Abstract
The midbrain contains an auditory map of space that is shaped by visual experience1,2,3. When barn owls are raised wearing spectacles that horizontally displace the visual field, the auditory space map in the external nucleus of the inferior colliculus (ICX) shifts according to the optical displacement of the prisms4. Topographic visual activity in the optic tectum could serve as the template that instructs the auditory space map5. We studied the effects of a restricted, unilateral lesion in the portion of the optic tectum that represents frontal space. Here we show that such a lesion eliminates adaptive adjustments specifically in the portion of the auditory map that represents frontal space on the same side of the brain, while the rest of the map continues to adjust adaptively. Thus, activity in the tectum calibrates the auditory space map in a location-specific manner. Because the site of adaptive changes is the ICX4,6,7, the results also indicate that the tectum provides a topographic instructive signal that controls adaptive auditory plasticity in the ICX.
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References
Knudsen, E. I. & Brainard, M. S. Visual instruction of the neural map of auditory space in the developing optic tectum. Science 253, 85–87 (1991).
King, A J. A map of auditory space in the mammalian brain: neural computation and development. Exp. Physiol. 78, 559–590 (1993).
Withington-Wray, D. J., Binns, K. E. & Keating, M. J. The maturation of the superior collicular map of auditory space in the guinea pig is disrupted by developmental visual deprivation. Eur. J. Neurosci. 2, 682–692 (1990).
Brainard, M. S. & Knudsen, E. I. Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl. J. Neurosci. 13, 4589–4608 (1993).
Hyde, P. S. & Knudsen, E. I. A topographic instructive signal guides the adjustment of the auditory space map in the optic tectum. J. Neursci. (in the press).
Feldman, D. E. & Knudsen, E. I. An anatomical basis for visual calibration of the auditory space map in the barn owl's midbrain. J. Neurosci. 17, 6820–6837 (1997).
DeBello, W. M., Feldman, D. E. & Knudsen, E. I. Adaptive axonal remodelling in the midbrain auditory space map. J. Neurosci. 21, 3161–3174 (2001).
Stein, B. E. & Meredith, M. A. The Merging of the Senses (MIT Press, Cambridge, Massachusetts, 1993).
Knudsen, E. I. Auditory and visual maps of space in the optic tectum of the owl. J. Neurosci. 2, 1177–1194 (1982).
Middlebrooks, J. C. & Knudsen, E. I. A neural code for auditory space in the cat's superior colliculus. J. Neurosci. 4, 2621–2634 (1984).
King, A. J. & Hutchings, M. E. Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: A map of auditory space. J. Neurophysiol. 57, 596–624 (1987).
King, A. J. & Carlile, S. Changes induced in the representation of auditory space in the superior colliculus by rearing ferrets with binocular eyelid suture. Exp. Brain Res. 94, 444–455 (1993).
Knudsen, E. I. & Brainard, M. S. Creating a unified representation of visual and auditory space in the brain. Annu. Rev. Neurosci. 18, 19–44 (1995).
Knudsen, E. I. & Knudsen, P. F. Space-mapped auditory projections from the inferior colliculus to the optic tectum in the barn owl (Tyto alba). J. Comp. Neurol. 218, 187–196 (1983).
Hyde, P. S. & Knudsen, E. I. Topographic projection from the optic tectum to the auditory space map in the inferior colliculus of the barn owl. J. Comp. Neurol. 421, 146–160 (2000).
Luksch, H., Gauger, B. & Wagner, H. A candidate pathway for a visual instructional signal to the barn owl's auditory system. J. Neurosci. 20, RC70:1–4 (2000).
Gold, J. I. & Knudsen, E. I. A site of auditory experience-dependent plasticity in the neural representation of auditory space in the barn owl's inferior colliculus. J. Neurosci. 20, 3469–3486 (2000).
Knudsen, E. I. & Mogdans, J. Vision-independent adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl optic tectum. J. Neurosci. 12, 3485–3493 (1992).
Knudsen, E. I., Esterly, S. D. & du Lac, S. Stretched and upside-down maps of auditory space in the optic tectum of blind-reared owls: acoustic basis and behavioral correlates. J. Neurosci. 11, 1727–1747 (1991).
Brainard, M. S. & Knudsen, E. I. Sensitive periods for visual calibration of the auditory space map in the barn owl optic tectum. J. Neurosci. 18, 3929–3942 (1998).
Zheng, W. & Knudsen, E. I. Gabaergic inhibition antagonizes adaptive adjustment of the owl's auditory space map during the initial phase of plasticity. J. Neurosci. 21, 4356–4365 (2001).
Knudsen, E. I., Cohen, Y. E. & Masino, T. Characterization of a forebrain gaze field in the archistriatum of the barn owl: microstimulation and anatomical connections. J. Neurosci. 15, 5139–5151 (1995).
King, A. J., Hutchings, M. E., Moore, D. R. & Blakemore, C. Developmental plasticity in the visual and auditory representations in the mammalian superior colliculus. Nature 332, 73–76 (1988).
Withington-Wray, D. J., Binns, K. E., Dhanjal, S. S., Brickley, S. G. & Keating, M. J. The maturation of the superior collicular map of auditory space in the guinea pig is disrupted by developmental auditory deprivation. Eur. J. Neurosci. 2, 693–703 (1990).
Gold, J. I. & Knudsen, E. I. Hearing impairment induces frequency-specific adjustments in auditory spatial tuning in the optic tectum of young owls. J. Neurophysiol. 82, 2197–2209 (1999).
Gold, J. I. & Knudsen, E. I. Abnormal auditory experience induces frequency-specific adjustments in unit tuning for binaural localization cues in the optic tectum of juvenile owls. J. Neurosci. 20, 862–877 (2000).
Batista, A. P., Buneo, C. A., Snyder, L. H. & Andersen, R. A. Reach plans in eye-centered coordinates. Science 285, 257–260 (1999).
Cohen, Y. E. & Andersen, R. A. Reaches to sounds encoded in an eye-centered reference frame. Neuron 27, 647–652 (2000).
Troyer, T. W. & Doupe, A. J. An associational model of birdsong sensorimotor learning I. Efference copy and the learning of song syllables. J. Neurophysiol. 84, 1204–1223 (2000).
Klier, E. M., Wang, H. & Crawford, J. D. The superior colliculus encodes gaze commands in retinal coordinates. Nature Neurosci. 4, 627–632 (2001).
Acknowledgements
We thank B. Newsome, J. Raymond, S. McConnell, J. Gold, B. Linkenhoker and Y. Gutfreund for comments on the manuscript. This work was supported by grants from the March of Dimes and the National Institute on Deafness and other Communication Disorders (NIDCD).
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Hyde, P., Knudsen, E. The optic tectum controls visually guided adaptive plasticity in the owl's auditory space map. Nature 415, 73–76 (2002). https://doi.org/10.1038/415073a
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DOI: https://doi.org/10.1038/415073a
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