Anatomical traces of juvenile learning in the auditory system of adult barn owls

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Abstract

Early experience plays a powerful role in shaping adult neural circuitry and behavior. In barn owls, early experience markedly influences sound localization. Juvenile owls that learn new, abnormal associations between auditory cues and locations in visual space as a result of abnormal visual experience can readapt to the same abnormal experience in adulthood, when plasticity is otherwise limited. Here we show that abnormal anatomical projections acquired during early abnormal sensory experience persist long after normal experience has been restored. These persistent projections are perfectly situated to provide a physical framework for subsequent readaptation in adulthood to the abnormal sensory conditions experienced in early life. Our results show that anatomical changes that support strong learned neural connections early in life can persist even after they are no longer functionally expressed. This maintenance of silenced neural circuitry that was once adaptive may represent an important mechanism by which the brain preserves a record of early experience.

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Figure 1: Anatomical changes in the midbrain that accompany prism rearing.
Figure 2: ITD tuning in the optic tectum after prism rearing and prism removal.
Figure 3: Retrograde labeling in normal, shifted and experienced owls.
Figure 4: Anterograde labeling in normal and experienced owls.

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Acknowledgements

We thank R. Desai and D. Ro for assistance with digital tracing of anatomical data; P. Knudsen for technical assistance and owl care; and C. Darian-Smith, Y. Gutfreund, J. Bergan and K. Maczko for critical comments on the manuscript. B.A.L. and E.I.K. conceived the experiments; B.A.L. did the experiments and, with C.v.d.O., analyzed the data and created the figures; and B.A.L. and E.I.K. co-wrote the manuscript. This work was supported by grants to E.I.K. from the NIH (National Institute of Deafness and other Communication Disorders) and the McKnight Foundation. B.A.L. was supported by a National Defense Science and Engineering Graduate Fellowship, an NIH training grant, and a Gerald J. Lieberman Fellowship.

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Correspondence to Eric I Knudsen.

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Supplementary information

Supplementary Fig. 1

Similar distributions of bouton densities in normal and experienced owls. (a) Representative axon segment with boutons (punctate swellings). (b) Bouton frequency measurements in normal and experienced owls. Symbols indicate number of axon segments with the given bouton frequency (X axis). Circles: center projection region, normal owls (mean = 12±4; n = 55). Squares: center projection region, experienced owls (mean = 13±5; n = 98). Triangles: acquired projection region, experienced owls (mean = 11±5; n = 102). (JPG 35 kb)

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Linkenhoker, B., von der Ohe, C. & Knudsen, E. Anatomical traces of juvenile learning in the auditory system of adult barn owls. Nat Neurosci 8, 93–98 (2005) doi:10.1038/nn1367

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