The optic tectum controls visually guided adaptive plasticity in the owl's auditory space map

Nature ◽  
2002 ◽  
Vol 415 (6867) ◽  
pp. 73-76 ◽  
Author(s):  
Peter S. Hyde ◽  
Eric I. Knudsen
1994 ◽  
Vol 72 (6) ◽  
pp. 2875-2891 ◽  
Author(s):  
J. Mogdans ◽  
E. I. Knudsen

1. The optic tectum of the barn owl contains a physiological map of interaural level difference (ILD) that underlies, in part, its map of auditory space. Monaural occlusion shifts the range of ILDs experienced by an animal and alters the correspondence of ILDs with source locations. Chronic monaural occlusion during development induces an adaptive shift in the tectal ILD map that compensates for the effects of the earplug. The data presented in this study indicate that one site of plasticity underlying this adaptive adjustment is in the posterior division of the ventral nucleus of the lateral lemniscus (VLVp), the first site of ILD comparison in the auditory pathway. 2. Single and multiple unit sites were recorded in the optic tecta and VLVps of ketamine-anesthetized owls. The owls were raised from 4 wk of age with one ear occluded with an earplug. Auditory testing, using digitally synthesized dichotic stimuli, was carried out 8-16 wk later with the earplug removed. The adaptive adjustment in ILD coding in each bird was quantified as the shift from normal ILD tuning measured in the optic tectum. Evidence of adaptive adjustment in the VLVp was based on statistical differences between the VLVp's ipsilateral and contralateral to the occluded ear in the sensitivity of units to excitatory-ear and inhibitory-ear stimulation. 3. The balance of excitatory to inhibitory influences on VLVp units was shifted in the adaptive direction in six out of eight owls. In three of these owls, adaptive differences in inhibition, but not in excitation, were found. For this group of owls, the patterns of response properties across the two VLVps can only be accounted for by plasticity in the VLVp. For the other three owls, the possibility that the difference between the two VLVps resulted from damage to one of the VLVps could not be eliminated, and for one of these, plasticity at a more peripheral site (in the cochlea or cochlear nucleus) could also explain the data. In the remaining two owls, there was no evidence of adaptive adjustment in the VLVp despite large adaptive adjustments in the optic tectum. 4. The adjustment of ILD coding in the VLVp was always substantially smaller than expected based on the adjustment of ILD tuning in the optic tectum measured in the same animals. This indicates the involvement of at least one additional site of adaptive plasticity in the auditory pathway above the level of the VLVp.(ABSTRACT TRUNCATED AT 400 WORDS)


2006 ◽  
Vol 96 (2) ◽  
pp. 813-825 ◽  
Author(s):  
Yoram Gutfreund ◽  
Eric I. Knudsen

Auditory neurons in the owl’s external nucleus of the inferior colliculus (ICX) integrate information across frequency channels to create a map of auditory space. This study describes a powerful, sound-driven adaptation of unit responsiveness in the ICX and explores the implications of this adaptation for sensory processing. Adaptation in the ICX was analyzed by presenting lightly anesthetized owls with sequential pairs of dichotic noise bursts. Adaptation occurred in response even to weak, threshold-level sounds and remained strong for more than 100 ms after stimulus offset. Stimulation by one range of sound frequencies caused adaptation that generalized across the entire broad range of frequencies to which these units responded. