adaptively to match the visual displacement. In the present study, we show that this functional plasticity is accompanied by axonal remodeling. The ICX receives auditory input from the central nucleus of the inferior colliculus (ICC) via topographic axonal projections. We used the anterograde tracer biocytin to study experience-dependent changes in the spatial pattern of axons projecting from the ICC to the ICX. The projection fields in normal adults were sparser and more restricted than those in normal juveniles. The projection fields in prism-reared adults were denser and broader than those in normal adults and contained substantially more bouton-laden axons that were appropriately positioned in the ICX to convey adaptive auditory spatial information. Quantitative comparison of results from juvenile and prism-reared owls indicated that prism experience led to topographically appropriate axonal sprouting and synaptogenesis. We conclude that this elaboration of axons represents the formation of an adaptive neuronal circuit. The density of axons and boutons in the normal projection zone was preserved in prism-reared owls. The coexistence of two different circuits encoding alternative maps of space may underlie the ability of prism-reared owls to readapt to normal conditions as adults.

Neuroperception. Superior auditory spatial tuning in conductors.

Conducting a large orchestra is an impressive feat that simultaneously requires the intake of the whole musical gestalt and the analytical decomposition of the orchestral sound into its components1. How, for example, does a conductor identify a specific musician within a multiplayer section? Here we provide evidence from brain-potential recordings that experienced professional conductors develop enhanced auditory localization mechanisms in peripheral space.

Plasticity in the neural coding of auditory space in the mammalian brain.

Sound localization relies on the neural processing of monaural and binaural spatial cues that arise from the way sounds interact with the head and external ears. Neurophysiological studies of animals raised with abnormal sensory inputs show that the map of auditory space in the superior colliculus is shaped during development by both auditory and visual experience. An example of this plasticity is provided by monaural occlusion during infancy, which leads to compensatory changes in auditory spatial tuning that tend to preserve the alignment between the neural representations of visual and auditory space. Adaptive changes also take place in sound localization behavior, as demonstrated by the fact that ferrets raised and tested with one ear plugged learn to localize as accurately as control animals. In both cases, these adjustments may involve greater use of monaural spectral cues provided by the other ear. Although plasticity in the auditory space map seems to be restricted to development, adult ferrets show some recovery of sound localization behavior after long-term monaural occlusion. The capacity for behavioral adaptation is, however, task dependent, because auditory spatial acuity and binaural unmasking (a measure of the spatial contribution to the "cocktail party effect") are permanently impaired by chronically plugging one ear, both in infancy but especially in adulthood. Experience-induced plasticity allows the neural circuitry underlying sound localization to be customized to individual characteristics, such as the size and shape of the head and ears, and to compensate for natural conductive hearing losses, including those associated with middle ear disease in infancy.

Abnormal Auditory Experience Induces Frequency-Specific Adjustments in Unit Tuning for Binaural Localization Cues in the Optic Tectum of Juvenile Owls

Early auditory experience shapes the auditory spatial tuning of neurons in the barn owl's optic tectum in a frequency-dependent manner. We examined the basis for this adaptive plasticity in terms of changes in tuning for frequency-specific interaural time differences (ITDs) and level differences (ILDs), the dominant sound localization cues. We characterized broadband and narrowband ITD and ILD tuning in normal owls and in owls raised with an acoustic filtering device in one ear that caused frequency-dependent changes in sound timing and level. In normal owls, units were tuned to frequency-specific ITD and ILD values that matched those produced by sound sources located in their visual receptive fields. In contrast, in device-reared owls, ITD tuning at most sites was shifted from normal by approximately 55 microsec toward open-ear leading for 4 kHz stimuli and 15 microsec toward the opposite-ear leading for 8 kHz stimuli, reflecting the acoustic effects of the device. ILD tuning was shifted in the adaptive direction by approximately 3 dB for 4 kHz stimuli and 8 dB for 8 kHz stimuli, but these shifts were substantially smaller than expected based on the acoustic effects of the device. Most sites also exhibited conspicuously abnormal frequency-response functions, including a strong dependence on stimulus ITD and a reduction of normally robust responses to 6 kHz stimuli. The results demonstrate that the response properties of high-order auditory neurons in the optic tectum are adjusted during development to reflect the influence of frequency-specific features of the binaural localization cues experienced by the individual.

