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Neural substrates of sound localization
Neural substrates of sound localization Michael Stanford University
Recent
behavioral
forebrain
and
Neurophysiological and monaural
School of Medicine,
experiments
midbrain
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cues contribute
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Current Opinion
in Neurobiology
Introduction Sound localization is a complex computational task. The location of a sound source is not represented directly in the cochlea. Instead, it must be derived centrally from the signals arriving at both ears. The features of these signals that vary with the location of a source provide the cues for sound localization (for a recent review, see [l]); these include the relative times of arrival of signals at both ears (interaural time difference), the relative levels (or intensities) of the signals at both ears (interaural level difference), and the spectrum of the signal received at each ear. To localize a sound, the nervous system must first encode the localization cues produced by the sound, and then correctly associate those cues with the spatial location of the sound source. This review focuses on recent advances in our understanding of, first, the contribution of forebrain and midbrain pathways to the interpretation of sound localization cues and the execution of sound localization behaviors, second, the processing of localization cues within these pathways that generate spatially tuned auditory neurons and, third, the influence of experience on the representation of auditory space within these pathways.
Pathways mediating
sound localization
behavior
Assessment of sound localization
The involvement of specific brain regions in sound localization has been extensively investigated by measuring behavioral deficits caused by selective lesions [2,3]. The interpretation of lesion studies is complicated because the severity of localization deficits depends strongly on
1994,
4~557-562
both the sensory processing and the behavioral response that is required of the animal. Deficits tend to be most severe in paradigms that require localization of a sound presented from one of many possible source locations. In contrast, if animals are tested with only two possible source locations, performance may be normal, even after extensive lesions [3,4-l. In this case, animals may perform the task by learning to recognize differences in the spectrum, intensity or reverberation of the sounds produced by the two speakers without actually localizing them. In the studies described below, sounds were presented from multiple locations, minimizing the possibility that animals could employ a strategy of sound recognition rather than sound localization.
Contributions of forebrain and midbrain to localization
In several studies, unilateral lesions of auditory cortex and other forebrain regions have been shown to cause sound localization deficits restricted primarily to the contralateral hemifield (see [3] for review). Complex localization behavior, such as moving towards the location from which a sound was briefly presented, is typically eliminated by cortical lesions (although there is some variability across species) [2,3]. In contrast, the orientation of the head and eyes towards the location of a sound source may be preserved, even after extensive bilateral cortical lesions [5-l. These results suggest that subcortical mechanisms are capable of computing sound source location and subserving orienting responses (e.g. redirection of gaze), but that forebrain regions are required for complex localization behaviors. Recent studies have demonstrated that in the barn owl, separate pathways in the forebrain and midbrain contribute in parallel to sound localization [6**,7**] (Fig. 1).
Abbreviations CABA--y-aminobutyric
acid; K-inferior colliculus; Kx-external nucleus of the IC; ILD-interaural ITD-interaural time difference; OT--optic tectum; SC-superior colliculus; VLVp-posterior subdivision of the nucleus ventralis lemnisci lateralis. 0 Current Biology Ltd ISSN 0959-4388
level difference;
557
Sensory systems
Following unilateral lesion or pharmacological inactivation of the forebrain pathway at the level of the auditory thalamus, owls are still capable of orienting their gaze accurately towards the location of sound sources [6**,7*“]. However, when the optic tectum (OT; superior colhculus in mammals) on the same side of the brain is also inactivated, owls can no longer orient their gaze towards contralateral sound sources, though they can still hear and shift their gaze [7**]. Unilateral inactivation of the midbrain pathway alone at the level of either the external nucleus of the inferior colliculus (ICx) [6**] or OT [7**], reduces the probability of orienting responses but does not eliminate them. These findings demonstrate that either pathway alone is capable of subserving orientation of gaze towards sound sources. The midbrain pathway contains neurons tuned for the location of sound sources and a mapped representation of auditory space that first appears at the level of the ICx [8]. The finding that the capacity for sound localization can persist after lesioning the ICx [6**], therefore, further suggests that the forebrain and midbrain pathways can independently compute representations of sound source location.
