Adaptation in the Auditory Space Map of the Barn Owl

2006 ◽  
Vol 96 (2) ◽  
pp. 813-825 ◽  
Author(s):  
Yoram Gutfreund ◽  
Eric I. Knudsen
Keyword(s):  
Inferior Colliculus ◽  
Spatial Information ◽  
Short Term Memory ◽  
Threshold Level ◽  
Central Nucleus ◽  
Visually Guided ◽  
Auditory Space ◽  
Visual Spatial ◽  
Stimulus Offset ◽  
A Site

Auditory neurons in the owl’s external nucleus of the inferior colliculus (ICX) integrate information across frequency channels to create a map of auditory space. This study describes a powerful, sound-driven adaptation of unit responsiveness in the ICX and explores the implications of this adaptation for sensory processing. Adaptation in the ICX was analyzed by presenting lightly anesthetized owls with sequential pairs of dichotic noise bursts. Adaptation occurred in response even to weak, threshold-level sounds and remained strong for more than 100 ms after stimulus offset. Stimulation by one range of sound frequencies caused adaptation that generalized across the entire broad range of frequencies to which these units responded. Identical stimuli were used to test adaptation in the lateral shell of the central nucleus of the inferior colliculus (ICCls), which provides input directly to the ICX. Compared with ICX adaptation, adaptation in the ICCls was substantially weaker, shorter lasting, and far more frequency specific, suggesting that part of the adaptation observed in the ICX was attributable to processes resident to the ICX. The sharp tuning of ICX neurons to space, along with their broad tuning to frequency, allows ICX adaptation to preserve a representation of stimulus location, regardless of the frequency content of the sound. The ICX is known to be a site of visually guided auditory map plasticity. ICX adaptation could play a role in this cross-modal plasticity by providing a short-term memory of the representation of auditory localization cues that could be compared with later-arriving, visual–spatial information from bimodal stimuli.

scholarly journals Forebrain Pathway for Auditory Space Processing in the Barn Owl

1998 ◽  
Vol 79 (2) ◽  
pp. 891-902 ◽  
Author(s):  
Yale E. Cohen ◽  
Greg L. Miller ◽  
Eric I. Knudsen
Keyword(s):  
Inferior Colliculus ◽  
Sound Localization ◽  
Spatial Information ◽  
Barn Owl ◽  
Afferent Input ◽  
Central Nucleus ◽  
Appreciable Effect ◽  
Auditory Space ◽  
Space Processing ◽  
Field L

Cohen, Yale E., Greg L. Miller, and Eric I. Knudsen. Forebrain pathway for auditory space processing in the barn owl. J. Neurophysiol. 79: 891–902, 1998. The forebrain plays an important role in many aspects of sound localization behavior. Yet, the forebrain pathway that processes auditory spatial information is not known for any species. Using standard anatomic labeling techniques, we used a “top-down” approach to trace the flow of auditory spatial information from an output area of the forebrain sound localization pathway (the auditory archistriatum, AAr), back through the forebrain, and into the auditory midbrain. Previous work has demonstrated that AAr units are specialized for auditory space processing. The results presented here show that the AAr receives afferent input from Field L both directly and indirectly via the caudolateral neostriatum. Afferent input to Field L originates mainly in the auditory thalamus, nucleus ovoidalis, which, in turn, receives input from the central nucleus of the inferior colliculus. In addition, we confirmed previously reported projections of the AAr to the basal ganglia, the external nucleus of the inferior colliculus (ICX), the deep layers of the optic tectum, and various brain stem nuclei. A series of inactivation experiments demonstrated that the sharp tuning of AAr sites for binaural spatial cues depends on Field L input but not on input from the auditory space map in the midbrain ICX: pharmacological inactivation of Field L eliminated completelyauditory responses in the AAr, whereas bilateral ablation of the midbrain ICX had no appreciable effect on AAr responses. We conclude, therefore, that the forebrain sound localization pathway can process auditory spatial information independently of the midbrain localization pathway.

Binaural processing of sound pressure level in the inferior colliculus

1987 ◽  
Vol 57 (4) ◽  
pp. 1130-1147 ◽  
Author(s):  
M. N. Semple ◽  
L. M. Kitzes
Keyword(s):  
Inferior Colliculus ◽  
Sound Pressure ◽  
Spatial Information ◽  
Discharge Rate ◽  
Excitatory Input ◽  
Central Nucleus ◽  
Intensity Difference ◽  
Inhibitory Input ◽  
Directional Information ◽  
Discharge Rates

