Map Of Auditory Space Research Articles

Incremental training increases the plasticity of the auditory space map in adult barn owls.

The plasticity in the central nervous system that underlies learning is generally more restricted in adults than in young animals. In one well-studied example, the auditory localization pathway has been shown to be far more limited in its capacity to adjust to abnormal experience in adult than in juvenile barn owls. Plasticity in this pathway has been induced by exposing owls to prismatic spectacles that cause a large, horizontal shift of the visual field. With prisms, juveniles learn new associations between auditory cues, such as interaural time difference (ITD), and locations in visual space, and acquire new neurophysiological maps of ITD in the optic tectum, whereas adults do neither. Here we show that when the prismatic shift is experienced in small increments, maps of ITD in adults do change adaptively. Once established through incremental training, new ITD maps can be reacquired with a single large prismatic shift. Our results show that there is a substantially greater capacity for plasticity in adults than was previously recognized and highlight a principled strategy for tapping this capacity that could be applied in other areas of the adult central nervous system.

Precise inhibition is essential for microsecond interaural time difference coding.

Microsecond differences in the arrival time of a sound at the two ears (interaural time differences, ITDs) are the main cue for localizing low-frequency sounds in space. Traditionally, ITDs are thought to be encoded by an array of coincidence-detector neurons, receiving excitatory inputs from the two ears via axons of variable length ('delay lines'), to create a topographic map of azimuthal auditory space. Compelling evidence for the existence of such a map in the mammalian lTD detector, the medial superior olive (MSO), however, is lacking. Equally puzzling is the role of a--temporally very precise glycine--mediated inhibitory input to MSO neurons. Using in vivo recordings from the MSO of the Mongolian gerbil, we found the responses of ITD-sensitive neurons to be inconsistent with the idea of a topographic map of auditory space. Moreover, local application of glycine and its antagonist strychnine by iontophoresis (through glass pipette electrodes, by means of an electric current) revealed that precisely timed glycine-controlled inhibition is a critical part of the mechanism by which the physiologically relevant range of ITDs is encoded in the MSO. A computer model, simulating the response of a coincidence-detector neuron with bilateral excitatory inputs and a temporally precise contralateral inhibitory input, supports this conclusion.

The optic tectum controls visually guided adaptive plasticity in the owl's auditory space map.

The midbrain contains an auditory map of space that is shaped by visual experience. When barn owls are raised wearing spectacles that horizontally displace the visual field, the auditory space map in the external nucleus of the inferior colliculus (ICX) shifts according to the optical displacement of the prisms. Topographic visual activity in the optic tectum could serve as the template that instructs the auditory space map. We studied the effects of a restricted, unilateral lesion in the portion of the optic tectum that represents frontal space. Here we show that such a lesion eliminates adaptive adjustments specifically in the portion of the auditory map that represents frontal space on the same side of the brain, while the rest of the map continues to adjust adaptively. Thus, activity in the tectum calibrates the auditory space map in a location-specific manner. Because the site of adaptive changes is the ICX, the results also indicate that the tectum provides a topographic instructive signal that controls adaptive auditory plasticity in the ICX.

Neuronas que codifican la dirección del sonido

In the auditory system, the inner ear breaks down complex signals into their spectral components, and encodes the amplitude and phase of each. In order to infer sound direction in space, a computation on each frequency component of the sound must be performed. Space specific neurons in the owl s inferior colliculus respond only to sounds coming from a particular direction and represent the results of this computation. The interaural time difference (ITD) and interaural level difference (ILD define the auditory space for the owl and are processed in separate neural pathways. The parallel pathways that process these cues merge in the external nucleus of the inferior colliculus where the space specific neurons are selective to combinations of ITD and ILD. How do inputs from the two sources interact to produce combination selectivity to ITD ILD pairs? A multiplication of postsynaptic potentials tuned to ITD and ILD can account for the subthreshold responses of these neurons to ITD ILD pairs. Examples of multiplication by neurons or neural circuits are scarce, but many computational models assume the existence of this basic operation. The owl s auditory system uses such operation to create a 2 dimensional map of auditory space. The map of space in the owl s auditory system shows important similarities with representations of space in the cerebral cortex and other sensory systems. In encoding space or other stimulus features, individual neurons appear to possess analogous functional properties related to the synthesis of high order receptive fields.