Hearing impairment induces frequency-specific adjustments in auditory spatial tuning in the optic tectum of young owls.

Bimodal, auditory-visual neurons in the optic tectum of the barn owl are sharply tuned for sound source location. The auditory receptive fields (RFs) of these neurons are restricted in space primarily as a consequence of their tuning for interaural time differences and interaural level differences across broad ranges of frequencies. In this study, we examined the extent to which frequency-specific features of early auditory experience shape the auditory spatial tuning of these neurons. We manipulated auditory experience by implanting in one ear canal an acoustic filtering device that altered the timing and level of sound reaching the eardrum in a frequency-dependent fashion. We assessed the auditory spatial tuning at individual tectal sites in normal owls and in owls raised with the filtering device. At each site, we measured a family of auditory RFs using broadband sound and narrowband sounds with different center frequencies both with and without the device in place. In normal owls, the narrowband RFs for a given site all included a common region of space that corresponded with the broadband RF and aligned with the site's visual RF. Acute insertion of the filtering device in normal owls shifted the locations of the narrowband RFs away from the visual RF, the magnitude and direction of the shifts depending on the frequency of the stimulus. In contrast, in owls that were raised wearing the device, narrowband and broadband RFs were aligned with visual RFs so long as the device was in the ear but not after it was removed, indicating that auditory spatial tuning had been adaptively altered by experience with the device. The frequency tuning of tectal neurons in device-reared owls was also altered from normal. The results demonstrate that experience during development adaptively modifies the representation of auditory space in the barn owl's optic tectum in a frequency-dependent manner.

Tuned in when out of sight

It has been reported previously that blind humans show improved auditory discrimination, as if to compensate for the sensory lack in the visual modality (e.g. 1 Lessard N. et al. Early-blind human subjects localize sound sources better than sighted subjects. Nature. 1998; 395: 278-280 Crossref PubMed Scopus (478) Google Scholar ). However, it is unclear how this sensory enhancement relates to altered cortical activation patterns found in these blind individuals. A recent study by Röder et al. makes an important contribution to the investigation of this phenomenon by comparing behavioural and electrophysiological measures of auditory spatial tuning in congenitally blind individuals and normally sighted but blindfolded control subjects 2 Röder B. et al. Improved auditory spatial tuning in blind humans. Nature. 1999; 400: 162-166 Crossref PubMed Scopus (510) Google Scholar . In an attentional paradigm, brief noise bursts were presented in random sequence with equal probability from one of four central and four peripheral speakers. Subjects were instructed to attend either to a central or to a peripheral loudspeaker and to detect infrequent higher-pitched sounds when they came from the target speaker, but to ignore sounds from all other speakers. The results showed that the blind subjects had better localization abilities than those of the control subjects, but only when they attended to peripheral auditory space. ERP recordings measured at the same time revealed sharper tuning curves for the component of the ERP related to early spatial attention in the blind subjects, and differences in the scalp topography of the ERP responses strongly suggest that there is a reorganization of the neural substrates for early auditory processing in the congenitally blind. This study adds support to the notion that when the brain is faced with the loss of one sensory modality, it reacts with compensatory changes in the remaining modalities.

Improved auditory spatial tuning in blind humans.