Neural
representation
of sound location
Within the lower brainstem, parallel pathways generate neurons that are sensitive to individual localization cues, such as the interaural time difference (ITD) or the interaural level difference (ILD), within a narrow range of frequencies (for recent reviews, see [S,S,lO*]). These neurons are typically responsive to sounds from broad or multiple regions of space, because the information provided by individual localization cues does not uniquely specify the location of a sound source [l,ll]. Within
both the forebrain and midbrain localization pathways, however, some neurons respond selectively to sounds from a restricted region ofspace [3,8,12*]. These spatially tuned neurons derive from the refinement of tuning for individual localization cues and from the combination of information both across different frequencies and across different types of cues. Recent experiments, described below, have advanced our understanding of these processes.
Refinement of ILD tuning in the inferior colliculus
Significant processing of auditory spatial information occurs within the inferior colliculus (IC). GABAergic inhibition within the IC has previously been shown to sharpen neural tuning for ITDs and to help eliminate the phase ambiguity of narrow band sounds [13,14]. Recent experiments suggest that GABAergic inhibition similarly refines tuning for ILDs within the IC. The majority of ILD-sensitive neurons in the IC are excited by sounds at the contralateral ear and inhibited by sounds at the ipsilateral ear. In addition, some IC neurons respond poorly to monaural stimuli at either ear and instead are tuned to specific intermediate values of ILD. In both the barn owl [15**] and the bat [lo’], iontophoresis of the GABAA inhibitor bicuculline into the IC generally reduced inhibition from both ipsilateral and contralateral ears, so that ILD tuning broadened and some neurons became completely insensitive to ILD. In the barn owl, much of the inhibition responsible for sharpening the ILD tuning of neurons in the IC derives from projections arising in the posterior subdivision of the nucleus ventralis lemnisci lateralis (VLVp) [ 15**]. Experiments in which activity in the VLVp was pharmacologically manipulated while recording ILD sensitivity
Fig. 1.
Forebrain
for sound tory
and midbrain
localization.
nuclei
pathways
Brainstem
that process
audi-
both monaural
and binaural signals project in parallel to Complex
localization
the central nucleus of the inferior
collicu-
lus (ICC). The classical ascending auditory pathway continues from the ICC to the auditory thalamus and then to the forebrain. The midbrain Orientation
Forebrain
of gaze
classical
and involves ternal
pathway branches from the
pathway at the level of the ICC a projection
nucleus
first to the ex-
of the inferior
colliculus
(ICx) and then to the optic rectum (OT). Spatially
tuned auditory
map of auditory in the OT midbrain
vviv
neurons
space are found
and ICx.
The
forebrain
pathways are reciprocally
and a both and inter-
connected by direct and indirect connec-
pathway
tions (gray arrows). Both pathways can in-
Auditory
dependently compute sound source loca-
brainstem
tion and direct orientation
of gaze. How-
ever, in some species at least, the fore-
nuclei
brain pathway is required for more com0 1994 Current Op~mon in Neurobiology
plex behaviors,
such as movement to the
location of a sound source.
Neural substrates of sound localization Brainard
in the IC suggest that the VLVp contralateral to the IC provides inhibition from the ipsilateral ear, whereas the VLVp ipsilateral to the IC provides inhibition from the contralateral ear [15**]. An analogous source of inhibition in mammals is the dorsal nucleus of the lateral lemniscus, which, like the VLVp [ 171, contains ipsilateral ear neurons, sends a bilateral GABAergic projection to the IC and contributes to acoustically evoked inhibition in the contralateral IC [18*,19].