In Brief

The optic tectum of a barn owl contains auditory and visual space maps that are aligned so that the owl accurately orients its gaze to the source of a sound. This calibration is experience-dependent; when an owl is raised wearing prism glasses, the auditory receptive fields of neurons in the optic tectum shift in order to compensate for the shifted visual fields. To determine if this plasticity occurs via topographic (point-by-point) or foveal-directed comparisons, researchers from Stanford University raised owls with prism glasses and then removed them. Next, animals were fitted with glasses that exposed the center and periphery of their visual fields to different conditions and were allowed to readjust for several weeks. Subsequent recordings in the optic tectum suggested that point-by-point topographic signals are used in calibration of the auditory space map, because visual occlusion diminished the amount of auditory adjustment that occurred in the corresponding portion of the optic tectum. (J. Neurosci. 21, 8586–8593). LO

A Topographic Instructive Signal Guides the Adjustment of the Auditory Space Map in the Optic Tectum

Maps of auditory space in the midbrain of the barn owl (Tyto alba) are calibrated by visual experience. When owls are raised wearing prismatic spectacles that displace the visual field in azimuth, the auditory receptive fields of neurons in the optic tectum shift to compensate for the optical displacement of the visual field. This shift results primarily from a shift in the tuning of tectal neurons for interaural time difference. The visually based instructive signal that guides this plasticity could be based on a topographic, point-by-point comparison between auditory and visual space maps or on a foveation-dependent visual assessment of the accuracy of auditory orienting responses. To distinguish between these two possibilities, we subjected owls to optical conditions that differed in the center of gaze and the visual periphery. A topographic signal would cause the portions of the space map representing the central and peripheral regions of visual space to adjust differently, according to the optical conditions that exist in each region. In contrast, a foveation-based signal would cause both portions of the map to adjust similarly, according to the optical conditions that exist at the center of gaze. In six of seven experiments, adaptive changes were as predicted by a topographic instructive signal. Although the results do not rule out the possible contribution of a foveation-based signal, they demonstrate that a topographic instructive signal is, indeed, involved in the calibration of the auditory space map in the barn owl optic tectum.

GABAergic Inhibition Antagonizes Adaptive Adjustment of the Owl's Auditory Space Map during the Initial Phase of Plasticity

We studied the influence of GABA-mediated inhibition on adaptive adjustment of the owl's auditory space map during the initial phase of plasticity. Plasticity of the auditory space map was induced by subjecting owls to a chronic prismatic displacement of the visual field. In the initial stages of plasticity, inhibition suppressed responses to behaviorally appropriate, newly functional excitatory inputs. As a result, adaptive changes in excitatory input were only partially expressed as postsynaptic spike activity. This masking effect of inhibition on map plasticity did not depend on the activity of NMDA receptors at the synapses that supported the newly learned responses. On the basis of these results, we propose that the pattern of feedforward inhibition is less dynamic than the pattern of feedforward excitation at the site of plasticity. As a result, initially in the adjustment process the preexisting pattern of feedforward GABAergic inhibition opposes changes in the auditory space map and tends to preserve the established response properties of the network. The implications of this novel role of inhibition for the functional plasticity of the brain are discussed.

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.

Auditory spatial receptive fields created by multiplication.

Examples of multiplication by neurons or neural circuits are scarce, although many computational models use this basic operation. The owl's auditory system computes interaural time (ITD) and level (ILD) differences to create a two-dimensional map of auditory space. Space-specific neurons are selective for combinations of ITD and ILD, which define, respectively, the horizontal and vertical dimensions of their receptive fields. A multiplication of separate postsynaptic potentials tuned to ITD and ILD, rather than an addition, can account for the subthreshold responses of these neurons to ITD-ILD pairs. Other nonlinear processes improve the spatial tuning of the spike output and reduce the fit to the multiplicative model.

Adaptive adjustment of connectivity in the inferior colliculus revealed by focal pharmacological inactivation.

In the midbrain sound localization pathway of the barn owl, a map of auditory space is synthesized in the external nucleus of the inferior colliculus (ICX) and transmitted to the optic tectum. Early auditory experience shapes these maps of auditory space in part by modifying the tuning of the constituent neurons for interaural time difference (ITD), a primary cue for sound-source azimuth. Here we show that these adaptive modifications in ITD tuning correspond to changes in the pattern of connectivity within the inferior colliculus. We raised owls with an acoustic filtering device in one ear that caused frequency-dependent changes in sound timing and level. As reported previously, device rearing shifted the representation of ITD in the ICX and tectum but not in the primary source of input to the ICX, the central nucleus of the inferior colliculus (ICC). We applied the local anesthetic lidocaine (QX-314) iontophoretically in the ICC to inactivate small populations of neurons that represented particular values of frequency and ITD. We measured the effect of this inactivation in the optic tecta of a normal owl and owls raised with the device. In the normal owl, inactivation at a critical site in the ICC eliminated responses in the tectum to the frequency-specific ITD value represented at the site of inactivation in the ICC. The location of this site was consistent with the known pattern of ICC-ICX-tectum connectivity. In the device-reared owls, adaptive changes in the representation of ITD in the tectum corresponded to dramatic and predictable changes in the locations of the critical sites of inactivation in the ICC. Given that the abnormal representation of ITD in the tectum depended on frequency and was likely conveyed directly from the ICX, these results suggest that experience causes large-scale, frequency-specific adjustments in the pattern of connectivity between the ICC and the ICX.

