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The descending corticocollicular pathway mediates learning-induced auditory plasticity

Nature Neuroscience volume 13, pages253–260(2010)Cite this article

Abstract

Descending projections from sensory areas of the cerebral cortex are among the largest pathways in the brain, suggesting that they are important for subcortical processing. Although corticofugal inputs have been shown to modulate neuronal responses in the thalamus and midbrain, the behavioral importance of these changes remains unknown. In the auditory system, one of the major descending pathways is from cortical layer V pyramidal cells to the inferior colliculus in the midbrain. We examined the role of these neurons in experience-dependent recalibration of sound localization in adult ferrets by selectively killing the neurons using chromophore-targeted laser photolysis. When provided with appropriate training, animals normally relearn to localize sound accurately after altering the spatial cues available by reversibly occluding one ear. However, this ability was lost after eliminating corticocollicular neurons, whereas normal sound-localization accuracy was unaffected. The integrity of this descending pathway is therefore critical for learning-induced localization plasticity.

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Figure 1: Experimental design.
Figure 2: Effect of unilateral auditory corticocollicular lesions on sound-localization accuracy.
Figure 3: Effect of monaural occlusion on auditory-localization accuracy by the control ferrets (left column) and the ferrets with left auditory corticocollicular lesions (right column).
Figure 4: Effect of occluding the right ear on sound-localization accuracy.
Figure 5: Effect of occluding the left ear on sound-localization accuracy.
Figure 6: Reduction in density of layer V neurons in the primary auditory cortex in the corticocollicular lesion group.
Figure 7: Reduction in the number of layer V pyramidal neurons in the primary auditory cortex following corticocollicular lesions.
Figure 8: (a,b) Two examples of the distribution of retrograde-labeled fluorescent cells in the left auditory cortex for a ferret from the corticocollicular lesion group (a) and one from the control group (b).

References

  1. 1

    Gilbert, C.D., Li, W. & Piech, V. Perceptual learning and adult cortical plasticity. J. Physiol. (Lond.) 587, 2743–2751 (2009).

    CAS  Article  Google Scholar 

  2. 2

    Dahmen, J.C. & King, A.J. Learning to hear: plasticity of auditory cortical processing. Curr. Opin. Neurobiol. 17, 456–464 (2007).

    CAS  Article  Google Scholar 

  3. 3

    Edeline, J.M. & Weinberger, N.M. Thalamic short-term plasticity in the auditory system: associative returning of receptive fields in the ventral medial geniculate body. Behav. Neurosci. 105, 618–639 (1991).

    CAS  Article  Google Scholar 

  4. 4

    Tzounopoulos, T. & Kraus, N. Learning to encode timing: mechanisms of plasticity in the auditory brainstem. Neuron 62, 463–469 (2009).

    CAS  Article  Google Scholar 

  5. 5

    Suga, N. & Ma, X. Multiparametric corticofugal modulation and plasticity in the auditory system. Nat. Rev. Neurosci. 4, 783–794 (2003).

    CAS  Article  Google Scholar 

  6. 6

    Sillito, A.M., Jones, H.E., Gerstein, G.L. & West, D.C. Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 369, 479–482 (1994).

    CAS  Article  Google Scholar 

  7. 7

    Krupa, D.J., Ghazanfar, A.A. & Nicolelis, M.A. Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proc. Natl. Acad. Sci. USA 96, 8200–8205 (1999).

    CAS  Article  Google Scholar 

  8. 8

    Xiao, Z. & Suga, N. Modulation of cochlear hair cells by the auditory cortex in the mustached bat. Nat. Neurosci. 5, 57–63 (2002).

    CAS  Article  Google Scholar 

  9. 9

    Perrot, X. et al. Evidence for corticofugal modulation of peripheral auditory activity in humans. Cereb. Cortex 16, 941–948 (2006).

    Article  Google Scholar 

  10. 10

    Alvarado, J.C., Stanford, T.R., Vaughan, J.W. & Stein, B.E. Cortex mediates multisensory, but not unisensory, integration in superior colliculus. J. Neurosci. 27, 12775–12786 (2007).

    CAS  Article  Google Scholar 

  11. 11

    Luo, F., Wang, Q., Kashani, A. & Yan, J. Corticofugal modulation of initial sound processing in the brain. J. Neurosci. 28, 11615–11621 (2008).

    CAS  Article  Google Scholar 

  12. 12

    Suga, N. Role of corticofugal feedback in hearing. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 194, 169–183 (2008).

    Google Scholar 

  13. 13

    Ma, X. & Suga, N. Plasticity of bat's central auditory system evoked by focal electric stimulation of auditory and/or somatosensory cortices. J. Neurophysiol. 85, 1078–1087 (2001).

    CAS  Article  Google Scholar 

  14. 14

    Yan, J., Zhang, Y. & Ehret, G. Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice. J. Neurophysiol. 93, 71–83 (2005).

    Article  Google Scholar 

  15. 15

    Yan, J. & Ehret, G. Corticofugal modulation of midbrain sound processing in the house mouse. Eur. J. Neurosci. 16, 119–128 (2002).