Despite reports of improved auditory discrimination capabilities in blind humans and visually deprived animals, there is no general agreement as to the nature or pervasiveness of such compensatory sensory enhancements. Neuroimaging studies have pointed out differences in cerebral organization between blind and sighted humans, but the relationship between these altered cortical activation patterns and auditory sensory acuity remains unclear. Here we compare behavioural and electrophysiological indices of spatial tuning within central and peripheral auditory space in congenitally blind and normally sighted but blindfolded adults to test the hypothesis (raised by earlier studies of the effects of auditory deprivation on visual processing) that the effects of visual deprivation might be more pronounced for processing peripheral sounds. We find that blind participants displayed localization abilities that were superior to those of sighted controls, but only when attending to sounds in peripheral auditory space. Electrophysiological recordings obtained at the same time revealed sharper tuning of early spatial attention mechanisms in the blind subjects. Differences in the scalp distribution of brain electrical activity between the two groups suggest a compensatory reorganization of brain areas in the blind that may contribute to the improved spatial resolution for peripheral sound sources.

Chapter 24 The development of topographically-aligned maps of visual and auditory space in the superior colliculus

The role of the superior colliculus in attending and orienting to sensory stimuli is facilitated by the presence within this midbrain nucleus of superimposed maps of different sensory modalities. We have studied the steps involved in the development of topographically-aligned maps of visual and auditory space in the ferret superior colliculus. Injections of fluorescent beads into the superficial layers showed that the projection from the contralateral retina displays topographic order on the day of birth (PO). Recordings made from these layers at the time of eye opening, approximately 1 month later, revealed the presence of an adult-like map of visual space. In contrast, the auditory space map in the deeper layers emerged gradually over a much longer period of postnatal life. In adult ferrets in which one eye had been deviated laterally just before eye opening, the auditory spatial tuning of single units recorded in the contralateral superior colliculus was shifted by a corresponding amount, so that the registration of the visual and auditory maps was maintained. Chronic application of the NMDA-receptor antagonist MK801 disrupted the normal development of the auditory space map, but had no effect on the visual map in either juvenile or adult animals, or on the auditory map once it had matured. These findings indicate that visual cues may play an instructive role, possibly via a Hebbian mechanism of synaptic plasticity, in the development of appropriately tuned auditory responses, thereby ensuring that the neural representations of both modalities share the same coordinates. Changes observed in the auditory representation following partial lesions of the superficial layers at PO suggest that these layers may provide the source of the visual signals responsible for experience-induced plasticity in auditory spatial tuning.

Neural substrates of sound localization

Recent behavioral experiments suggest that parallel pathways in the forebrain and midbrain are capable of mediating sound localization. Neurophysiological studies have advanced our understanding of how binaural and monaural localization cues contribute to the representations of auditory space within these pathways. Experience-dependent modifications of auditory spatial tuning in both the forebrain and midbrain pathways indicate that sensory input during development customizes an individual's neural processing of spatial information.

Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl

The optic tectum (homolog of the superior colliculus) contains mutually aligned neural maps of auditory and visual space. During development, the organization of the auditory map is guided by spatial information provided by vision: barn owls raised wearing prismatic spectacles, which optically shift the visual field and the visual map in the optic tectum, develop an auditory map that is shifted by an approximately equivalent amount, such that alignment between the two maps is preserved (Knudsen and Brainard, 1991). In this study we investigated whether this shift in the auditory map is intrinsic to the optic tectum or whether it reflects plasticity at an earlier stage in the auditory pathway. Owls were raised wearing prismatic spectacles that displaced the visual field by 23 degrees to the left or right. This manipulation alters the normal correspondence between locations in the visual field and interaural time difference (ITD), the primary cue for the azimuth of a sound source. In normal owls and in owls with at least 150 d of prism experience, extracellular unit recordings were used to assess the representations of ITD at anatomically and physiologically defined sites in the optic tectum and in the two prior stages of the auditory pathway, the external and central nuclei of the inferior colliculus (ICx and ICc). In the optic tectum of normal owls, the values of ITD to which units responded most strongly (best ITDs) varied systematically with the azimuths of unit visual receptive fields (VRFs). In the prism-reared owls, best ITDs were shifted from normal toward the values of ITD produced by sounds at the locations of the units' optically displaced VRFs. In the ICx of prism-reared owls, the representation of ITD also was shifted from normal, by an amount and in a direction that could completely account for the shift in ITD measured in the optic tectum. At some sites in the ICx, the shift in ITD tuning was apparent within the first 7-8 msec of the response; shifted tuning at such short latencies argues that the altered representation of ITD in the ICx reflects plasticity in the ascending auditory pathway, and is not the result of descending activity from higher auditory centers. In the ICc, which immediately precedes the ICx in the ascending pathway, the representation of ITD was normal. The results indicate that the visual instruction of auditory spatial tuning of neurons in the optic tectum reflects plasticity at the level of the ICx, the site where the auditory map of space is first synthesized.