Cortical codes for sound localization

It is well known that there is a point-to-point map of auditory space in the midbrain: each neuron is tuned to a particular sound-source location, and neurons' preferred locations are topograph- ically represented in a neural structure. In the auditory cortex, however, researchers have consistently failed to demonstrate evidence for such an auditory space map, despite the well-known necessity of the auditory cortex for normal sound localization. Cortical neurons show generally broad spatial tuning, and the preferred locations are not systematically organized on the cortex in a topographical fashion. An al- ternative hypothesis is presented here: Individual single neurons represent auditory space panoramically by space-specific characteristics of their spike patterns. Information about any particular sound-source location is distributed across a large population of neurons, and we predict accurate localization judge- ment by combining information across those neurons. In our analyses of experimental data using an artificial neural network algorithm, we were able to recognize spike patterns of single neurons to iden- tify sound-source locations throughout 360 ◦ of space. The amount of information carried by a moderate size of neural ensemble appeared sufficient to account for the accuracy of location judgements by be- having animals.

Auditory Peripersonal Space in Humans: a Case of Auditory-Tactile Extinction

Animal experiments have shown that the spatial correspondence between auditory and tactile receptive fields of ventral pre-motor neurons provides a map of auditory peripersonal space around the head. This allows neurons to localize a near sound with respect to the head. In the present study, we demonstrated the existence of an auditory peripersonal space around the head in humans. In a right-brain damaged patient with tactile extinction, a sound delivered near the ipsilesional side of the head extinguished a tactile stimulus delivered to the contralesional side of the head (cross-modal auditory-tactile extinction). In contrast, when an auditory stimulus was presented far from the head, cross-modal extinction was dramatically reduced. This spatially specific cross-modal extinction was found only when a complex sound like a white noise burst was presented; pure tones did not produce spatially specific cross-modal extinction. These results show a high degree of functional similarity between the characteristics of the auditory peripersonal space representation in humans and monkeys. This similarity suggests that analogous physiological substrates might be responsible for coding this multisensory integrated representation of peripersonal space in human and non-human primates.

Topographical projection from the superior colliculus to the nucleus of the brachium of the inferior colliculus in the ferret: convergence of visual and auditory information

The normal maturation of the auditory space map in the deeper layers of the ferret superior colliculus (SC) depends on signals provided by the superficial visual layers, but it is unknown where or how these signals influence the developing auditory responses. Here we report that tracer injections in the superficial layers label axons with en passant and terminal boutons, both in the deeper layers of the SC and in their primary source of auditory input, the nucleus of the brachium of the inferior colliculus (nBIC). Electron microscopy confirmed that biocytin-labelled SC axons form axodendritic synapses on nBIC neurons. Injections of biotinylated dextran amine in the nBIC resulted in anterograde labelling in the deeper layers of the SC, as well as retrogradely labelled superficial and deep SC neurons, whose distribution varied systematically with the rostrocaudal placement of the injection sites in the nBIC. Topographical order in the projection from the SC to the ipsilateral nBIC was confirmed using fluorescent microspheres. We demonstrated the existence of functional SC-nBIC connections by making whole-cell current-clamp recordings from young ferret slices. Both monosynaptic and polysynaptic EPSPs were generated by electrical stimulation of either the superficial or deep SC layers. In addition to unimodal auditory units, both visual and bimodal visual-auditory units were recorded in the nBIC in vivo and their incidence was higher in juvenile ferrets than in adults. The SC-nBIC circuit provides a potential means by which visual and other sensory or premotor signals may be delivered to the nBIC to calibrate the representation of auditory 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.

Projections from the rostral pole of the inferior colliculus to the cat superior colliculus

The neuroanatomical data given here reveal a dense projection from the rostral pole of the cat inferior colliculus (rpIC) to the superior colliculus (SC). A portion of this pathway distributes in ‘patches’ across the ventral portion of the intermediate grey layer. These finding suggest that the rpIC input to the SC might play a role in determining the auditory receptive fields of SGI neurons and in the construction of the SC’s precise two dimensional map of auditory space.

Topographic projection from the optic tectum to the auditory space map in the inferior colliculus of the barn owl.

