Skip to main content

Development and Function of Inhibitory Circuitry in the Avian Auditory Brainstem

  • Chapter
  • First Online:
Auditory Development and Plasticity

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 64))

  • 842 Accesses

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Code, R. A., & Rubel, E. W. (1989). Glycine-immunoreactivity in the auditory brain stem of the chick. Hearing Research, 40, 67–172.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Darrow, K. N., Maison, S. F., & Liberman, M. C. (2006). Cochlear efferent feedback balances interaural sensitivity. Nature Neuroscience, 9, 1474–1476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Gillespie, D. C., Kim, G., & Kandler, K. (2005). Inhibitory synapses in the developing auditory system are glutamatergic. Nature Neuroscience, 8, 332–338.

    Article  CAS  PubMed  Google Scholar 

  • Grothe, B., Pecka, M., & McAlpine, D. (2010). Mechanisms of sound localization in mammals. Physiological Reviews, 90, 983–1012.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Köppl, C., & Carr, C. E. (2003). Computational diversity in the cochlear nucleus angularis of the barn owl. Journal of Neurophysiology, 89, 2313–2329.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Lippe, W. R. (1994) Rhythmic spontaneous activity in the developing avian auditory system. The Journal of Neuroscience, 14, 1486–1495.

    CAS  PubMed  Google Scholar 

  • Lu, T., & Trussell, L. O. (2000). Inhibitory transmission mediated by asynchronous transmitter release. Neuron, 26, 683–694.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Monsivais, P., & Rubel, E. W. (2001). Accommodation enhances depolarizing inhibition in central neurons. The Journal of Neuroscience, 21, 7823–7830.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Represa, A., & Ben-Ari, Y. (2005). Trophic actions of GABA on neuronal development. Trends in Neuroscience, 6, 278–283.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubel, E. W., & Fritzsch, B. (2002). Auditory system development: Primary auditory neurons and their targets. Annual Review of Neuroscience, 25, 51–101.

    Article  CAS  PubMed  Google Scholar 

  • Seidl, A. H., Rubel, E. W., & Barría, A. (2014). Differential conduction velocity regulation in ipsilateral and contralateral collaterals innervating brainstem coincidence detector neurons. The Journal of Neuroscience, 34, 4914–4919.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

Download references

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.

Compliance with Ethics Requirements

R. Michael Burger declares that he has no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Michael Burger .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

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

Download citation

Publish with us

Policies and ethics