Abstract
The avian auditory system has provided an excellent model circuit to explore important features of acoustic processing. For example, in the chicken (Gallus gallus) system, in 1975 Parks and Rubel first confirmed the coincidence detection based delay line model of sound localization in vertebrates that was originally proposed by Jeffress in 1948. Further, the system provides an unmatched experimental substrate to investigate cellular physiology and morphology in light of computational function. Many anatomical and physiologically specialized features of auditory neurons have been identified first in birds, and often complementary properties are observed in mammals. These discoveries have contributed substantially to our general understanding of processing of acoustic signals, and the function of inhibition specifically. However, many mechanistic features of inhibitory physiology in the avian system contrast sharply with those of mammals, while achieving similar computational outcomes. This chapter reviews the major progress made toward understanding inhibitory roles in auditory function with a focus on three areas: (1) development of inhibitory circuitry, (2) functional organization of the inhibitory network, and (3) synaptic physiology of inhibition in birds. Although many specific mechanisms of inhibition in birds differ from those of mammals, these circuits exhibit remarkable convergence when viewed from a functional perspective.
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References
Apostolides, P. F., & Trussell, L. O. (2013). Rapid, activity-independent turnover of vesicular transmitter content at a mixed glycine/GABA synapse. The Journal of Neuroscience, 33, 4768–4781.
Burger, R. M., & Rubel, E. W. (2008). Encoding of interaural timing for binaural hearing. In A. I. Baasbaum, A. Kaneko, G. M. Shepherd, G. Westheimer, et al. (Eds.), The senses: A comprehensive reference, Vol. 3: Audition (pp. 613–630). San Diego: Academic Press.
Burger, R. M., Cramer, K. S., Pfeiffer, J. D., & Rubel, E. W. (2005). The avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways. The Journal of Comparative Neurology, 481, 6–18.
Burger, R. M., Fukui, I., Ohmori, H., & Rubel, E. W. (2011). Inhibition in the balance: Binaurally coupled inhibitory feedback in sound localization circuitry. Journal of Neurophysiology, 106, 4–14.
Carr, C. E., & Konishi, M. (1990). A circuit for detection of interaural time differences in the brain stem of the barn owl. The Journal of Neuroscience, 10, 3227–3246.
Carr, C. E., Fujita, I., & Konishi, M. (1989). Distribution of GABAergic neurons and terminals in the auditory system of the barn owl. The Journal of Comparative Neurology, 286,190–207.
Code, R. A., & Rubel, E. W. (1989). Glycine-immunoreactivity in the auditory brain stem of the chick. Hearing Research, 40, 67–172.
Code, R. A., Burd, G. D., & Rubel, E. W. (1989). Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: Ontogeny of gradients in terminal staining. The Journal of Comparative Neurology, 284, 504–518.
Colburn, H. S. (1996). Computational models of binaural processing. In Hawkins, H. L., McMullen, T., Popper, A. N., & Fay, R. R. (Eds.), Auditory computation (pp. 332–400). New York: Springer-Verlag.
Coleman, W. L., Fischl, M. J., Weimann, S. R., & Burger, R. M. (2011). GABAergic and glycinergic inhibition modulate monaural auditory response properties in the avian superior olivary nucleus. Journal of Neurophysiology, 105, 2405–2420.
Cramer, K. S., Fraser, S. E., & Rubel, E. W. (2000). Embryonic origins of auditory brain-stem nuclei in the chick hindbrain. Developmental Biology, 224, 138–151.
Darrow, K. N., Maison, S. F., & Liberman, M. C. (2006). Cochlear efferent feedback balances interaural sensitivity. Nature Neuroscience, 9, 1474–1476.
Dasika, V. K., White, J. A., Carney, L. H., & Colburn, H. S. (2005). Effects of inhibitory feedback in a network model of avian brain stem. Journal of Neurophysiology, 94, 400–414.
Fischl, M. J., & Burger, R. M. (2014). Glycinergic transmission modulates GABAergic inhibition in the avian auditory pathway. Frontiers in Neural Circuits, doi:10.3389/fncir.2014.00019.
Fischl, M. J., Weimann, S. R., Kearse, M., & Burger, R. M. (2014). Slowly emerging glycinergic transmission enhances inhibition in the sound localization pathway of the avian auditory system. Journal of Neurophysiology, 111, 565–572.
Fukui, I., Sato, T., & Ohmori, H. (2006). Improvement of phase information at low sound frequency in nucleus magnocellularis of the chicken. Journal of Neurophysiology, 96, 633–641.
Fukui, I., Burger, R. M., Ohmori, H., & Rubel, E. W. (2010). GABAergic inhibition sharpens the frequency tuning and enhances phase locking in chicken nucleus magnocellularis neurons. The Journal of Neuroscience, 30, 12075–12083.
