The Central Auditory System of Reptiles and Birds

Carr, Catherine E.; Code, Rebecca A.

doi:10.1007/978-1-4612-1182-2_5

Cited by 62 publications

(60 citation statements)

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“…In the avian auditory brain stem, acoustic timing and intensity cues are processed in separate ascending pathways, then reconverge in the midbrain to generate a map of auditory space (Carr and Code 2000;Konishi 1978a, 1978b;Konishi et al 1985Konishi et al , 1988Moiseff and Konishi 1983;Sullivan and Konishi 1984;Takahashi et al 1984). The two anatomically distinct cochlear nuclei, nucleus magnocellularis (NM) and nucleus angularis (NA), each receive information from the auditory nerve and specialize for encoding timing information (NM) and intensity, or sound level, information (NA) for the computation of sound location (Boord 1968;Carr and Boudreau 1991;Parks and Rubel 1978;Puelles et al 2007;Reyes et al 1994;Sullivan and Konishi 1984;Trussell 1999).…”

Section: Introductionmentioning

confidence: 99%

Heterogeneous Calretinin Expression in the Avian Cochlear Nucleus Angularis

Bloom

Williams

MacLeod

2014

JARO

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Multiple calcium-binding proteins (CaBPs) are expressed at high levels and in complementary patterns in the auditory pathways of birds, mammals, and other vertebrates, but whether specific members of the CaBP family can be used to identify neuronal subpopulations is unclear. We used double immunofluorescence labeling of calretinin (CR) in combination with neuronal markers to investigate the distribution of CR-expressing neurons in brainstem sections of the cochlear nucleus in the chicken (Gallus gallus domesticus). While CR was homogeneously expressed in cochlear nucleus magnocellularis, CR expression was highly heterogeneous in cochlear nucleus angularis (NA), a nucleus with diverse cell types analogous in function to neurons in the mammalian ventral cochlear nucleus. To quantify the distribution of CR in the total NA cell population, we used antibodies against neuronal nuclear protein (NeuN), a postmitotic neuronspecific nuclear marker. In NA neurons, NeuN label was variably localized to the cell nucleus and the cytoplasm, and the intensity of NeuN immunoreactivity was inversely correlated with the intensity of CR immunoreactivity. The percentage of CR+neurons in NA increased from 31 % in embryonic (E)17/18 chicks, to 44 % around hatching (E21), to 51 % in postnatal day (P) 8 chicks. By P8, the distribution of CR + neurons was uniform, both rostrocaudal and in the tonotopic (dorsoventral) axis.Immunoreactivity for the voltage-gated potassium ion channel Kv1.1, used as a marker for physiological type, showed broad and heterogeneous postsynaptic expression in NA, but did not correlate with CR expression. These results suggest that CR may define a subpopulation of neurons within nucleus angularis.

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Section: Introductionmentioning

confidence: 99%

Heterogeneous Calretinin Expression in the Avian Cochlear Nucleus Angularis

Bloom

Williams

MacLeod

2014

JARO

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“…Inasmuch as these terminals are perisomatic, they resemble the endbulb synapses in the avian NM and the mammalian AVCN, and the similarities suggest that they represent a homologous population corresponding to the NM of birds and turtles (Belekhova et al, 2008;Carr and Code, 2000;Grothe et al, 2005). Szpir et al (1990) labeled individual axons and noted larger axosomatic terminals in NMM than in the other first-order nuclei.…”

Section: Organization Of the First-order Nucleimentioning

confidence: 86%

“…The nucleus angularis projects to the superior olive, to the lemniscal nuclei, and to the central nucleus of the auditory midbrain. The parallel ascending projections of angularis and laminaris may or may not overlap with one another and probably do overlap in the primitive condition (for reviews see Carr, 1992;Carr and Code, 2000). The connections of the central auditory system are well known in mammals and follow a similar ascending trajectory (for reviews see Grothe et al, 2005;Rouiller, 1997).…”

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

“…The first-order nuclei of the lizard have been described as showing a great deal of interspecific variation (for reviews see Carr and Code, 2000;Manley, 1981). In many lizards, four nuclear populations that receive primary auditory inputs have been recognized: a medial and lateral nucleus magnocellularis and a medial and lateral angularis (Miller, Szpir et al, 1995).…”

Section: Organization Of the First-order Nucleimentioning

confidence: 99%

“…These findings are consistent with results from the alligator lizard (Szpir et al, 1990) and confirm Spzir et al's finding that two populations of auditory nerve fibers project to nonoverlapping first-order targets. Note that direct electrophysiological and anatomical evidence for the separation of the two nerve populations is presently lacking in gecko.The first-order nuclei of the lizard have been described as showing a great deal of interspecific variation (for reviews see Carr and Code, 2000;Manley, 1981). In many lizards, four nuclear populations that receive primary auditory inputs have been recognized: a medial and lateral nucleus magnocellularis and a medial and lateral angularis (Miller, Szpir et al, 1995).…”

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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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Comparative Psychology of Audition

Moss

Carr

2003

Handbook of Psychology

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Many animal species use sound to orient in the environment, detect predators, and communicate with conspecifics. Auditory systems have evolved to enable these behaviors, permitting the detection, localization, and discrimination of acoustic events. This chapter provides an overview of auditory systems and behavior in a variety of animal species, including insects, amphibians, birds, and mammals. Emphasizing a comparative and evolutionary perspective, the chapter details features of the auditory pathway—from the ear to central structures involved in the processing of acoustic stimuli. Anatomical pathways and physiological response characteristics of neurons at different stages of the auditory pathway are described. The chapter also reviews behavioral measures of auditory function, emphasizing studies of absolute hearing sensitivity, frequency selectivity, temporal resolution, sound localization, and scene analysis. Comparisons of auditory system anatomy, physiology, and function across species reveal exquisite specializations but also many common principles across the animal kingdom.

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The Central Auditory System of Reptiles and Birds

Cited by 62 publications

References 217 publications

Heterogeneous Calretinin Expression in the Avian Cochlear Nucleus Angularis

Heterogeneous Calretinin Expression in the Avian Cochlear Nucleus Angularis

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

Comparative Psychology of Audition

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