Neural tuning for monaural spectral cues
In the mammalian superior colliculus (SC) and ICx, most spatially tuned neurons maintain their selectivity for azimuthal sound source location after monaural occlusion or cochlear ablation [20,21*,22]. Unlike the case for binaural hearing, this selectivity is maintained only for near-threshold sound levels and is lost as the sound level is increased. Two separate mechanisms potentially contribute to this type of spatial tuning in the absence of binaural cues. First, the external ear maximally amplifies sounds from a restricted region of space, the location of which varies with frequency. Consequently, low-level stimuli may elicit responses only from within the region of maximum amplification, whereas high-level stimuli are above threshold for all locations. The azimuthal sensitivity of some neurons in the IC [23] and auditory nerve [24*] can be explained by the direction-dependent amplification by the ear at the frequencies to which the neurons are most responsive. Second, the shape of the spectrum that results from the filtering of broadband sounds by the external ear (monaural spectrum) varies with the location of the source but does not depend on the level of the sound [l] _Hence, neurons can potentially develop spatial tuning by integrating information across ti-equencies in order to respond to appropriate monaural spectra. The most persuasive evidence that monaural spatial tuning in the SC utilizes spectral cues is the finding that some neurons are tuned to locations that do not appear to correspond with locations from which sounds are maximally amplified by the external ears [21’,25*]. Evidence for utilization of monaural spectral cues in the SC could be further strengthened by a careful demonstration that spatial tuning cannot be explained by the combination of ear directionality and frequency tuning, and that spatial selectivity under monaural conditions requires broadband stimuli. Spatial tuning that remains substantially unchanged after disruption of binaural cues (by plugging one ear) also has been demonstrated for some neurons in cat primary auditory cortex [26**]. For many of these neurons, unlike those in the SC, monaurally characterized receptive field sizes do not expand with increasing sound levels. Indeed, responses to sounds from all locations are often inhibited for high sound levels, as is the case for many binaurally characterized ILD-sensitive neurons [27’,28*]. Furthermore, these neurons are not spatially tuned for tonal stimuli. These findings strongly indicate that the
spatial tuning of some cortical neurons derives in part horn their selectivity for monaural spectral cues. In both the cortex and the SC, most of the neurons that are tuned under monaural conditions are also sensitive to binaural cues [21*,22,25’,26”]. Moreover, it appears that tuning for any one cue may help eliminate ambiguities associated with other cues. For example, some cortical neurons under monaural conditions have discrete receptive fields in both ipsilateral and contralateral space. Under binaural conditions, inhibition may eliminate responses to sounds in ipsilateral space, leaving a single restricted receptive field [26*.]. Such integration of information across different localization cues is required to eliminate ambiguities associated with individual cues
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Plasticity of auditory
spatial representations
The correspondences between sound localization cues and spatial locations depend on the geometry of the head and external ears. Because these features change over the course of development and vary between individuals, the developing nervous system can anticipate only approximately the values of auditory cues that will be produced by sounds at particular spatial locations. Earlier studies have demonstrated that both sound localization behavior and the neurophysiological representation of auditory space are customized according to the experience of the individual [12*,29]. Recent experiments have focused on the influence of visual experience on the representation of auditory space in both the forebrain and midbrain.
Visual deprivation
Two competing hypotheses are currently being explored regarding the influence of visual deprivation during development on sound localization. The ‘sensory compensation’ hypothesis suggests that increased reliance on audition in visually deprived animals should result in enhanced sound localization capabilities. The ‘visual calibration’ hypothesis suggests that spatial information provided by vision is required to learn the values of localization cues associated with locations in space, and that visual deprivation should degrade sound localization behavior and the neural representation of auditory space. Both hypotheses have received support from recent studies. In cats reared with closed eyes (binocular eyelid suture), the amount of anterior ectosylvian cortex devoted to the representation of auditory information is expanded at the expense of adjacent areas normally representing visual information [3000]. Furthermore, the auditory spatial tuning of neurons in the expanded forebrain representation is sharper than in normal cats [31.*]. The increased representation of auditory information in the forebrain parallels the earlier finding in cats reared with closed eyes of an increased percentage of auditory neurons in the SC
559
560
Sensory systems
and the significant presence of auditory normally visual superficial layers [32].
responses
in the
In contrast to these findings, rearing ferrets with closed eyes does not appreciably alter the laminar distribution of auditory responsive neurons in the SC [33*]. Moreover, although the sharpness of tuning for sound source location is normal, the systematic progression of receptive field locations across the SC is somewhat degraded, as has previously been observed in both guinea pigs and barn owls reared with closed eyes [34,35]. Representation of sound source location requires both tuning for localization cues and accurate association of cues with spatial locations. Differential dependence of these two processes on visual experience may partially reconcile the various experimental findings. Sharpness of tuning may be largely unaffected (in SC) or sharpened (in anterior ectosylvian cortex) in visually deprived animals. Cues may be inaccurately associated with spatial locations, however, as suggested by the degraded maps of auditory space in the SC of lid-sutured animals. No comparable assessment is possible in the forebrain, because no systematic forebrain representation of auditory space has yet been found. Alternatively, the seemingly different results of visual deprivation may reflect differences between species, conditions under which animals were reared, or the brain regions examined. In this light, it would be interesting to determine whether rearing cats with closed eyes results in sharpened tuning for spatial location in the SC, as suggested by the finding of sharpened auditory tuning in the forebrain, as well as a degraded auditory space map, consistent with findings in the SC of other species [33*,34,35].