Ge, S., Goh, E. L., Sailor, K. A., Kitabatake, Y., et al. (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature, 439(7076), 589–593.
Gillespie, D. C., Kim, G., & Kandler, K. (2005). Inhibitory synapses in the developing auditory system are glutamatergic. Nature Neuroscience, 8, 332–338.
Grothe, B., Pecka, M., & McAlpine, D. (2010). Mechanisms of sound localization in mammals. Physiological Reviews, 90, 983–1012.
Hackett, J. T., Jackson, H., & Rubel, E. W. (1982). Synaptic excitation of the second and third order auditory neurons in the avian brain stem. Neuroscience, 7, 1455–1469.
Howard, M. A., & Rubel, E. W. (2010). Dynamic spike thresholds during synaptic integration preserve and enhance temporal response properties in the avian cochlear nucleus. The Journal of Neuroscience, 30, 12063–12074.
Howard, M. A., Burger, R. M., & Rubel, E. W. (2007). A developmental switch from GABAergic excitation to inhibition controlled by K+ conductances. The Journal of Neuroscience, 27, 2112–2123.
Hyson, R. L., Reyes, A. D., & Rubel, E. W. (1995). A depolarizing inhibitory response to GABA in brainstem auditory neurons of the chick. Brain Research, 677, 117–126.
Jackson, H., Hackett, J. T., & Rubel, E. W. (1982). Organization and development of brain stem auditory nuclei in the chick: Ontogeny of postsynaptic responses. The Journal of Comparative Neurology, 210, 80–86.
Jhaveri, S., & Morest, D. K. (1982). Sequential alterations of neuronal architecture in nucleus magnocellularis of the developing chicken: A Golgi study. Neuroscience, 7, 837–853.
Kandler, K., & Friauf, E. (1995). Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. The Journal of Neuroscience, 15, 6890–6904.
Köppl, C., & Carr, C. E. (2003). Computational diversity in the cochlear nucleus angularis of the barn owl. Journal of Neurophysiology, 89, 2313–2329.
Kopp-Scheinpflug, C., Dehmel, S., Dörrscheidt, G. J., & Rübsamen, R. (2002). Interaction of excitation and inhibition in anteroventral cochlear nucleus neurons that receive large endbulb synaptic endings. The Journal of Neuroscience, 22, 11004–11018.
Korn, M. J., Koppel, S. J., Li, L. H., Mehta, D., et al. (2012). Astrocyte-secreted factors modulate the developmental distribution of inhibitory synapses in nucleus laminaris of the avian auditory brainstem. The Journal of Comparative Neurology, 520, 1262–1277.
Lachica, E. A., Rübsamen, R., & Rubel, E. W. (1994). GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus. The Journal of Comparative Neurology, 348, 403–418.
Lippe, W. R. (1994) Rhythmic spontaneous activity in the developing avian auditory system. The Journal of Neuroscience, 14, 1486–1495.
Lu, T., & Trussell, L. O. (2000). Inhibitory transmission mediated by asynchronous transmitter release. Neuron, 26, 683–694.
Lu, T., & Trussell, L. O. (2001). Mixed excitatory and inhibitory GABA-mediated transmission in chick cochlear nucleus. The Journal of Physiology (London), 535, 125–131.
Moiseff, A., & Konishi, M. (1983). Binaural characteristics of units in the owl’s brainstem auditory pathway: Precursors of restricted spatial receptive fields. The Journal of Neuroscience, 3, 2553–2562.
Molea, D., & Rubel, E. W. (2003). Timing and topography of nucleus magnocellularis innervation by the cochlear ganglion. The Journal of Comparative Neurology, 466, 557–591.
Monsivais, P., & Rubel, E. W. (2001). Accommodation enhances depolarizing inhibition in central neurons. The Journal of Neuroscience, 21, 7823–7830.
Monsivais, P., Yang, L., & Rubel, E. W. (2000). GABAergic inhibition in nucleus magnocellularis: Implications for phase locking in the avian auditory brainstem. The Journal of Neuroscience, 20, 2954–2963.
Nabekura, J., Katsurabayashi, S., Kakazu, Y., Shibata, S., et al. (2004). Developmental switch from GABA to glycine release in single central synaptic terminals. Nature Neuroscience, 7, 17–23.
Nerlich, J., Kuenzel, T., Keine, C., Korenic, A., et al. (2014a). Dynamic fidelity control to the central auditory system: Synergistic glycine/GABAergic inhibition in the cochlear nucleus. The Journal of Neuroscience, 34, 11604–11620.
