Ephrin‐B2 reverse signaling is required for topography but not pattern formation of lateral superior olivary inputs to the inferior colliculus

Wallace, Matthew M.; Kavianpour, Sarah M.; Gabriele, Mark L.

doi:10.1002/cne.23243

Cited by 13 publications

(24 citation statements)

References 59 publications

(98 reference statements)

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“…Bilateral LSO patterns and those arising from the contralateral DCN and dorsal nucleus of the lateral lemniscus (DNLL) all exhibit remarkable projection specificity prior to experience, targeting defined synaptic domains of frequency-band laminae (Fathke and Gabriele, 2009). Much like their layered counterparts in the CNIC, modular (Wallace et al, 2013) and extramodular (Torii et al, 2013) LCIC arrangements emerge during early postnatal development.…”

Section: Auditory Midbrainmentioning

confidence: 99%

“…To assess Eph/ephrin cues in establishing continuous CNIC and discrete LCIC maps, a recent study explored the specific involvement of ephrin-B2 in developing topographic projections from the LSO to IC (Wallace et al, 2013). In contrast to the strict tonotopy observed in wild type mice, ephrin-B2 lacZ /+ mutants (compromised reverse signaling) lacked any clear projection topography.…”

Section: Auditory Midbrainmentioning

confidence: 99%

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Axon guidance in the auditory system: Multiple functions of Eph receptors

Cramer

Gabriele

2014

Neuroscience

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The neural pathways of the auditory system underlie our ability to detect sounds and to transform amplitude and frequency information into rich and meaningful perception. While it shares some organizational features with other sensory systems, the auditory system has some unique functions that impose special demands on precision in circuit assembly. In particular, the cochlear epithelium creates a frequency map rather than a space map, and specialized pathways extract information on interaural time and intensity differences to permit sound source localization. The assembly of auditory circuitry requires the coordinated function of multiple molecular cues. Eph receptors and their ephrin ligands constitute a large family of axon guidance molecules with developmentally regulated expression throughout the auditory system. Functional studies of Eph/ephrin signaling have revealed important roles at multiple levels of the auditory pathway, from the cochlea to the auditory cortex. These proteins provide graded cues used in establishing tonotopically ordered connections between auditory areas, as well as discrete cues that enable axons to form connections with appropriate postsynaptic partners within a target area. Throughout the auditory system, Eph proteins help to establish patterning in neural pathways during early development. This early targeting, which is further refined with neuronal activity, establishes the precision needed for auditory perception.

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Section: Auditory Midbrainmentioning

confidence: 99%

Section: Auditory Midbrainmentioning

confidence: 99%

Axon guidance in the auditory system: Multiple functions of Eph receptors

Cramer

Gabriele

2014

Neuroscience

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“…The Eph receptors and their ligands, the ephrins, play a strong role in the development of the auditory system in mice by patterning the tonotopic structure from the auditory periphery to the brainstem and up to the auditory cortex [1–3]. Eph-ephrin interactions involve two subfamilies: As and Bs.…”

Section: Introductionmentioning

confidence: 99%

“…The mouse organ of Corti and spiral ganglion cells have strong expression of EphA4, EphB1, B2, B3, ephrin-A2, -A5, and ephrin-B1, -B2 [7–9]. Recent findings underscore the importance of Eph-ephrin signaling in the mammalian inferior colliculus (IC) prior to hearing onset [3, 10]. Graded and modular expression patterns of EphA4 and ephrin-B2 correlate with developing projections to various IC subdivisions, suggesting their involvement in guiding tonotopic and patterned arrangements in the mouse midbrain [10].…”

Section: Introductionmentioning

confidence: 99%

“…Graded and modular expression patterns of EphA4 and ephrin-B2 correlate with developing projections to various IC subdivisions, suggesting their involvement in guiding tonotopic and patterned arrangements in the mouse midbrain [10]. Furthermore, accurate topographic mapping of terminal fields from the lateral superior olive to the IC is lost in ephrin-B2 mutants with compromised signaling [3]. Given the involvement of these subcortical auditory circuits in the ASR and the influences of Eph-ephrins on their development and organization, we hypothesize that Eph-ephrin mutants will display altered pre-pulse inhibition (PPI) when compared to controls and wild-types (WTs).…”

Section: Introductionmentioning

confidence: 99%

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The effects of Eph–ephrin mutations on pre-pulse inhibition in mice