Visual guidance of spatial tuning
Experiments in barn owls have demonstrated that spatial information provided by vision can actively guide the associations of sound localization cues with spatial locations [36,37**]. The OT of normal owls contains mutually aligned maps of auditory and visual space [S]. The azimuthal alignment of these maps reflects the tuning of tectal neurons to the values of ITD produced by sources at the locations of their visual receptive fields [38]. In owls reared wearing prismatic spectacles that optically shift the visual field along the horizon, neurons become tuned to abnormal values of ITD associated with their optically displaced visual receptive fields [37”]. Hence, vision provides a signal that actively guides the topography of the auditory map in the tectum. The visually guided changes in the tectal representation of auditory space can be accounted for by plasticity in the ICx [37**]. This is the first site in the midbrain sound localization pathway of owls [8], and at least some mammalian species [20], where a mapped representation of auditory space appears, suggesting that spatial information provided by vision alters only that portion of the
pathway specifically concerned with of auditory cues in a spatial context.
the interpretation
Adult plasticity
Earlier studies have found that sound localization becomes refractory to experience-dependent modification after certain ‘sensitive periods’ during early life [12*,29]. For example, young owls can adaptively adjust both the neural map of auditory space in the OT and sound localization behavior in response to the abnormal localization cues caused by monaural occlusion, whereas adult owls can not [39]. A recent study has found, however, that significant adaptive adjustments occur in the tectal auditory space map of adult owls following alteration of localization cues by modification of the external ears [40**]. The alterations of sound localization cues, particularly ITDs, by ear modification are less severe than those due to monaural occlusion [40**]. This suggests that while plasticity may be reduced in adult animals, the capacity to adapt to small changes in localization cues is retained. This capacity is appropriate to the demands on the adult nervous system, which normally will experience only small changes in the correspondences between localization cues and sound source locations.
Conclusions Parallel auditory pathways in the forebrain and midbrain can independently compute sound source location and execute localization behaviors. However, significant differences exist between the capabilities and organization of these pathways. Although either pathway can subserve orientation of gaze towards sound sources, in most species the forebrain pathway appears to be critical for creating a representation that can be used for more complex and perhaps ‘cognitive’ responses. The nature of this forebrain representation remains an important and unanswered question: although individual forebrain neurons are tuned for the spatial location of auditory stimuli, no mapped representation like that in the midbrain pathway has been found. Nevertheless, both pathways must ultimately establish representations based on the neural encoding of monaural and binaural localization cues, and the correct associations of these cues with spatial locations. These processes are significantly shaped by experience, which customizes sound localization mechanisms for the individual.
Acknowledgements I thank DE Feldman, JI Gold and EI Knudsen for helpful discussions and comments on the manuscript. This work was supported in part by NIH grant ROl-DC00155 to EI Knudsen.
Neural
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Brainard MS, Knudsen El: Experience-Dependent Plasticity in the Inferior Colliculus: a Site for Visual Calibration of the Neural Representation of Auditory Space in the Barn Owl. / Neurosci 1993, 13:4589-46@8. In the OT of owls reared with prismatic spectacles that displace the visual field, bimodal neurons become tuned to the values of sound localization cues that correspond with their optically displaced visual receptive fields. The visually guided changes in the auditory space map of the OT can be accounted for by plasticity in the ICx. These results indicate that spatial information provided by vision can dictate the topography of the auditory spatial representation in the midbrain and identify a site where this experience-dependent plasticity operates.
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30. ..
Rauschecker JP, Korte M: Auditory Compensation for Early Blindness in Cat Cerebral Cortex. / Neurosci 1993, 13:4538-4548. Visual, auditory and somatosensory responses were characterized for neurons in the anterior ectosylvian cortex of normal cats and cats reared with binocular eyelid suture. Each modality is normally represented in a separate region of anterior ectosylvian cortex. In lid-sutured cats, auditory and somatosensory representations were expanded at the expense of the visual representation. This study and I31**1 provide the best evidence for compensatory improvements in the processing of auditory spatial information following visual deprivation. 31. ..
Korte M, Rauschecker JP: Auditory Spatial Tuning of Cortical Neurons is Sharpened in Cats wi-:h Early Blindness. 1 Neurophysio/ 1993, 70: 1717-l 721. Azimuthal spatial tuning was measured for neurons in the anterior ectosylvian cortex of normal cats and cats reared with binocular lid suture. Spatial tuning was significantly sharper for neurons in lid-sutured cats than in normals.
40. ..
