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The Journal of Neuroscience, May 27, 2009, 29(21):6871-6882; doi:10.1523/JNEUROSCI.5513-08.2009

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Development/Plasticity/Repair
Effects of Restricted Basilar Papillar Lesions and Hair Cell Regeneration on Auditory Forebrain Frequency Organization in Adult European Starlings

Dexter R. F. Irvine,^1,3 Mel Brown,¹ Marc R. Kamke,² and Edwin W Rubel³

¹School of Psychology, Psychiatry and Psychological Medicine, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Victoria 3800, Australia, ²The University of Queensland, Queensland Brain Institute, Brisbane, Queensland 4072, Australia, and ³Virginia Merrill Bloedel Hearing Research Center, University of Washington, Seattle, Washington 98195

Correspondence should be addressed to Dr. Dexter R. F. Irvine, School of Psychology, Psychiatry and Psychological Medicine, Monash University, Melbourne, VIC 3800, Australia. Email: d.irvine{at}med.monash.edu.au

The frequency organization of neurons in the forebrain Field L complex (FLC) of adult starlings was investigated to determine the effects of hair cell (HC) destruction in the basal portion of the basilar papilla (BP) and of subsequent HC regeneration. Conventional microelectrode mapping techniques were used in normal starlings and in lesioned starlings either 2 d or 6–10 weeks after aminoglycoside treatment. Histological examination of the BP and recordings of auditory brainstem evoked responses confirmed massive loss of HCs in the basal portion of the BP and hearing losses at frequencies >2 kHz in starlings tested 2 d after aminoglycoside treatment. In these birds, all neurons in the region of the FLC in which characteristic frequencies (CFs) normally increase from 2 to 6 kHz had CF in the range of 2–4 kHz. The significantly elevated thresholds of responses in this region of altered tonotopic organization indicated that they were the residue of prelesion responses and did not reflect CNS plasticity. In the long-term recovery birds, there was histological evidence of substantial HC regeneration. The tonotopic organization of the high-frequency region of the FLC did not differ from that in normal starlings, but the mean threshold at CF in this frequency range was intermediate between the values in the normal and lesioned short-recovery groups. The recovery of normal tonotopicity indicates considerable stability of the topography of neuronal connections in the avian auditory system, but the residual loss of sensitivity suggests deficiencies in high-frequency HC function.

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Received Nov. 17, 2008; revised April 23, 2009; accepted April 25, 2009.

Correspondence should be addressed to Dr. Dexter R. F. Irvine, School of Psychology, Psychiatry and Psychological Medicine, Monash University, Melbourne, VIC 3800, Australia. Email: d.irvine{at}med.monash.edu.au

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