Skip to main content

Modulatory Mechanisms Controlling Auditory Processing

  • Chapter
  • First Online:
Synaptic Mechanisms in the Auditory System

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 41))

Abstract

The importance of neuromodulation for auditory processing is, essentially, that “tone” matters. The tone of a message can carry as much information as the ­message itself, and clearly there are parallels in everyday experience as illustrated by the above quote. In the brain, the tone of auditory processing is determined by neural systems that also contribute to changes in behavioral state, such as arousal and attention. The extent to which these changes involve neuromodulation depends, at least in part, on how one defines the term. Yet the end result – setting the tone of a message – is fundamental to auditory function. The goals of this chapter is to explain what neuromodulation is (hint: it depends on who you’re talking to) and to describe some of its mechanisms and how they affect neural processing. To illustrate the main points, examples of neural processing focus on the auditory system where possible, and examples of neuromodulation focus on cholinergic modulation of auditory processing.

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 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
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

  • Bakin, J. S., & Weinberger, N. M. (1996). Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proceedings of the National Academy of Sciences of the United States of America, 93, 11219–11224.

    Article  PubMed  CAS  Google Scholar 

  • Barrera, N. P., & Edwardson, J. M. (2008). The subunit arrangement and assembly of ionotropic receptors. Trends in Neurosciences, 31(11), 569–576.

    Article  PubMed  CAS  Google Scholar 

  • Baskerville, K. A., Chang, H. T., & Herron, P. (1993). Topography of cholinergic afferents from the nucleus basalis of Meynert to representational areas of sensorimotor cortices in the rat. Journal of Comparative Neurology, 335, 552–562.

    Article  PubMed  CAS  Google Scholar 

  • Bear, M. F., Connors, B. W., & Paradiso, M. A. (2007). Neuroscience: Exploring the brain (3 rd ed.). Philadelphia, PA: Lippincott Williams & Wilkins.

    Google Scholar 

  • Berg, D. K., Conroy, W. G., Liu, Z., & Zago, W. M. (2006). Nicotinic signal transduction machinery. Journal of Molecular Neuroscience, 30(1–2), 149–152.

    Article  PubMed  CAS  Google Scholar 

  • Broide, R. S., & Leslie, F. M. (1999). The alpha7 nicotinic acetylcholine receptor in neuronal plasticity. Molecular Neurobiology, 20(1), 1–16.

    Article  PubMed  CAS  Google Scholar 

  • Chen, G., & Yan, J. (2007). Cholinergic modulation incorporated with a tone presentation induces frequency-specific threshold decreases in the auditory cortex of the mouse. European Journal of Neuroscience, 25(6), 1793–1803.

    Article  PubMed  Google Scholar 

  • Cull-Candy, S., Brickley, S., & Farrant, M. (2001). NMDA receptor subunits: Diversity, development and disease. Current Opinion in Neurobiology, 11(3), 327–335.

    Article  PubMed  CAS  Google Scholar 

  • Descarries, L., & Mechawar, N. (2000). Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central nervous system. Progress in Brain Research, 125, 27–47.

    Article  PubMed  CAS  Google Scholar 

  • Diamond, D. M., & Weinberger, N. M. (1989). Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. Behavioral Neuroscience, 103, 471–494.

    Article  PubMed  CAS  Google Scholar 

  • Edeline, J.-M. (2003). The thalamo-cortical auditory receptive fields: Regulation by the states of vigilance, learning and the neuromodulatory systems. Experimental Brain Research, 153(4), 554–572.

    Article  Google Scholar 

  • Edeline, J.-M., Hars, B., Maho, C., & Hennevin, E. (1994). Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. Experimental Brain Research, 97, 373–386.

    Article  CAS  Google Scholar 

  • Edeline, J.-M., Manunta, Y., & Hennevin, E. (2000). Auditory thalamus neurons during sleep: Changes in frequency selectivity, threshold, and receptive field size. Journal of Neurophysiology, 84(2), 934–952.