Knudsen El, Esterly SD, Olsen JF: Adaptive Plasticity of the Auditory Space Map in the Optic Tectum of Adult and Baby Barn Owls in Response to External Ear Modification. / Neurophysiol 1994, 71:79-94. The representation of auditory space in the OT was characterized in adult and baby barn owls that had been chronically exposed to abnormal localization cues by removal of the facial ruff and preaural flaps that comprise the external ear. In baby and adult owls, the neural maps of both ITD and ILD were adaptively adjusted so as to partially restore the normal topography of the auditory space map. The results demonstrate that significant plasticity in the neural representation of auditory space persists in adult animals.
MS
Brainard,
School
Department
of Medicine,
of Neurobiology,
Stanford,
California
Stanford 94305-5401,
University USA.
Recent
behavioral
forebrain
and
Neurophysiological and monaural
School of Medicine,
experiments
midbrain
are
that
tuning
sensory
in input
suggest capable
studies have advanced
localization
cues contribute
space within these pathways. spatial
S Brainard
both
parallel
mediating
forebrain
development
customizes
the
of auditory
modifications
midbrain
in
localization.
of how binaural
to the representations and
USA
pathways sound
our understanding
Experience-dependent
the
during
that
of
Stanford,
of auditory
pathways
an individual’s
indicate neural
processing of spatial information.
Current Opinion
in Neurobiology
Introduction Sound localization is a complex computational task. The location of a sound source is not represented directly in the cochlea. Instead, it must be derived centrally from the signals arriving at both ears. The features of these signals that vary with the location of a source provide the cues for sound localization (for a recent review, see [l]); these include the relative times of arrival of signals at both ears (interaural time difference), the relative levels (or intensities) of the signals at both ears (interaural level difference), and the spectrum of the signal received at each ear. To localize a sound, the nervous system must first encode the localization cues produced by the sound, and then correctly associate those cues with the spatial location of the sound source. This review focuses on recent advances in our understanding of, first, the contribution of forebrain and midbrain pathways to the interpretation of sound localization cues and the execution of sound localization behaviors, second, the processing of localization cues within these pathways that generate spatially tuned auditory neurons and, third, the influence of experience on the representation of auditory space within these pathways.
Pathways mediating
sound localization
behavior
Assessment of sound localization
The involvement of specific brain regions in sound localization has been extensively investigated by measuring behavioral deficits caused by selective lesions [2,3]. The interpretation of lesion studies is complicated because the severity of localization deficits depends strongly on
1994,
4~557-562
both the sensory processing and the behavioral response that is required of the animal. Deficits tend to be most severe in paradigms that require localization of a sound presented from one of many possible source locations. In contrast, if animals are tested with only two possible source locations, performance may be normal, even after extensive lesions [3,4-l. In this case, animals may perform the task by learning to recognize differences in the spectrum, intensity or reverberation of the sounds produced by the two speakers without actually localizing them. In the studies described below, sounds were presented from multiple locations, minimizing the possibility that animals could employ a strategy of sound recognition rather than sound localization.
Contributions of forebrain and midbrain to localization
In several studies, unilateral lesions of auditory cortex and other forebrain regions have been shown to cause sound localization deficits restricted primarily to the contralateral hemifield (see [3] for review). Complex localization behavior, such as moving towards the location from which a sound was briefly presented, is typically eliminated by cortical lesions (although there is some variability across species) [2,3]. In contrast, the orientation of the head and eyes towards the location of a sound source may be preserved, even after extensive bilateral cortical lesions [5-l. These results suggest that subcortical mechanisms are capable of computing sound source location and subserving orienting responses (e.g. redirection of gaze), but that forebrain regions are required for complex localization behaviors. Recent studies have demonstrated that in the barn owl, separate pathways in the forebrain and midbrain contribute in parallel to sound localization [6**,7**] (Fig. 1).
Abbreviations CABA--y-aminobutyric
acid; K-inferior colliculus; Kx-external nucleus of the IC; ILD-interaural ITD-interaural time difference; OT--optic tectum; SC-superior colliculus; VLVp-posterior subdivision of the nucleus ventralis lemnisci lateralis. 0 Current Biology Ltd ISSN 0959-4388
level difference;
557
Sensory systems
Following unilateral lesion or pharmacological inactivation of the forebrain pathway at the level of the auditory thalamus, owls are still capable of orienting their gaze accurately towards the location of sound sources [6**,7*“]. However, when the optic tectum (OT; superior colhculus in mammals) on the same side of the brain is also inactivated, owls can no longer orient their gaze towards contralateral sound sources, though they can still hear and shift their gaze [7**]. Unilateral inactivation of the midbrain pathway alone at the level of either the external nucleus of the inferior colliculus (ICx) [6**] or OT [7**], reduces the probability of orienting responses but does not eliminate them. These findings demonstrate that either pathway alone is capable of subserving orientation of gaze towards sound sources. The midbrain pathway contains neurons tuned for the location of sound sources and a mapped representation of auditory space that first appears at the level of the ICx [8]. The finding that the capacity for sound localization can persist after lesioning the ICx [6**], therefore, further suggests that the forebrain and midbrain pathways can independently compute representations of sound source location.