Nerlich, J., Keine, C., Rübsamen, R., Burger, R. M., & Milenkovic, I. (2014b). Activity-dependent modulation of inhibitory synaptic kinetics in the cochlear nucleus. Frontiers in Neural Circuits, doi:10.3389/fncir.2014.00145.
Nishino, E., Yamada, R., Kuba, H., Hioki, H., et al. (2008). Sound-intensity-dependent compensation for the small interaural time difference cue for sound source localization. The Journal of Neuroscience, 28, 7153–7164.
Oline, S. N., & Burger, R. M. (2014). Short-term synaptic depression is topographically distributed in the cochlear nucleus of the chicken. The Journal of Neuroscience, 34, 1314–1324.
Oline, S. N., Ashida, G., & Burger, R. M. (2016). Tonotopic optimization for temporal processing in the cochlear nucleus. The Journal of Neuroscience, 36, 8500–8515.
Overholt, E. M., Rubel, E. W., & Hyson, R. L. (1992). A circuit for coding interaural time differences in the chick brainstem. The Journal of Neuroscience, 12, 1698–1708.
Parks, T. N., & Rubel, E. W. (1975). Organization and development of brain stem auditory nuclei of the chicken: Organization of projections from n. magnocellularis to n. laminaris. The Journal of Comparative Neurology, 164, 435–448.
Peña, J. L., Viete, S., Albeck, Y., & Konishi, M. (1996). Tolerance to sound intensity of binaural coincidence detection in the nucleus laminaris of the owl. The Journal of Neuroscience, 16, 7046–7054.
Represa, A., & Ben-Ari, Y. (2005). Trophic actions of GABA on neuronal development. Trends in Neuroscience, 6, 278–283.
Roberts, M. T., Seeman, S. C., & Golding, N. L. (2013). A mechanistic understanding of the role of feedforward inhibition in the mammalian sound localization circuitry. Neuron, 78, 923–935.
Rubel, E. W., & Fritzsch, B. (2002). Auditory system development: Primary auditory neurons and their targets. Annual Review of Neuroscience, 25, 51–101.
Seidl, A. H., Rubel, E. W., & BarrÃa, A. (2014). Differential conduction velocity regulation in ipsilateral and contralateral collaterals innervating brainstem coincidence detector neurons. The Journal of Neuroscience, 34, 4914–4919.
Soares, D., Chitwood, R. A., Hyson, R. L., & Carr, C. E. (2002). Intrinsic neuronal properties of the chick nucleus angularis. Journal of Neurophysiology, 88, 152–162.
Tabor, K., Coleman, W. L., Rubel, E. W., & Burger, R. M. (2012). Tonotopic organization of the superior olivary nucleus in the chicken (Gallus gallus). The Journal of Comparative Neurology, 520, 1493–1508.
Tang, Z. Q., & Lu, Y. (2012). Two GABAA responses with distinct kinetics in a sound localization circuit. The Journal of Physiology (London), 590, 3787–3805.
von Bartheld, C. S., Code, R. A., & Rubel, E. W. (1989). GABAergic neurons in brainstem auditory nuclei of the chick: Distribution, morphology, and connectivity. The Journal of Comparative Neurology, 287, 470–483.
Wojcik, S. M., Katsurabayashi, S., Guillemin, I., Friauf, E., et al. (2006). A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron, 50(4), 575–587.
Yamada, R., Okuda, H., Kuba, H., Nishino, E., et al. (2013). The cooperation of sustained and phasic inhibitions increases the contrast of ITD-tuning in low-frequency neurons of the chick nucleus laminaris. The Journal of Neuroscience, 33, 3927–3938.
Yang, L., Monsivais, P., & Rubel, E. W. (1999). The superior olivary nucleus and its influence on nucleus laminaris: A source of inhibitory feedback for coincidence detection in the avian auditory brainstem. The Journal of Neuroscience, 19, 2313–2325.
Young, S. R., & Rubel, E. W. (1983). Frequency-specific projections of individual neurons in chick brainstem auditory nuclei. The Journal of Neuroscience, 3, 1373–1378.
Acknowledgments
Above all, I would like to thank my mentor and friend, Ed Rubel. Thank you for demonstrating high expectations, while never losing sight of science as a joyful pursuit. I would also like to thank the many colleagues who have contributed the work referenced in this chapter for continuing to inspire my own.
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R. Michael Burger declares that he has no conflict of interest.
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Burger, R.M. (2017). Development and Function of Inhibitory Circuitry in the Avian Auditory Brainstem. In: Cramer, K., Coffin, A., Fay, R., Popper, A. (eds) Auditory Development and Plasticity. Springer Handbook of Auditory Research, vol 64. Springer, Cham. https://doi.org/10.1007/978-3-319-21530-3_5
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