Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl

Takahashi, Terry T.; Carr, Catherine; Brecha, Nicholas C.; Konishi, Masakazu

doi:10.1523/jneurosci.07-06-01843.1987

Cited by 101 publications

(65 citation statements)

References 31 publications

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“…PV-ir predominates in a restricted core region of the central nucleus, with CR and CB-ir in the surrounding peripheral areas of the central nucleus. These complementary patterns of expression in amphibians and reptiles are similar to the patterns of CR and acetylcholinesterase expression observed in the core and shell regions of the central nucleus of the barn owl inferior colliculus (Adolphs, 1993;Takahashi et al, 1987).Separate, nonoverlapping projections from first-order, olivary, and lemniscal nuclei are somewhat incompatible with the tonotopy observed in the central nucleus of the auditory midbrain of mammals, archosaurs, and amphibians. In these vertebrates, the inferior colliculus is characterized by first-order projections throughout the central nucleus and by a dorsoventral low-to high-frequency tonotopy, although the pattern and frequency range differ (for reviews see Covey and Carr, 2005;Grothe et al, 2005).…”

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confidence: 57%

“…They label neurons in the central auditory system of mammals such as rat (Lohmann and Friauf, 1996;Pór et al, 2005), guinea pig (Caicedo et al, 1996), and human (Bazwinsky et al, 2003); in birds such as chicken (Parks et al, 1997) and barn owl (Kubke et al, 1999;Takahashi et al, 1987); and in lizards (Dávila et al, 2000), turtles (Belekhova et al, 2004), and amphibians (Morona and González, 2009). We therefore used antibodies against calretinin (CR), parvalbumin (PV), and calbindin-D28k (CB), along with antibodies against glutamic acid decarboxylase (GAD) and synaptic vesicle protein 2 (SV2), to describe the gecko ascending auditory pathways.…”

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Calcium‐binding protein immunoreactivity characterizes the auditory system of Gekko gecko

Yang

Tang

Carr

2010

J of Comparative Neurology

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Geckos use vocalizations for intraspecific communication, but little is known about the organization of their central auditory system. We therefore used antibodies against the calciumbinding proteins calretinin (CR), parvalbumin (PV), and calbindin-D28k (CB) to characterize the gecko auditory system. We also examined expression of both glutamic acid decarboxlase (GAD) and synaptic vesicle protein (SV2). Western blots showed that these antibodies are specific to gecko brain. All three calcium-binding proteins were expressed in the auditory nerve, and CR immunoreactivity labeled the first-order nuclei and delineated the terminal fields associated with the ascending projections from the first-order auditory nuclei. PV expression characterized the superior olivary nuclei, whereas GAD immunoreactivity characterized many neurons in the nucleus of the lateral lemniscus and some neurons in the torus semicircularis. In the auditory midbrain, the distribution of CR, PV, and CB characterized divisions within the central nucleus of the torus semicircularis. All three calcium-binding proteins were expressed in nucleus medialis of the thalamus. These expression patterns are similar to those described for other vertebrates.Keywords cochlear nucleus; magnocellularis; laminaris; angularis; torus Over 30 years have passed since Foster and Hall (1978) reported that the ascending auditory pathways of the iguana resemble both the mammalian and the avian auditory pathways, from the level of the first-order neurons in the VIIIth nerve to the telencephalon. They recognized a basic plan for the organization of the auditory system in terrestrial vertebrates but also pointed out that the auditory capacities of the lizards were largely unknown. We now know more about the peripheral (Manley, 1990;Wever, 1978) and central (for reviews see Carr, 1992;Grothe et al., 2005;ten Donkelaar et al., 1987) auditory systems of lizards, but still know little about central auditory processing. We have therefore used Gekko gecko for further analysis of the lizard central auditory system.Geckos are auditory specialists that use vocalizations for intraspecific communication (Marcellini, 1977;Tang et al., 2001). Their ears differ from those of other reptiles such as archosaurs and turtles. Lepidosaur ears are highly directional, with middle ears connected through the mouth cavity (Christensen-Dalsgaard and Manley, 2008). This patent connection enhances the directionality of the ear by allowing sound access to both sides of NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript each tympanic membrane. The acoustically coupled ear creates directional responses from the tympanum Manley, 2005, 2008). Additionally, lizards have independently evolved micromechanical hair cell tuning, permitting emergence of sensitive high-frequency hearing in a specialized region of the papilla (Manley, 2002). Thus lizard auditory systems might reveal specializations for hearing high frequencies and sound localization.We have begun our analysis of liza...

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confidence: 57%

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confidence: 99%

Calcium‐binding protein immunoreactivity characterizes the auditory system of Gekko gecko

Yang

Tang

Carr

2010

J of Comparative Neurology

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“…In CNIC, a distinct afferent domain has been described for calretinin-immunopositive fibers. Calretinin immunostaining appears to be a neurochemical marker for the medial superior olivary nucleus (MSO) projections to the IC in birds (Takahashi et al, 1987) and most likely in mammals Alvarado et al, 2004) as well, although other inputs may be included that occupy overlapping domains. The location and pattern of distribution of CB correspond to afferent inputs to the CNIC from LSO.…”

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confidence: 99%

Quantitative assessment of developing afferent patterns in the cat inferior colliculus revealed with calbindin immunohistochemistry and tract tracing methods