Neural
representation
of sound location
Within the lower brainstem, parallel pathways generate neurons that are sensitive to individual localization cues, such as the interaural time difference (ITD) or the interaural level difference (ILD), within a narrow range of frequencies (for recent reviews, see [S,S,lO*]). These neurons are typically responsive to sounds from broad or multiple regions of space, because the information provided by individual localization cues does not uniquely specify the location of a sound source [l,ll]. Within
both the forebrain and midbrain localization pathways, however, some neurons respond selectively to sounds from a restricted region ofspace [3,8,12*]. These spatially tuned neurons derive from the refinement of tuning for individual localization cues and from the combination of information both across different frequencies and across different types of cues. Recent experiments, described below, have advanced our understanding of these processes.
Refinement of ILD tuning in the inferior colliculus
Significant processing of auditory spatial information occurs within the inferior colliculus (IC). GABAergic inhibition within the IC has previously been shown to sharpen neural tuning for ITDs and to help eliminate the phase ambiguity of narrow band sounds [13,14]. Recent experiments suggest that GABAergic inhibition similarly refines tuning for ILDs within the IC. The majority of ILD-sensitive neurons in the IC are excited by sounds at the contralateral ear and inhibited by sounds at the ipsilateral ear. In addition, some IC neurons respond poorly to monaural stimuli at either ear and instead are tuned to specific intermediate values of ILD. In both the barn owl [15**] and the bat [lo’], iontophoresis of the GABAA inhibitor bicuculline into the IC generally reduced inhibition from both ipsilateral and contralateral ears, so that ILD tuning broadened and some neurons became completely insensitive to ILD. In the barn owl, much of the inhibition responsible for sharpening the ILD tuning of neurons in the IC derives from projections arising in the posterior subdivision of the nucleus ventralis lemnisci lateralis (VLVp) [ 15**]. Experiments in which activity in the VLVp was pharmacologically manipulated while recording ILD sensitivity
Fig. 1.
Forebrain
for sound tory
and midbrain
localization.
nuclei
pathways
Brainstem
that process
audi-
both monaural
and binaural signals project in parallel to Complex
localization
the central nucleus of the inferior
collicu-
lus (ICC). The classical ascending auditory pathway continues from the ICC to the auditory thalamus and then to the forebrain. The midbrain Orientation
Forebrain
of gaze
classical
and involves ternal
pathway branches from the
pathway at the level of the ICC a projection
nucleus
first to the ex-
of the inferior
colliculus
(ICx) and then to the optic rectum (OT). Spatially
tuned auditory
map of auditory in the OT midbrain
vviv
neurons
space are found
and ICx.
The
forebrain
pathways are reciprocally
and a both and inter-
connected by direct and indirect connec-
pathway
tions (gray arrows). Both pathways can in-
Auditory
dependently compute sound source loca-
brainstem
tion and direct orientation
of gaze. How-
ever, in some species at least, the fore-
nuclei
brain pathway is required for more com0 1994 Current Op~mon in Neurobiology
plex behaviors,
such as movement to the
location of a sound source.
Neural substrates of sound localization Brainard
in the IC suggest that the VLVp contralateral to the IC provides inhibition from the ipsilateral ear, whereas the VLVp ipsilateral to the IC provides inhibition from the contralateral ear [15**]. An analogous source of inhibition in mammals is the dorsal nucleus of the lateral lemniscus, which, like the VLVp [ 171, contains ipsilateral ear neurons, sends a bilateral GABAergic projection to the IC and contributes to acoustically evoked inhibition in the contralateral IC [18*,19].