    Article  Google Scholar 

  16. 16

    Ma, X. & Suga, N. Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats. Proc. Natl. Acad. Sci. USA 98, 14060–14065 (2001).

    CAS  Article  Google Scholar 

  17. 17

    Zhou, X. & Jen, P.H. Corticofugal modulation of directional sensitivity in the midbrain of the big brown bat, Eptesicus fuscus. Hear. Res. 203, 201–215 (2005).

    Article  Google Scholar 

  18. 18

    Nakamoto, K.T., Jones, S.J. & Palmer, A.R. Descending projections from auditory cortex modulate sensitivity in the midbrain to cues for spatial position. J. Neurophysiol. 99, 2347–2356 (2008).

    Article  Google Scholar 

  19. 19

    Macklis, J.D. Transplanted neocortical neurons migrate selectively into regions of neuronal degeneration produced by chromophore-targeted laser photolysis. J. Neurosci. 13, 3848–3863 (1993).

    CAS  Article  Google Scholar 

  20. 20

    Magavi, S.S., Leavitt, B.R. & Macklis, J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 405, 951–955 (2000).

    CAS  Article  Google Scholar 

  21. 21

    King, A.J., Doubell, T.P. & Schnupp, J.W.H. The shape of ears to come: dynamic coding of auditory space. Trends Cog. Sci. 5, 261–270 (2001).

    Article  Google Scholar 

  22. 22

    Chase, S.M. & Young, E.D. Cues for sound localization are encoded in multiple aspects of spike trains in the inferior colliculus. J. Neurophysiol. 99, 1672–1682 (2008).

    Article  Google Scholar 

  23. 23

    Jenkins, W.M. & Merzenich, M.M. Role of cat primary auditory cortex for sound-localization behavior. J. Neurophysiol. 52, 819–847 (1984).

    CAS  Article  Google Scholar 

  24. 24

    Kavanagh, G.L. & Kelly, J.B. Contributions of auditory cortex to sound localization in the ferret (Mustela putorius). J. Neurophysiol. 57, 1746–1766 (1987).

    CAS  Article  Google Scholar 

  25. 25

    Heffner, H.E. & Heffner, R.S. Effect of bilateral auditory cortex lesions on sound localization in Japanese macaques. J. Neurophysiol. 64, 915–931 (1990).

    CAS  Article  Google Scholar 

  26. 26

    Spierer, L., Tardif, E., Sperdin, H., Murray, M.M. & Clarke, S. Learning-induced plasticity in auditory spatial representations revealed by electrical neuroimaging. J. Neurosci. 27, 5474–5483 (2007).

    CAS  Article  Google Scholar 

  27. 27

    Nodal, F.R., Bajo, V.M., Parsons, C.H., Schnupp, J.W.H. & King, A.J. Sound localization behavior in ferrets: comparison of acoustic orientation and approach-to-target responses. Neuroscience 154, 397–408 (2008).

    CAS  Article  Google Scholar 

  28. 28

    Thompson, G.C. & Masterton, R.B. Brain stem auditory pathways involved in reflexive head orientation to sound. J. Neurophysiol. 41, 1183–1202 (1978).

    CAS  Article  Google Scholar 

  29. 29

    Lomber, S.G., Payne, B.R. & Cornwell, P. Role of the superior colliculus in analyses of space: superficial and intermediate layer contributions to visual orienting, auditory orienting, and visuospatial discriminations during unilateral and bilateral deactivations. J. Comp. Neurol. 441, 44–57 (2001).

    CAS  Article  Google Scholar 

  30. 30

    Kacelnik, O., Nodal, F.R., Parsons, C.H. & King, A.J. Training-induced plasticity of auditory localization in adult mammals. PLoS Biol. 4, e71 (2006).

    Article  Google Scholar 

  31. 31

    Bajo, V.M., Nodal, F.R., Bizley, J.K., Moore, D.R. & King, A.J. The ferret auditory cortex: descending projections to the inferior colliculus. Cereb. Cortex 17, 475–491 (2007).

    Article  Google Scholar 

  32. 32

    Winer, J.A., Larue, D.T., Diehl, J.J. & Hefti, B.J. Auditory cortical projections to the cat inferior colliculus. J. Comp. Neurol. 400, 147–174 (1998).

    CAS  Article  Google Scholar 

  33. 33

    King, A.J., Jiang, Z.D. & Moore, D.R. Auditory brainstem projections to the ferret superior colliculus: anatomical contribution to the neural coding of sound azimuth. J. Comp. Neurol. 390, 342–365 (1998).

    CAS  Article  Google Scholar 

  34. 34

    Knudsen, E.I., Esterly, S.D. & Knudsen, P.F. Monaural occlusion alters sound localization during a sensitive period in the barn owl. J. Neurosci. 4, 1001–1011 (1984).

    CAS  Article  Google Scholar 

  35. 35

    King, A.J., Parsons, C.H. & Moore, D.R. Plasticity in the neural coding of auditory space in the mammalian brain. Proc. Natl. Acad. Sci. USA 97, 11821–11828 (2000).

