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      Talking back: Development of the olivocochlear efferent system

      1 , 1
      Wiley Interdisciplinary Reviews: Developmental Biology
      Wiley

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          Abstract

          <p class="first" id="P1">Developing sensory systems must coordinate the growth of neural circuitry spanning from receptors in the peripheral nervous system (PNS) to multi-layered networks within the central nervous system (CNS). This breadth presents particular challenges, as nascent processes must navigate across the CNS-PNS boundary and coalesce into a tightly intermingled wiring pattern, thereby enabling reliable integration from the PNS to the CNS and back. In the auditory system, feedforward spiral ganglion neurons (SGNs) from the periphery collect sound information via tonotopically organized connections in the cochlea and transmit this information to the brainstem for processing via the VIII <sup>th</sup> cranial nerve. In turn, feedback olivocochlear neurons (OCNs) housed in the auditory brainstem send projections into the periphery, also through the VIII <sup>th</sup> nerve. OCNs are motor neuron-like efferent cells that influence auditory processing within the cochlea and protect against noise damage in adult animals. These aligned feedforward and feedback systems develop in parallel, with SGN central axons reaching the developing auditory brainstem around the same time that the OCN axons extend out towards the developing inner ear. Recent findings have begun to unravel the genetic and molecular mechanisms that guide OCN development, from their origins in a generic pool of motor neuron precursors to their specialized roles as modulators of cochlear activity. One recurrent theme is the importance of efferent-afferent interactions, as afferent SGNs guide OCNs to their final locations within the sensory epithelium, and efferent OCNs shape the activity of the developing auditory system. </p><p id="P2">Inner ear efferents (IEEs) provide feedback to the inner ear. Originating with facial branchial motor neurons (FBMNs) from a pool of MNv progenitors in the brainstem, IEE precursors produce olivocochlear neurons (OCNs) and vestibular efferent neurons (VENs). In the cochlea, OCN axons project along spiral ganglion neuron (SGN) afferent processes. </p><p id="P3"> <div class="figure-container so-text-align-c"> <img alt="" class="figure" src="/document_file/cf02f5b3-65dc-4dad-84df-ebdb4f0d6bf1/PubMedCentral/image/nihms971444u1.jpg"/> </div> </p>

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          Mechanisms underlying spontaneous patterned activity in developing neural circuits.

          Patterned, spontaneous activity occurs in many developing neural circuits, including the retina, the cochlea, the spinal cord, the cerebellum and the hippocampus, where it provides signals that are important for the development of neurons and their connections. Despite there being differences in adult architecture and output across these various circuits, the patterns of spontaneous network activity and the mechanisms that generate it are remarkably similar. The mechanisms can include a depolarizing action of GABA (gamma-aminobutyric acid), transient synaptic connections, extrasynaptic transmission, gap junction coupling and the presence of pacemaker-like neurons. Interestingly, spontaneous activity is robust; if one element of a circuit is disrupted another will generate similar activity. This research suggests that developing neural circuits exhibit transient and tunable features that maintain a source of correlated activity during crucial stages of development.
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            Auditory-nerve response from cats raised in a low-noise chamber.

            A litter of four cats, born and raised in a soundproofed chamber, was studied in an attempt to determine which, if any, features of the auditory-nerve response from routinely available cats might be due to the chronic effects of noise exposure. Two features of routine-normal response were especially suspect in this regard: (1) a "notch" in the distribution of single-unit thresholds centered at characteristic frequencies (CF's) near 3 kHz and (2) a compression of the distribution of rates of spontaneous discharge for units with CF above 10 kHz. A third feature of response in routine animals was the presence of a small number (roughly 10%) of units with virtually no spontaneous discharge and very high thresholds, sometimes 80 dB less sensitive than high-spontaneous units of similar CF. In the data from chamber-raised animals, the high-spontaneous units showed exceptionally low thresholds at all CF regions, however, there were signs of the midfrequency notch in the threshold distribution of at least two of these animals. The compression of the spontaneous rate distribution was not seen in any of the three most sensitive animals. The data suggest that there is a significant amount of "normal pathology" in the high-CF units from routine animals. Low-spontaneous, high-threshold units were present in all four chamber-raised ears with the same characteristics as in routine animals (exceptionally narrow tuning curves and exceptionally low maximum discharge rates) and at roughly the same percentage of the unit sample. A class of units with medium spontaneous rates and intermediate thresholds could also be identified. The possible significance of a classification of auditory-nerve units according to spontaneous rate is discussed.
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              Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling.

              Distinct classes of motor neurons and ventral interneurons are generated by the graded signaling activity of Sonic hedgehog (Shh). Shh controls neuronal fate by establishing different progenitor cell populations in the ventral neural tube that are defined by the expression of Pax6 and Nkx2.2. Pax6 establishes distinct ventral progenitor cell populations and controls the identity of motor neurons and ventral interneurons, mediating graded Shh signaling in the ventral spinal cord and hindbrain.
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                Author and article information

                Journal
                Wiley Interdisciplinary Reviews: Developmental Biology
                WIREs Dev Biol
                Wiley
                17597684
                November 2018
                November 2018
                June 26 2018
                : 7
                : 6
                : e324
                Affiliations
                [1 ]Department of Neurobiology; Harvard Medical School; Boston Massachusetts
                Article
                10.1002/wdev.324
                6185769
                29944783
                e6d2e0e1-1a5c-4db0-80c0-ed205087af60
                © 2018

                http://doi.wiley.com/10.1002/tdm_license_1.1

                http://onlinelibrary.wiley.com/termsAndConditions#vor

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