2005

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The central nucleus of the inferior colliculus (CNIC) is comprised of an orderly series of fibrodendritic layers. These layers include integrative circuitry for as many as 13 different ascending auditory pathways, each tonotopically ordered. Calcium-binding proteins, such as calbindin-D28k (CB), may be useful neurochemical markers for specific subsets of afferent input in these layers and their spatial organization that are developmentally regulated. In this study, CBimmunohistochemistry was used to examine 1-42 postnatal-day-old kitten and adult cat CNIC and anterograde tracers were used to label afferent projections from the lateral superior olivary nucleus (LSO) to the CNIC at similar ages. A distinct axonal plexus that is CB-immunopositive is described. This CB-afferent compartment is present at birth and persists throughout the ages examined. Already at birth, the CB-immunostained plexus in kitten CNIC is organized into discrete bands that are approximately 75 μm thick and 500 μm long. In adult CNIC, the periodic banded pattern of CBimmunostained fibers is similar to that in kittens albeit bands are thicker (145 μm) and longer (700 μm). Growth in band thickness in adult cat appears proportional to growth of the IC, whereas length of the dense CB-immunostained bands is somewhat more focused in the central region of fibrodendritic layers. The banded pattern of the CB-immunostained plexus is well correlated with the location and dimension of afferent projections from the LSO in newborn kitten labeled with carbocyanine dye, 1,1′-dioctodecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate and in adult cat labeled with wheat germ agglutinin conjugated with horseradish peroxidase. The results reveal a neurochemical marker for one type of synaptic compartment in CNIC layers, banding, that is organized before hearing onset in kittens, but that may undergo some postnatal pruning. Keywords fibrodendritic laminae; banding pattern; calcium-binding proteins; lateral superior olivary nucleus; carbocyanine dyeIn the auditory midbrain, the inferior colliculus (IC) is comprised of a large, seemingly homogeneous, central nucleus (CNIC) surrounded by a complex and heterogeneous arrangement of several paracentral nuclei (Berman, 1968;Rockel and Jones, 1973a,b;Morest and Oliver, 1984 (Rockel and Jones, 1973a;Oliver and Morest, 1984). With only a few exceptions, all ascending hindbrain auditory pathways project to the CNIC and end in cochleotopic fashion within a series of these fibrodendritic layers. Overlaid on this network of hindbrain inputs are additional inputs from regions of auditory cortex and the contralateral IC as well as non-auditory structures (for review, see Oliver and Shneiderman, 1989). Less numerous are stellate cells and a subset of intrinsic axonal collaterals that depart from this laminar framework and cross laminar boundaries (Oliver et al., 1991).Overall, the stereotypical structure of the CNIC belies the underlying complexity, intrinsic structure, and functional relationships within layers that ...

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“…A 3-dimensional computer reconstruction (Boulder HVEM 3-D Reconstruction Program) of one IC was made from these drawings and rotated for a horizontal view of the nucleus. Alternate sections from 3 owls were used for immunohistochemical staining with an antibody to calbindin; they were processed by the method used on barn owls by Takahashi et al (1987). Retrograde tracers were injected into the optic tecta of 3 owls to label neurons in IC.…”

Section: Methodsmentioning

confidence: 99%

Spatial selectivity and binaural responses in the inferior colliculus of the great horned owl

Volman

Konishi

1989

J. Neurosci.

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In this study we have investigated the processing of auditory cues for sound localization in the great horned owl (Bubo virginianus). Previous studies have shown that the barn owl, whose ears are asymmetrically oriented in the vertical plane, has a 2-dimensional, topographic representation of auditory space in the external division of the inferior colliculus (ICx). As in the barn owl, the great horned owl's ICx is anatomically distinct and projects to the optic tectum. Neurons in ICx respond over only a small range of azimuths (mean = 32 degrees), and azimuth is topographically mapped. In contrast to the barn owl, the great horned owl has bilaterally symmetrical ears and its receptive fields are not restricted in elevation. The binaural cues available for sound localization were measured both with cochlear microphonic recordings and with a microphone attached to a probe tube in the auditory canal. Interaural time disparity (ITD) varied monotonically with azimuth. Interaural intensity differences (IID) also changed with azimuth, but the largest IIDs were less than 15 dB, and the variation was not monotonic. Neither ITD nor IID varied systematically with changes in the vertical position of a sound source. We used dichotic stimulation to determine the sensitivity of ICx neurons to these binaural cues. Best ITD of ICx units was topographically mapped and strongly correlated with receptive-field azimuth. The width of ITD tuning curves, measured at 50% of the maximum response, averaged 72 microseconds. All ICx neurons responded only to binaural stimulation and had nonmonotonic IID tuning curves. Best IID was weakly, but significantly, correlated with best ITD (r = 0.39, p less than 0.05). The IID tuning curves, however, were broad (mean 50% width = 24 dB), and 67% of the units had best IIDs within 5 dB of 0 dB IID. ITD tuning was sensitive to variations in IID in the direction opposite to that expected for time-intensity trading, but the magnitude of this effect was only 1.5 microseconds/dB IID. We conclude that, in the great horned owl, the spatial selectivity of ICx neurons arises primarily from their ITD tuning. Except for the absence of elevation selectivity and the narrow range of best IIDs, ICx in the great horned owl appears to be organized much the same as in the barn owl.

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Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl

Cited by 101 publications

References 31 publications

Calcium‐binding protein immunoreactivity characterizes the auditory system of Gekko gecko

Calcium‐binding protein immunoreactivity characterizes the auditory system of Gekko gecko

Quantitative assessment of developing afferent patterns in the cat inferior colliculus revealed with calbindin immunohistochemistry and tract tracing methods

Spatial selectivity and binaural responses in the inferior colliculus of the great horned owl

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