    CAS  Article  Google Scholar 

  36. 36

    Bauer, R.W., Matuzsa, J.L., Blackmer, F. & Glucksberg, S. Noise localization after unilateral attenuation. J. Acoust. Soc. Am. 40, 441–444 (1966).

    Article  Google Scholar 

  37. 37

    Florentine, M. Relation between lateralization and loudness in asymmetrical hearing losses. J. Am. Audiol. Soc. 1, 243–251 (1976).

    CAS  PubMed  Google Scholar 

  38. 38

    Van Wanrooij, M.M. & Van Opstal, A.J. Sound localization under perturbed binaural hearing. J. Neurophysiol. 97, 715–726 (2007).

    Article  Google Scholar 

  39. 39

    Mrsic-Flogel, T.D., King, A.J. & Schnupp, J.W.H. Encoding of virtual acoustic space stimuli by neurons in ferret primary auditory cortex. J. Neurophysiol. 93, 3489–3503 (2005).

    Article  Google Scholar 

  40. 40

    Woods, T.M., Lopez, S.E., Long, J.H., Rahman, J.E. & Recanzone, G.H. Effects of stimulus azimuth and intensity on the single-neuron activity in the auditory cortex of the alert macaque monkey. J. Neurophysiol. 96, 3323–3337 (2006).

    Article  Google Scholar 

  41. 41

    Jiang, W., Jiang, H. & Stein, B.E. Two corticotectal areas facilitate multisensory orientation behavior. J. Cogn. Neurosci. 14, 1240–1255 (2002).

    Article  Google Scholar 

  42. 42

    Hofman, M. & van Opstal, A.J. Binaural weighting of pinna cues in human sound localization. Exp. Brain Res. 148, 458–470 (2003).

    CAS  Article  Google Scholar 

  43. 43

    Jin, C., Corderoy, A., Carlile, S. & van Schaik, A. Contrasting monaural and interaural spectral cues for human sound localization. J. Acoust. Soc. Am. 115, 3124–3141 (2004).

    Article  Google Scholar 

  44. 44

    Eyding, D., Macklis, J.D., Neubacher, U., Funke, K. & Wörgötter, F. Selective elimination of corticogeniculate feedback abolishes the electroencephalogram dependence of primary visual cortical receptive fields and reduces their spatial specificity. J. Neurosci. 23, 7021–7033 (2003).

    CAS  Article  Google Scholar 

  45. 45

    Davis, K.A., Ramachandran, R. & May, B.J. Single-unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences. J. Neurophysiol. 82, 164–175 (1999).

    CAS  Article  Google Scholar 

  46. 46

    Pollak, G.D., Burger, R.M., Park, T.J., Klug, A. & Bauer, E.E. Roles of inhibition for transforming binaural properties in the brainstem auditory system. Hear. Res. 168, 60–78 (2002).

    Article  Google Scholar 

  47. 47

    Oliver, D.L. Neuronal organization of the inferior colliculus. in The Inferior Colliculus (eds Winer, J.A. & Schreiner, C.E.) 69–114 (Springer, New York, 2005).

  48. 48

    Polley, D.B., Steinberg, E.E. & Merzenich, M.M. Perceptual learning directs auditory cortical map reorganization through top-down influences. J. Neurosci. 26, 4970–4982 (2006).

    CAS  Article  Google Scholar 

  49. 49

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

    CAS  Article  Google Scholar 

  50. 50

    Weinberger, N.M. Specific long-term memory traces in primary auditory cortex. Nat. Rev. Neurosci. 5, 279–290 (2004).

    CAS  Article  Google Scholar 

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Acknowledgements

We are grateful to J.D. Macklis and R. Fricker-Gates for helping us to set up the chromophore-targeted laser photolysis technique and to B. Willmore for statistical advice. K. Allen and A. Fieger assisted with the early stages of the project, and J. Bizley, R. Campbell, D. Kumpik and S. Spires contributed to the behavioral testing and provided valuable discussion. This work was supported by the Wellcome Trust through a Principal Research Fellowship to A.J.K. (WT076508AIA) and a project grant to A.J.K. and D.R.M. (WT069600/Z/02/Z).

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Author notes

  1. David R Moore

    Present address: Present address: MRC Institute of Hearing Research, Nottingham, UK.,

Affiliations

  1. Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK

    Victoria M Bajo, Fernando R Nodal, David R Moore & Andrew J King

Authors
  1. Victoria M Bajo
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  3. David R Moore
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Contributions

This study was conceived by V.M.B., A.J.K. and D.R.M. and designed by V.M.B. and A.J.K. The behavioral experiments were performed by V.M.B., F.R.N. and A.J.K. The anatomical studies were carried out by V.M.B., who jointly analyzed all of the data with F.R.N. A.J.K., V.M.B. and F.R.N. wrote the paper with assistance from D.R.M.

Corresponding author

Correspondence to Andrew J King.

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Bajo, V., Nodal, F., Moore, D. et al. The descending corticocollicular pathway mediates learning-induced auditory plasticity. Nat Neurosci 13, 253–260 (2010). https://doi.org/10.1038/nn.2466

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