Development of Auditory Afferents to the Central Nucleus of the Inferior Colliculus

Brunso‐Bechtold, Judy K.; Henkel, Craig K.

doi:10.1007/0-387-27083-3_18

Cited by 8 publications

(8 citation statements)

References 98 publications

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“…Similar early development of afferent circuits in IC has been reported. For instance, LSO projections have formed a banded pattern in IC before hearing onset in both kittens and ferrets (Brunso-Bechtold and Henkel, 2005;Henkel et al, 2005) and DNLL projections are banded before hearing onset in rat as well (Gabriele et al, 2000b). In the present study, the disruption of a normal banded pattern of crossed DNLL axons in the IC of P12 rat following unilateral cochlear ablation on P9 is consistent with spontaneous activity in ascending auditory pathways being a critical factor in shaping the spatial arrangement of DNLL projections in IC.…”

Section: Activity-dependent Changes In Developing Circuitssupporting

confidence: 86%

“…Similarly, banded projections from LSO to the IC have been observed in kittens at birth (Brunso-Bechtold and Henkel, 2005;Henkel et al, 2005), several days before acoustically driven activity is present in the auditory midbrain (Moore and Irvine, 1979). Consequently, the timing of these events suggests that patterns of spontaneous activity or spatially distributed molecular guidance cues may well be vital for initial assembly and maintenance of integrative circuits in the IC.…”

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confidence: 78%

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Unilateral cochlear ablation before hearing onset disrupts the maintenance of dorsal nucleus of the lateral lemniscus projection patterns in the rat inferior colliculus

2006

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During postnatal development, ascending and descending auditory inputs converge to form fibrodendritic layers within the central nucleus of the inferior colliculus (IC). Before the onset of hearing, specific combinations of inputs segregate into bands separated by interband spaces. These bands may define functional zones within the IC. Previous studies in our laboratory have shown that unilateral or bilateral cochlear ablation at postnatal day 2 (P2) disrupts the development of afferent bands from the dorsal nucleus of the lateral lemniscus (DNLL) to the IC. These results suggest that spontaneous activity propagated from the cochlea is required for the segregation of afferent bands within the developing IC. To test if spontaneous activity from the cochlea also may be required to maintain segregated bands of DNLL input, we performed cochlear ablations in rat pups at P9, after DNLL bands already are established. All animals were killed at P12 and glass pins coated with carbocyanine dye, DiI (1,1′-dioctodecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate), subsequently were placed in the commissure of Probst to label the crossed projections from both DNLLs. When compared with surgical controls, experimental results showed a similar pattern of DNLL bands in the IC contralateral to the ablated cochlea, but a disruption of DNLL bands in the IC ipsilateral to the cochlear ablation. The present results suggest that cochlear ablation after DNLL bands have formed may affect the maintenance of banded DNLL projections within the central nucleus of the IC. KeywordsDNLL; DiI; development; afferent bands; GABA; deafferentation The central nucleus of the inferior colliculus (IC) is composed of a series of cochleotopically ordered layers that preserve frequency-specific processing of various auditory features. Multiple auditory nuclei target the IC and terminate in afferent compartments along these cochleotopic layers (Oliver and Shneiderman, 1989b). It is likely that these afferent compartments within the IC create an intrinsic organization capable of integrating inputs from different auditory nuclei (Oliver and Shneiderman, 1989a;Cant and Benson, 2006).A banded organization of afferent projections to the IC develops quite early, in fact, well before auditory experience could shape functioning synaptic circuits. For example, crossed projections from the dorsal nucleus of the lateral lemniscus (DNLL) to the central nucleus of the IC have organized into bands about one week before hearing onset in rat (Gabriele et al.,

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Section: Activity-dependent Changes In Developing Circuitssupporting

confidence: 86%

mentioning

confidence: 78%

Unilateral cochlear ablation before hearing onset disrupts the maintenance of dorsal nucleus of the lateral lemniscus projection patterns in the rat inferior colliculus

