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The descending corticocollicular pathway mediates learning-induced auditory plasticity

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).

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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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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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