The central auditory system could encode information about the location of a high-frequency sound source by comparing the sound pressure levels at the ears. Two potential computations are the interaural intensity difference (IID) and the average binaural intensity (ABI). In this study of the central nucleus of the inferior colliculus (ICC) of the anesthetized gerbil, we demonstrate that responses of 85% of the 97 single units in our sample were jointly influenced by IID and ABI. For a given ABI, discharge rate of most units is a sigmoidal function of IID, and peak rates occur at IIDs favoring the contralateral ear. Most commonly, successive increments of ABI cause successive shifts of the IID functions toward IIDs favoring the ipsilateral ear. Neurons displaying this behavior include many that would conventionally be classified EI (receiving predominantly excitatory input arising from one ear and inhibitory input from the other), many that would be classified EE (receiving predominantly excitatory input arising from each ear), and all that are responsive only to contralateral stimulation. The IID sensitivity of a very few EI neurons is unaffected by ABI, except near threshold. Such units could provide directional information that is independent of source intensity. A few EE neurons are very sensitive to ABI, but are minimally sensitive to IID. Nevertheless, our data indicate that responses of most EE units in ICC are strongly dominated by excitation of contralateral origin. For some units, discharge rate is nonmonotonically related to IID and is maximal when the stimuli at the two ears are of comparable sound pressure. This preference for zero IID is common for all binaural levels. Many EI neurons respond nonmonotonically to ABI. Discharge rates are greater for IIDs representative of contralateral space and are maximal at a single best ABI. For a subset of these neurons, the influence arising from the ipsilateral ear is comprised of a mixture of excitation and inhibition. As a consequence, discharge rates are nonmonotonically related not only to ABI but also to IID. This dual nonmonotonicity creates a clear focus of peak response at a particular ABI/IID combination. Because of their mixed monaural influences, such units would be ascribed to different classes of the conventional (EE/EI) binaural classification scheme depending on the binaural level presented. Several response classes were identified in this study, and each might contribute differently to the encoding of spatial information.(ABSTRACT TRUNCATED AT 400 WORDS)

Egocentric Action in Early Infancy: Spatial Frames of Reference for Saccades

1997 ◽  
Vol 8 (3) ◽  
pp. 224-230 ◽  
Author(s):  
Rick O. Gilmore ◽  
Mark H. Johnson
Keyword(s):  
Spatial Information ◽  
Visual Space ◽  
Frames Of Reference ◽  
Saccade Target ◽  
Visually Guided ◽  
Retinal Position ◽  
Position Information ◽  
Visual Spatial ◽  
Visually Guided Action ◽  
Spatial Frames Of Reference

The extent to which infants combine visual (i e, retinal position) and nonvisual (eye or head position) spatial information in planning saccades relates to the issue of what spatial frame or frames of reference influence early visually guided action We explored this question by testing infants from 4 to 6 months of age on the double-step saccade paradigm, which has shown that adults combine visual and eye position information into an egocentric (head- or trunk-centered) representation of saccade target locations In contrast, our results imply that infants depend on a simple retinocentric representation at age 4 months, but by 6 months use egocentric representations more often to control saccade planning Shifts in the representation of visual space for this simple sensorimotor behavior may index maturation in cortical circuitry devoted to visual spatial processing in general

scholarly journals Comparison of Midbrain and Thalamic Space-Specific Neurons in Barn Owls

2006 ◽  
Vol 95 (2) ◽  
pp. 783-790 ◽  
Author(s):  
María Lucía Pérez ◽  
José Luis Peña
Keyword(s):  
Inferior Colliculus ◽  
Spatial Information ◽  
Receptive Fields ◽  
Stimulus Frequency ◽  
Auditory Pathway ◽  
Mammalian Brain ◽  
Neural Pathways ◽  
Spatial Cues ◽  
Auditory Space ◽  
Barn Owls

Spatial receptive fields of neurons in the auditory pathway of the barn owl result from the sensitivity to combinations of interaural time (ITD) and level differences across stimulus frequency. Both the forebrain and tectum of the owl contain such neurons. The neural pathways, which lead to the forebrain and tectal representations of auditory space, separate before the midbrain map of auditory space is synthesized. The first nuclei that belong exclusively to either the forebrain or the tectal pathways are the nucleus ovoidalis (Ov) and the external nucleus of the inferior colliculus (ICx), respectively. Both receive projections from the lateral shell subdivision of the inferior colliculus but are not interconnected. Previous studies indicate that the owl's tectal representation of auditory space is different from those found in the owl's forebrain and the mammalian brain. We addressed the question of whether the computation of spatial cues in both pathways is the same by comparing the ITD tuning of Ov and ICx neurons. Unlike in ICx, the relationship between frequency and ITD tuning had not been studied in single Ov units. In contrast to the conspicuous frequency independent ITD tuning of space-specific neurons of ICx, ITD selectivity varied with frequency in Ov. We also observed that the spatially tuned neurons of Ov respond to lower frequencies and are more broadly tuned to ITD than in ICx. Thus there are differences in the integration of frequency and ITD in the two sound-localization pathways. Thalamic neurons integrate spatial information not only within a broader frequency band but also across ITD channels.