Auditory spatial tuning of cortical neurons is sharpened in cats with early blindness

1. The specificity for the location of a sound source in azimuth was measured in single neurons of the anterior ectosylvian (AE) region of the cat's cortex, which includes the anterior auditory field (AAF) and the anterior ectosylvian auditory field (AEA). 2. The influence of visual experience on auditory spatial tuning of these neurons was determined by comparing responses in cats with binocular deprivation from birth with those in normal control cats. 3. Spatial tuning was measured under near free-field conditions by presenting broadband sounds through a speaker in seven different azimuthal locations, from -60 to +60 degree at 20 degree intervals. Elevation was constant at the cats' ears. 4. In normal cats, a little over one-half of the neurons in the AE region (82/146 = 56%) showed some degree of azimuthal spatial tuning, as defined by at least a 2:1 ratio of responses between best and worst location. The rest (44%) were omnidirectional. 5. In binocularly deprived cats, a significantly higher proportion (70/82 = 86%) of the neurons in the AE region were spatially tuned. Only 14% were omnidirectional. Median spatial tuning width was significantly sharper than in normal cats. 6. We conclude that visual deprivation from birth induces intermodal changes that enhance the response specificity of neurons in the auditory cortex. These modifications may constitute the neural basis of behavioral compensation for early blindness.

A topographic representation of auditory space in the external nucleus of the inferior colliculus of the guinea-pig

The possibility that the external nucleus of the inferior colliculus (ICX) of the pigmented guinea-pig contains a map of auditory space has been investigated. Auditory stimuli consisted of broad-band sound delivered under free-field anechoic conditions from a range of positions around the animal's azimuthal axis. The responses of clusters of neurons in the ICX to threshold and to near-threshold stimuli displayed sharp spatial tuning. The responses recorded from rostral ICX revealed a preference for auditory stimuli in the anterior field while more caudal neurons preferentially responded to sounds presented in the posterior field. Neurons at intermediate points, along the rostro-caudal axis of the nucleus, displayed preferences for sound stimuli in appropriately intermediate field positions along the contralateral azimuthal axis. At higher stimulus intensities the spatial tuning of the responses decreased, but the optimal direction of preference was usually retained. The contribution of binaural processing to auditory spatial tuning was evident, since unilateral cochlea ablation destroyed the spatial tuning at higher stimulus intensities. The results presented provide the first evidence that a topographically ordered representation of the contralateral auditory azimuth is present in the ICX of a mammal.

Visual Instruction of the Neural Map of Auditory Space in the Developing Optic Tectum

Neural maps of visual and auditory space are aligned in the adult optic tectum. In barn owls, this alignment of sensory maps was found to be controlled during ontogeny by visual instruction of the auditory spatial tuning of neurons. Large adaptive changes in auditory spatial tuning were induced by raising owls with displacing prisms mounted in spectacle frames in front of the eyes; neurons became tuned to sound source locations corresponding to their optically displaced, rather than their normal, visual receptive field locations. The results demonstrate that visual experience during development calibrates the tectal auditory space map in a site-specific manner, dictating its topography and alignment with the visual space map.