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Experience-dependent plasticity in the nucleus laminaris of the barn owl

Christine Koeppl1, Go Ashida2, Sandra Brill3, Richard Kempter4, Hermann Wagner3 and Catherine Carr2
  • 1 Carl von Ossietzky University Oldenburg, Biology, Germany
  • 2 Univ Maryland, Biology, United States
  • 3 RWTH Aachen, Zoology, Germany
  • 4 Humboldt University, Institute for Theoretical Biology, Germany

Humans and animals rely on subtle interaural differences for sound localization. Such differences arise from different sound path lengths to the two ears and from shadowing effects of the head, leading to both interaural time and interaural level differences. In the barn owl, the neural processing of interaural time differences (ITD) is known in great detail. At the level of the first binaural convergence, the brainstem nucleus laminaris, a large array of coincidence detector cells, receiving input from delay-line axons from each ear, forms a first topographic map of ITDs. This is relayed to midbrain centers where it provides the horizontal coordinates for a neural representation of auditory space.
The association of particular ITDs with the corresponding locations in space is critically dependent on the size of the head and details of its shape. Young owls learn this and calibrate their sound localization using early visual and auditory experience. Experimentally altered auditory experience induces appropriate plastic adjustments in the midbrain representations of auditory space (Gold and Knudsen, 2000). Here we aim to determine whether this plasticity already arises at the level of the brainstem.
Young owls (from P21) were unilaterally fitted with an ear-canal insert designed to introduce a time delay to inputs from that ear (Gold and Knudsen, 1999). After growing up with this altered auditory experience to a minimum age of 3 months, the insert was removed and neurophonic responses were recorded extracellularly in nucleus laminaris (NL) under anesthesia. Small electrolytic lesions were placed at selected recording sites, to recover their precise position and determine whether the map of ITD was altered by experience.
The normal adult map of ITD in the barn owl’s NL is well known. When an electrode is lowered through the nucleus, approximately parallel to the delay lines, the phase of a monaurally or binaurally evoked neurophonic shifts in an orderly fashion that reflects the map of delays (Sullivan and Konishi, 1986, Wagner et al., 2005). Our hypothesis was that, if NL adjusts for the temporally altered input, the maps of ITD would be shifted compared to normal. In addition, complementary shifts are expected in the NL of both sides. Specifically, on the side ipsilateral to the ear insert, the point of zero ITD should shift ventrally, and dorsally on the contralateral side.
Of 8 owls raised with ear inserts, two are currently completed with the data fully analyzed. Lesions in the 3-4 kHz tonotopic band of NL on both sides of the brainstem confirmed that the point where zero ITD is represented was located more ventrally than normal on the side ipsilateral to the ear insert, and more dorsally on the contralataral side. These preliminary data suggest that experience-dependent plasticity does occur in the avian NL. The observed changes are suited to adjust the mapped ITD range with microsecond precision to the animal’s individual auditory experience.

Acknowledgements

This work was supported by NIH DC00436 to CEC, NIH P30 DC04664 to the University of Maryland Center for the Comparative and Evolutionary Biology of Hearing, the Hanse Wissenschaftkolleg, the Humboldt Foundation, the Bundesministerium fuer Bildung und Forschung (Bernstein Collaboration in Computational Neuroscience: Temporal Precision 01GQ07101 (HW) and 01GQ07102 (RK)

References

Gold, J. I., & Knudsen, E. I. (1999). Hearing impairment induces frequency-specific adjustments in auditory spatial tuning in the optic tectum of young owls. Journal of Neurophysiology, 82, 2197–2209.
Gold, J. I., & Knudsen, E. I. (2000). Abnormal auditory experience induces frequency-specific adjustments in unit tuning for binaural localization cues in the optic tectum of juvenile owls. The Journal of Neuroscience, 20, 862–877.
Sullivan, W. E., & Konishi, M. (1986). Neural map of interaural phase difference in the owl's brainstem. Proceedings of the National Academy of Sciences of the United States of America, 83, 8400–8404.
Wagner, H., Brill, S., Kempter, R., & Carr, C. E. (2005). Microsecond precision of phase delay in the auditory system of the barn owl. Journal of Neurophysiology, 94(2), 1655–1658. doi:10.1152/jn.01226.2004

Keywords: auditory, plasticity, Sound Localization

Conference: Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.

Presentation Type: Poster Presentation (see alternatives below as well)

Topic: Sensory: Audition

Citation: Koeppl C, Ashida G, Brill S, Kempter R, Wagner H and Carr C (2012). Experience-dependent plasticity in the nucleus laminaris of the barn owl. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00396

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Received: 01 May 2012; Published Online: 07 Jul 2012.