    PubMed  CAS  Google Scholar 

  • Fritz, J., Shamma, S., Elhilali, M., & Klein, D. (2003). Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nature Neuroscience, 6(11), 1216–1223.

    Article  PubMed  CAS  Google Scholar 

  • Froemke, R. C., Merzenich, M. M., & Schreiner, C. E. (2007). A synaptic memory trace for cortical receptive field plasticity. Nature, 450(7168), 425–429.

    Article  PubMed  CAS  Google Scholar 

  • Gill, D. L., Spassova, M. A., & Soboloff, J. (2006). Signal transduction: Calcium entry signals – trickles and torrents. Science, 313(5784), 183–184.

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Peon, R., Scherrer, H., & Jouvet, M. (1956). Modification of electric activity in cochlear nucleus during attention in unanesthetized cats. Science, 123(3191), 331–332.

    Article  PubMed  CAS  Google Scholar 

  • Kaczmarek, L. K., & Levitan, I. B. (Eds.). (1987). Neuromodulation. New York: Oxford University Press.

    Google Scholar 

  • Kilgard, M. P., & Merzenich, M. M. (1998). Cortical map reorganization enabled by nucleus basalis activity. Science, 279, 1714–1718.

    Article  PubMed  CAS  Google Scholar 

  • Livingstone, M. S., & Hubel, D. H. (1981). Effects of sleep and arousal on the processing of visual information in the cat. Nature, 291, 554–561.

    Article  PubMed  CAS  Google Scholar 

  • McCormick, D. A., & Feeser, H. R. (1990). Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience, 39, 103–113.

    Article  PubMed  CAS  Google Scholar 

  • McCormick, D. A., & Prince, D. A. (1986). Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. Nature, 319, 402–405.

    Article  PubMed  CAS  Google Scholar 

  • McGaugh, J. L. (2000). Memory – a century of consolidation. Science, 287(5451), 248–251.

    Article  PubMed  CAS  Google Scholar 

  • Mechawar, N., Cozzari, C., & Descarries, L. (2000). Cholinergic innervation in adult rat cerebral cortex: A quantitative immunocytochemical description. Journal of Comparative Neurology, 428(2), 305–318.

    Article  PubMed  CAS  Google Scholar 

  • Metherate, R., & Ashe, J. H. (1993). Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in rat auditory cortex. Synapse, 14, 132–143.

    Article  PubMed  CAS  Google Scholar 

  • Metherate, R., Cox, C. L., & Ashe, J. H. (1992). Cellular bases of neocortical activation: Modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. Journal of Neuroscience, 12, 4701–4711.

    PubMed  CAS  Google Scholar 

  • Miller, J. M., Sutton, D., Pfingst, B., Ryan, A., Beaton, R., & Gourevitch, G. (1972). Single cell activity in the auditory cortex of Rhesus monkeys: Behavioral dependency. Science, 177(47), 449–451.

    Article  PubMed  CAS  Google Scholar 

  • Moruzzi, G., & Magoun, H. W. (1949). Brain stem reticular formation and activation of the EEG. Electroencephalography and Clinical Neurophysiology, 1(4), 455–473.

    PubMed  CAS  Google Scholar 

  • Recanzone, G. H., Schreiner, C. E., & Merzenich, M. M. (1993). Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. Journal of Neuroscience, 13(1), 87–103.

    PubMed  CAS  Google Scholar 

  • Rosenbaum, D. M., Rasmussen, S. G., & Kobilka, B. K. (2009). The structure and function of G-protein-coupled receptors. Nature, 459(7245), 356–363.

    Article  PubMed  CAS  Google Scholar 

  • Schofield, B. R. (2010). Projections from auditory cortex to midbrain cholinergic neurons that project to the inferior colliculus. Neuroscience, 166(1), 231–240.