2006

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“…Coincident with shaping of topographic afferents along tonotopic IC dimensions (Brunso-Bechtold and Henkel, 2005), ephrin-B2 and EphA4 gradients span CNIC and LCIC Layer 3 frequency axes, with protein most concentrated in high-frequency domains. Inputs to more superficial aspects of the LCIC, however, are multimodal (Aitkin et al, 1981; Gruters and Groh, 2012) and discontinuous, exhibiting either discrete modular or extramodular terminal fields (Saldaña and Merchán, 1992; Saldaña et al, 1996; Shore and Zhou, 2006; Torii et al, 2013; Stebbings et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Graded and discontinuous EphA–ephrinB expression patterns in the developing auditory brainstem

et al. 2016

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Eph-ephrin interactions guide topographic mapping and pattern formation in a variety of systems. In contrast to other sensory pathways, their precise role in the assembly of central auditory circuits remains poorly understood. The auditory midbrain, or inferior colliculus (IC) is an intriguing structure for exploring guidance of patterned projections as adjacent subdivisions exhibit distinct organizational features. The central nucleus of the IC (CNIC) and deep aspects of its neighboring lateral cortex (LCIC, Layer 3) are tonotopically-organized and receive layered inputs from primarily downstream auditory sources. While less is known about more superficial aspects of the LCIC, its inputs are multimodal, lack a clear tonotopic order, and appear discontinuous, terminating in modular, patch/matrix-like distributions. Here we utilize X-Gal staining approaches in lacZ mutant mice (ephrin-B2, -B3, and EphA4) to reveal EphA-ephrinB expression patterns in the nascent IC during the period of projection shaping that precedes hearing onset. We also report early postnatal protein expression in the cochlear nuclei, the superior olivary complex, the nuclei of the lateral lemniscus, and relevant midline structures. Continuous ephrin-B2 and EphA4 expression gradients exist along frequency axes of the CNIC and LCIC Layer 3. In contrast, more superficial LCIC localization is not graded, but confined to a series of discrete ephrin-B2 and EphA4-positive Layer 2 modules. While heavily expressed in the midline, much of the auditory brainstem is devoid of ephrin-B3, including the CNIC, LCIC Layer 2 modular fields, the dorsal nucleus of the lateral lemniscus (DNLL), as well as much of the superior olivary complex and cochlear nuclei. Ephrin-B3 LCIC expression appears complementary to that of ephrin-B2 and EphA4, with protein most concentrated in presumptive extramodular zones. Described tonotopic gradients and seemingly complementary modular/extramodular patterns suggest Eph-ephrin guidance in establishing juxtaposed continuous and discrete neural maps in the developing IC prior to experience.

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“…Classic developmental events of neuronal birth, migration, circuit refinement and plasticity appear to be influenced significantly by both spontaneous and experience-dependent activity. These changes are dependent on calcium-mediated mechanisms (Brunso-Bechtold and Henkel, 2005). These calcium-mediated mechanisms in the neural signaling involve calcium-binding proteins, which identify the site of calcium-dependent activity.…”

Section: Introductionmentioning

confidence: 99%

Stereological investigation and expression of calcium-binding proteins in developing human inferior colliculus

Sharma

Nag

Wadhwa

et al. 2009

Journal of Chemical Neuroanatomy

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Development of Auditory Afferents to the Central Nucleus of the Inferior Colliculus

Cited by 8 publications

References 98 publications

Unilateral cochlear ablation before hearing onset disrupts the maintenance of dorsal nucleus of the lateral lemniscus projection patterns in the rat inferior colliculus

Unilateral cochlear ablation before hearing onset disrupts the maintenance of dorsal nucleus of the lateral lemniscus projection patterns in the rat inferior colliculus

Graded and discontinuous EphA–ephrinB expression patterns in the developing auditory brainstem

Stereological investigation and expression of calcium-binding proteins in developing human inferior colliculus

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