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Need for Speed and Precision: Structural and Functional Specialization in the Cochlear Nucleus of the Avian Auditory System

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Birds such as the barn owl and zebra finch are known for their remarkable hearing abilities that are critical for survival, communication and vocal learning functions. A key to achieving these hearing abilities is the speed and precision required for the temporal coding of sound; a process heavily dependent on the structural, synaptic and intrinsic specializations in the avian auditory brainstem. This dissertation focuses on the specialization of neurons in the chicken cochlear nucleus magnocellularis (NM), – a first order auditory brainstem structure analogous to bushy cells in the mammalian anteroventral cochlear nucleus. Similar to their mammalian counterpart, previous studies have shown that NM neurons are mostly adendritic and receive auditory nerve input through large axosomatic endbulb of Held synapses. Axonal projections from NM neurons to their downstream auditory targets are sophisticatedly programmed regarding their length, caliber, myelination and conduction velocity. The first major section of my dissertation documented the functional phenotype of NM neurons that are located in the mid- to high-frequency regions, and investigated their underlying ion channel properties. These NM neurons generate extremely fast and precise action potentials that are able to follow high-frequency inputs with good fidelity. One specific aim of this dissertation was to address open questions regarding the functional role and development of voltage dependent potassium and sodium channels in NM neurons. Using experimental and computational methods, I found that specialized voltage dependent potassium and sodium channel properties play important and unique roles in shaping the observed phenotype of NM neurons. Working synergistically with potassium channels, an atypical current known as resurgent sodium current also promotes rapid and precise action potential firing for NM neurons. Despite a handful of reports of resurgent sodium current in the mammalian auditory structures, my research is the first evidence that showed the presence of this current in the avian auditory system, suggesting a hearing principle shared across mammals and birds. In addition, the development of potassium and sodium channels was characterized regarding the onset of hearing. Interestingly, the aforementioned structural and functional specializations vary dramatically along the tonotopic axis. The second major section of my dissertation focused on the low-frequency NM (termed NMc) neurons that display extensive dendrites. Compared to adendritic, higher-frequency NM neurons, NMc neurons are largely unexplored. Therefore, another specific aim of this dissertation was to characterize the novel structural properties of NMc neurons in chickens. I found that NMc neurons receive auditory nerve input via small bouton synapses onto their dendrites, contain two subtypes with different morphology and express a variety of calcium binding proteins and neuropeptides. NMc neurons generate slower and less reliable action potentials and are most responsive to low-frequency inputs, likely due to differences in ion channel mechanisms. These functional properties of NMc neurons are in stark contrast to the speed and precision required by their higher-frequency counterparts. As such, another specific aim of this dissertation was to determine the underlying ion channel mechanisms that give rise to the NMc functional phenotype. Indeed, NMc neurons exhibit distinct properties of voltage dependent potassium and sodium channels, including resurgent sodium current. These observations suggest a plethora of encoding strategies for sounds of different acoustic frequencies, mechanisms likely shared across species.

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