In the barn owl (Tyto alba), the external nucleus of the inferior colliculus (ICX) contains a map of auditory space that is calibrated by visual experience. The source of the visually based instructive signal to the ICX is unknown. Injections of biotinylated dextran amine and Fluoro-Gold in the ICX retrogradely labelled neurons in layers 8-15 of the ipsilateral optic tectum (OT) that could carry this instructive signal. This projection was point-to-point and in register with the feed-forward, auditory projection from the ICX to the OT. Most labelled neurons were in layers 10-11, and most were bipolar. Tripolar, multipolar, and unipolar neurons were also observed. Multipolar neurons had dendrites that were oriented parallel to the tectal laminae. In contrast, most labelled bipolar and tripolar neurons had dendrites oriented perpendicular to the tectal laminae, extending superficially into the retino-recipient laminae and deep into the auditory recipient laminae. Therefore, these neurons were positioned to receive both visual and auditory information from particular locations in space. Biocytin injected into the superficial layers of the OT labelled bouton-laden axons in the ICX. These axons were generally finer than, but had similar bouton densities as, feed-forward auditory fibers in the ICX, labelled by injections of biocytin into the central nucleus of the inferior colliculus (ICC). These data demonstrate a point-to-point projection from the OT to the ICX that could provide a spatial template for calibrating the auditory space map in the ICX.

A Site of Auditory Experience-Dependent Plasticity in the Neural Representation of Auditory Space in the Barn Owl's Inferior Colliculus

The barn owl's optic tectum contains a map of auditory space that is based, in part, on a map of interaural time difference (ITD). Previous studies have shown that this ITD map is shaped by auditory experience. In this study, we investigated whether the plasticity responsible for experience-induced changes in ITD tuning in the tectum occurs within the tectum itself or at an earlier stage in the auditory pathway. We altered auditory experience in young owls by implanting an acoustic filtering device in one ear that caused frequency-dependent changes in sound timing and level. We analyzed the representation of ITD in normal and device-reared owls in two nuclei in the ascending pathway: the external nucleus of the inferior colliculus (ICX), the primary source of ascending auditory input to the tectum, and the lateral shell of the central nucleus of the inferior colliculus (ICCls), the primary source of input to the ICX. In the ICX, device rearing caused adaptive, frequency-dependent changes in ITD tuning, as well as changes in frequency tuning. These changes in tuning were similar to changes that occurred in the optic tectum in the same owls. In contrast, in the ICCls, tuning for ITD and frequency was unaffected by device rearing. The data indicate that plasticity at the level of the ICX is largely responsible for the adaptive adjustments in ITD tuning and frequency tuning that are observed in the optic tecta of owls raised with abnormal auditory experience.

A Candidate Pathway for a Visual Instructional Signal to the Barn Owl's Auditory System

Many organisms use multimodal maps to generate coherent neuronal representations that allow adequate responses to stimuli that excite several sensory modalities. During ontogeny of these maps, one modality typically acts as the dominant system the other modalities are aligned to. A well studied model for the alignment of sensory maps is the calibration of the auditory space map by the visual system in the optic tectum of the barn owl. However, a projection from the optic tectum to the site of plasticity in the auditory pathway that could deliver an instructive signal has not been found so far. We have analyzed the development of the connectivity between the bimodal (visual and auditory) map of space in the barn owl's optic tectum and the auditory space map in the inferior colliculus with tracing methods and intracellular fills. Neurons in the tectal stratum griseum centrale were found to be suited to deliver an alignment signal from the visual midbrain to the auditory pathway. These neurons are presumably part of the efferent tectal projection pathway that mediates head saccades. The implications of a sensory alignment signal possibly being delivered by a (pre)motor command pathway are discussed.

Sensory experience and the formation of a computational map of auditory space in the brain

The basic wiring of the brain is first established before birth by using a variety of molecular guidance cues. These connections are then refined by patterns of neural activity, which are initially generated spontaneously and subsequently driven by sensory experience. In the superior colliculus, a midbrain nucleus involved in the control of orienting behaviour, visual, auditory, and tactile inputs converge to form superimposed maps of sensory space. Maps of visual space and of the body surface arise from spatially ordered projections from the retina and skin, respectively. In contrast, the map of auditory space is computed within the brain by tuning the neurons to different localization cues that result from the acoustical properties of the head and ears. Establishing and maintaining the registration of the maps in the face of individual differences in the size and relative positions of different sense organs is an activity-dependent process in which the synaptic circuits underlying the auditory representation are modified and calibrated under the influence of both auditory and visual experience. BioEssays 1999;21:900–911. © 1999 John Wiley & Sons, Inc.

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.