Liuzzo

Gray

Wallace

et al. 2014

Physiology & Behavior

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Eph-ephrin signaling is known to be important in directing topographic projections in the afferent auditory pathway, including connections to various subdivisions of the inferior colliculus (IC). The acoustic startle-response (ASR) is a reliable reflexive behavioral response in mammals elicited by an unexpected intense acoustic startle-eliciting stimulus (ES). It is mediated by a sub-cortical pathway that includes the IC. The ASR amplitude can be measured with an accelerometer under the subject and can be decreased in amplitude by presenting a less intense, non-startling stimulus 5–300 ms before the ES. This reflexive decrement in ASR is called pre-pulse inhibition (PPI) and indicates that the relatively soft pre-pulse was heard. PPI is a general trait among mammals. Mice have been used recently to study this response and to reveal how genetic mutations affect neural circuits and hence the ASR and PPI. In this experiment, we measured the effect of Eph-ephrin mutations using control mice (C57BL/6J), mice with compromised EphA4 signaling (EphA4lacZ/+, EphA4lacZ/lacZ), and knockout ephrin-B3 mice (ephrin-B3 +/−, −/−). Control and EphA4lacZ/+ strains showed robust PPI (up to 75% decrement in ASR) to an offset of a 70 dB SPL background noise at 50 ms before the ES. Ephrin-B3 knockout mice and EphA4 homozygous mutants were only marginally significant in PPI (< 25% decrement and <33% decrement, respectively) to the same conditions. This decrement in PPI highlights the importance of ephrin-B3 and EphA4 interactions in ordering auditory behavioral circuits. Thus, different mutations in certain members of the signaling family produce a full range of changes in PPI, from minimal to nearly maximal. This technique can be easily adapted to study other aspects of hearing in a wider range of mutations. Along with ongoing neuroanatomical studies, this allows careful quantification of how the auditory anatomical, physiological and now behavioral phenotype is affected by changes in Eph-ephrin expression and functionality.

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Modular‐extramodular organization in developing multisensory shell regions of the mouse inferior colliculus

Dillingham

Behrooz

Gabriele

2017

J of Comparative Neurology

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The complex neuroanatomical connections of the inferior colliculus (IC) and its major subdivisions offer a juxtaposition of segregated processing streams with distinct organizational features. While the tonotopically layered central nucleus is well-documented, less is known about functional compartments in the neighboring lateral cortex (LCIC). In addition to a laminar framework, LCIC afferent-efferent patterns suggest a multimodal mosaic, consisting of a patchy modular network with surrounding extramodular domains. This study utilizes several neurochemical markers that reveal an emerging LCIC modular-extramodular microarchitecture. In newborn and post-hearing C57BL/6J and CBA/CaJ mice, histochemical and immunocytochemical stains were performed for acetylcholinesterase (AChE), nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d), glutamic acid decarboxylase (GAD), cytochrome oxidase (CO), and calretinin (CR). Discontinuous layer 2 modules are positive for AChE, NADPH-d, GAD, and CO throughout the rostrocaudal LCIC. While not readily apparent at birth, discrete cell clusters emerge over the first postnatal week, yielding an identifiable modular network prior to hearing onset. Modular boundaries continue to become increasingly distinct with age, as surrounding extramodular fields remain largely negative for each marker. Alignment of modular markers in serial sections suggests each highlight the same periodic patchy network throughout the nascent LCIC. In contrast, CR patterns appear complementary, preferentially staining extramodular LCIC zones. Double-labeling experiments confirm that NADPH-d, the most consistent developmental modular marker, and CR label separate, nonoverlapping LCIC compartments. Determining how this emerging modularity may align with similar LCIC patch-matrix-like Eph/ephrin guidance patterns, and how each interface with, and potentially influence developing multimodal LCIC projection configurations is discussed.

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Ephrin‐B2 reverse signaling is required for topography but not pattern formation of lateral superior olivary inputs to the inferior colliculus

Cited by 13 publications

References 59 publications

Axon guidance in the auditory system: Multiple functions of Eph receptors

Axon guidance in the auditory system: Multiple functions of Eph receptors

The effects of Eph–ephrin mutations on pre-pulse inhibition in mice

Modular‐extramodular organization in developing multisensory shell regions of the mouse inferior colliculus

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