    Article  PubMed  CAS  Google Scholar 

  • Seguela, P., Wadiche, J., Dineley-Miller, K., Dani, J. A., & Patrick, J. W. (1993). Molecular cloning, functional properties, and distribution of rat brain alpha7: A nicotinic cation channel highly permeable to calcium. Journal of Neuroscience, 13, 596–604.

    PubMed  CAS  Google Scholar 

  • Shute, C. C., & Lewis, P. R. (1967). The ascending cholinergic reticular system: Neocortical, olfactory and subcortical projections. Brain, 90(3), 497–520.

    Article  PubMed  CAS  Google Scholar 

  • Steriade, M. (1996). Arousal: Revisiting the reticular activating system. Science, 272(5259), 225–226.

    Article  PubMed  CAS  Google Scholar 

  • Steriade, M., Gloor, P., Llinas, R. R., Silva, F. H. L. d., & Mesulam, M.-M. (1990). Basic mechanisms of cerebral rhythmic activities. Electroencephalography and Clinical Neurophysiology, 76, 481–508.

    Article  PubMed  CAS  Google Scholar 

  • Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science, 262(5134), 679–685.

    Article  PubMed  CAS  Google Scholar 

  • Wainer, B. H., & Mesulam, M.-M. (1990). Ascending cholinergic pathways in the rat brain. In M. Steriade & D. Biesold (Eds.), Brain Cholinergic Systems (pp. 65–119). Oxford: Oxford University Press.

    Google Scholar 

  • Weinberger, N. M. (2004). Specific long-term memory traces in primary auditory cortex. Nature Reviews Neuroscience, 5(4), 279–290.

    Article  PubMed  CAS  Google Scholar 

  • Weinberger, N. M., Hopkins, W., & Diamond, D. M. (1984). Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: I. Primary field (AI). Behavioral Neuroscience, 98(2), 171–188.

    Article  PubMed  CAS  Google Scholar 

  • Weston, C. R., Lambright, D. G., & Davis, R. J. (2002). Signal transduction: MAP kinase signaling specificity. Science, 296(5577), 2345–2347.

    Article  PubMed  CAS  Google Scholar 

  • Woolf, N. J. (1991). Cholinergic systems in mammalian brain and spinal cord. Progress in Neurobiology, 37(6), 475–524.

    Article  PubMed  CAS  Google Scholar 

  • Yan, J., & Zhang, Y. (2005). Sound-guided shaping of the receptive field in the mouse auditory cortex by basal forebrain activation. European Journal of Neuroscience, 21(2), 563–576.

    Article  PubMed  CAS  Google Scholar 

  • Yarosh, C. A., Olito, A. C., & Ashe, J. H. (1988). AF-DX 116: A selective antagonist of the slow inhibitory postsynaptic potential and methacholine-induced hyperpolarization in superior cervical ganglion of the rabbit. Journal of Pharmacology and Experimental Therapeutics, 245(2), 419–425.

    PubMed  CAS  Google Scholar 

  • Yuste, R., & Sur, M. (1999). Development and plasticity of the cerebral cortex: From molecules to maps. Journal of Neurobiology, 41(1), 1–6.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Y., Hamilton, S. E., Nathanson, N. M., & Yan, J. (2006). Decreased input-specific plasticity of the auditory cortex in mice lacking M1 muscarinic acetylcholine receptors. Cerebral Cortex, 16(9), 1258–1265.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The author’s research cited here was supported by the National Institutes of Health (NIDCD DC02967 and NIDA DA12929) and the National Science Foundation (IBN 9510904).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raju Metherate .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Metherate, R. (2012). Modulatory Mechanisms Controlling Auditory Processing. In: Trussell, L., Popper, A., Fay, R. (eds) Synaptic Mechanisms in the Auditory System. Springer Handbook of Auditory Research, vol 41. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-9517-9_8

Download citation

Publish with us

Policies and ethics