Neural tuning for monaural spectral cues
In the mammalian superior colliculus (SC) and ICx, most spatially tuned neurons maintain their selectivity for azimuthal sound source location after monaural occlusion or cochlear ablation [20,21*,22]. Unlike the case for binaural hearing, this selectivity is maintained only for near-threshold sound levels and is lost as the sound level is increased. Two separate mechanisms potentially contribute to this type of spatial tuning in the absence of binaural cues. First, the external ear maximally amplifies sounds from a restricted region of space, the location of which varies with frequency. Consequently, low-level stimuli may elicit responses only from within the region of maximum amplification, whereas high-level stimuli are above threshold for all locations. The azimuthal sensitivity of some neurons in the IC [23] and auditory nerve [24*] can be explained by the direction-dependent amplification by the ear at the frequencies to which the neurons are most responsive. Second, the shape of the spectrum that results from the filtering of broadband sounds by the external ear (monaural spectrum) varies with the location of the source but does not depend on the level of the sound [l] _Hence, neurons can potentially develop spatial tuning by integrating information across ti-equencies in order to respond to appropriate monaural spectra. The most persuasive evidence that monaural spatial tuning in the SC utilizes spectral cues is the finding that some neurons are tuned to locations that do not appear to correspond with locations from which sounds are maximally amplified by the external ears [21’,25*]. Evidence for utilization of monaural spectral cues in the SC could be further strengthened by a careful demonstration that spatial tuning cannot be explained by the combination of ear directionality and frequency tuning, and that spatial selectivity under monaural conditions requires broadband stimuli. Spatial tuning that remains substantially unchanged after disruption of binaural cues (by plugging one ear) also has been demonstrated for some neurons in cat primary auditory cortex [26**]. For many of these neurons, unlike those in the SC, monaurally characterized receptive field sizes do not expand with increasing sound levels. Indeed, responses to sounds from all locations are often inhibited for high sound levels, as is the case for many binaurally characterized ILD-sensitive neurons [27’,28*]. Furthermore, these neurons are not spatially tuned for tonal stimuli. These findings strongly indicate that the
spatial tuning of some cortical neurons derives in part horn their selectivity for monaural spectral cues. In both the cortex and the SC, most of the neurons that are tuned under monaural conditions are also sensitive to binaural cues [21*,22,25’,26”]. Moreover, it appears that tuning for any one cue may help eliminate ambiguities associated with other cues. For example, some cortical neurons under monaural conditions have discrete receptive fields in both ipsilateral and contralateral space. Under binaural conditions, inhibition may eliminate responses to sounds in ipsilateral space, leaving a single restricted receptive field [26*.]. Such integration of information across different localization cues is required to eliminate ambiguities associated with individual cues
Pll-
Plasticity of auditory
spatial representations
The correspondences between sound localization cues and spatial locations depend on the geometry of the head and external ears. Because these features change over the course of development and vary between individuals, the developing nervous system can anticipate only approximately the values of auditory cues that will be produced by sounds at particular spatial locations. Earlier studies have demonstrated that both sound localization behavior and the neurophysiological representation of auditory space are customized according to the experience of the individual [12*,29]. Recent experiments have focused on the influence of visual experience on the representation of auditory space in both the forebrain and midbrain.
Visual deprivation
Two competing hypotheses are currently being explored regarding the influence of visual deprivation during development on sound localization. The ‘sensory compensation’ hypothesis suggests that increased reliance on audition in visually deprived animals should result in enhanced sound localization capabilities. The ‘visual calibration’ hypothesis suggests that spatial information provided by vision is required to learn the values of localization cues associated with locations in space, and that visual deprivation should degrade sound localization behavior and the neural representation of auditory space. Both hypotheses have received support from recent studies. In cats reared with closed eyes (binocular eyelid suture), the amount of anterior ectosylvian cortex devoted to the representation of auditory information is expanded at the expense of adjacent areas normally representing visual information [3000]. Furthermore, the auditory spatial tuning of neurons in the expanded forebrain representation is sharper than in normal cats [31.*]. The increased representation of auditory information in the forebrain parallels the earlier finding in cats reared with closed eyes of an increased percentage of auditory neurons in the SC
559
560
Sensory systems
and the significant presence of auditory normally visual superficial layers [32].