scholarly journals Alignment of sound localization cues in the nucleus of the brachium of the inferior colliculus

2014 ◽  
Vol 111 (12) ◽  
pp. 2624-2633 ◽  
Author(s):  
Sean J. Slee ◽  
Eric D. Young
Keyword(s):  
Inferior Colliculus ◽  
Sound Localization ◽  
Additive Model ◽  
Central Nucleus ◽  
Intensity Difference ◽  
Auditory Space ◽  
Directional Filtering ◽  
Spectral Cues ◽  
Spatial Alignment ◽  
Auditory Space Map

Accurate sound localization is based on three acoustic cues (interaural time and intensity difference and spectral cues from directional filtering by the pinna). In natural listening conditions, every spatial position of a sound source provides a unique combination of these three cues in “natural alignment.” Although neurons in the central nucleus (ICC) of the inferior colliculus (IC) are sensitive to multiple cues, they do not favor their natural spatial alignment. We tested for sensitivity to cue alignment in the nucleus of the brachium of the IC (BIN) in unanesthetized marmoset monkeys. The BIN receives its predominant auditory input from ICC and projects to the topographic auditory space map in the superior colliculus. Sound localization cues measured in each monkey were used to synthesize broadband stimuli with aligned and misaligned cues; spike responses to these stimuli were recorded in the BIN. We computed mutual information (MI) between the set of spike rates and the stimuli containing either aligned or misaligned cues. The results can be summarized as follows: 1) BIN neurons encode more information about auditory space when cues are aligned compared with misaligned. 2) Significantly more units prefer aligned cues in the BIN than in ICC. 3) An additive model based on summing the responses to stimuli with the localization cues varying individually accurately predicts the alignment preference with all cues varying. Overall, the results suggest that the BIN is the first site in the ascending mammalian auditory system that is tuned to natural combinations of sound localization cues.

scholarly journals Representation of Binaural Spatial Cues in Field L of the Barn Owl Forebrain

1998 ◽  
Vol 79 (2) ◽  
pp. 879-890 ◽  
Author(s):  
Yale E. Cohen ◽  
Eric I. Knudsen
Keyword(s):  
Information Processing ◽  
Inferior Colliculus ◽  
Spatial Information ◽  
Functional Organization ◽  
Barn Owl ◽  
Central Nucleus ◽  
Spatial Cues ◽  
High Frequency Region ◽  
Space Processing ◽  
Field L

Cohen, Yale E. and Eric I. Knudsen. Representation of binaural spatial cues in Field L of the barn owl forebrain. J. Neurophysiol. 79: 879–890, 1998. This study examined the representation of spatial information in the barn owl Field L, the first telencephalic processing stage of the classical auditory pathway. Field L units were recorded extracellularly, and their responses to dichotically presented interaural time differences (ITD) and interaural level differences (ILD) were tested. We observed a variety of tuning profiles in Field L. Some sites were not sensitive to ITD or ILD. Other sites, especially those in the high-frequency region, were highly selective for values of ITD and ILD. These sites had multipeaked (commonly called “phase ambiguous”) ITD tuning profiles and were tuned for a single value of ILD. The tuning properties of these sites are similar to those seen in the lateral shell of the central nucleus of the inferior colliculus. Although the tuning properties of Field L sites were similar to those observed in the inferior colliculus, the functional organization of this spatial information was fundamentally different. Whereas in the inferior colliculus spatial information is organized into global topographics maps, in Field L spatial information is organized into local clusters, with sites having similar binaural tuning properties grouped together. The representation of binaural cues in Field L suggests that it is involved in auditory space processing but at a lower level of information processing than the auditory archistriatum, a forebrain area that is specialized for processing spatial information, and that the levels of information processing in the forebrain space processing pathway are remarkably similar to those in the well-known midbrain space processing pathway.

Adaptive Adjustment of Connectivity in the Inferior Colliculus Revealed by Focal Pharmacological Inactivation

2001 ◽  
Vol 85 (4) ◽  
pp. 1575-1584 ◽  
Author(s):  
Joshua I. Gold ◽  
Eric I. Knudsen
Keyword(s):  
Inferior Colliculus ◽  
Large Scale ◽  
Interaural Time Difference ◽  
Primary Source ◽  
Central Nucleus ◽  
Small Populations ◽  
Auditory Space ◽  
Adaptive Adjustment ◽  
Auditory Experience ◽  
Critical Site

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.

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