responses
in the
In contrast to these findings, rearing ferrets with closed eyes does not appreciably alter the laminar distribution of auditory responsive neurons in the SC [33*]. Moreover, although the sharpness of tuning for sound source location is normal, the systematic progression of receptive field locations across the SC is somewhat degraded, as has previously been observed in both guinea pigs and barn owls reared with closed eyes [34,35]. Representation of sound source location requires both tuning for localization cues and accurate association of cues with spatial locations. Differential dependence of these two processes on visual experience may partially reconcile the various experimental findings. Sharpness of tuning may be largely unaffected (in SC) or sharpened (in anterior ectosylvian cortex) in visually deprived animals. Cues may be inaccurately associated with spatial locations, however, as suggested by the degraded maps of auditory space in the SC of lid-sutured animals. No comparable assessment is possible in the forebrain, because no systematic forebrain representation of auditory space has yet been found. Alternatively, the seemingly different results of visual deprivation may reflect differences between species, conditions under which animals were reared, or the brain regions examined. In this light, it would be interesting to determine whether rearing cats with closed eyes results in sharpened tuning for spatial location in the SC, as suggested by the finding of sharpened auditory tuning in the forebrain, as well as a degraded auditory space map, consistent with findings in the SC of other species [33*,34,35].
Visual guidance of spatial tuning
Experiments in barn owls have demonstrated that spatial information provided by vision can actively guide the associations of sound localization cues with spatial locations [36,37**]. The OT of normal owls contains mutually aligned maps of auditory and visual space [S]. The azimuthal alignment of these maps reflects the tuning of tectal neurons to the values of ITD produced by sources at the locations of their visual receptive fields [38]. In owls reared wearing prismatic spectacles that optically shift the visual field along the horizon, neurons become tuned to abnormal values of ITD associated with their optically displaced visual receptive fields [37”]. Hence, vision provides a signal that actively guides the topography of the auditory map in the tectum. The visually guided changes in the tectal representation of auditory space can be accounted for by plasticity in the ICx [37**]. This is the first site in the midbrain sound localization pathway of owls [8], and at least some mammalian species [20], where a mapped representation of auditory space appears, suggesting that spatial information provided by vision alters only that portion of the
pathway specifically concerned with of auditory cues in a spatial context.
the interpretation
Adult plasticity
Earlier studies have found that sound localization becomes refractory to experience-dependent modification after certain ‘sensitive periods’ during early life [12*,29]. For example, young owls can adaptively adjust both the neural map of auditory space in the OT and sound localization behavior in response to the abnormal localization cues caused by monaural occlusion, whereas adult owls can not [39]. A recent study has found, however, that significant adaptive adjustments occur in the tectal auditory space map of adult owls following alteration of localization cues by modification of the external ears [40**]. The alterations of sound localization cues, particularly ITDs, by ear modification are less severe than those due to monaural occlusion [40**]. This suggests that while plasticity may be reduced in adult animals, the capacity to adapt to small changes in localization cues is retained. This capacity is appropriate to the demands on the adult nervous system, which normally will experience only small changes in the correspondences between localization cues and sound source locations.
Conclusions Parallel auditory pathways in the forebrain and midbrain can independently compute sound source location and execute localization behaviors. However, significant differences exist between the capabilities and organization of these pathways. Although either pathway can subserve orientation of gaze towards sound sources, in most species the forebrain pathway appears to be critical for creating a representation that can be used for more complex and perhaps ‘cognitive’ responses. The nature of this forebrain representation remains an important and unanswered question: although individual forebrain neurons are tuned for the spatial location of auditory stimuli, no mapped representation like that in the midbrain pathway has been found. Nevertheless, both pathways must ultimately establish representations based on the neural encoding of monaural and binaural localization cues, and the correct associations of these cues with spatial locations. These processes are significantly shaped by experience, which customizes sound localization mechanisms for the individual.
Acknowledgements I thank DE Feldman, JI Gold and EI Knudsen for helpful discussions and comments on the manuscript. This work was supported in part by NIH grant ROl-DC00155 to EI Knudsen.
Neural
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40. ..
Knudsen El, Esterly SD, Olsen JF: Adaptive Plasticity of the Auditory Space Map in the Optic Tectum of Adult and Baby Barn Owls in Response to External Ear Modification. / Neurophysiol 1994, 71:79-94. The representation of auditory space in the OT was characterized in adult and baby barn owls that had been chronically exposed to abnormal localization cues by removal of the facial ruff and preaural flaps that comprise the external ear. In baby and adult owls, the neural maps of both ITD and ILD were adaptively adjusted so as to partially restore the normal topography of the auditory space map. The results demonstrate that significant plasticity in the neural representation of auditory space persists in adult animals.
MS
Brainard,
School
Department
of Medicine,
of Neurobiology,
Stanford,
California
Stanford 94305-5401,
University USA.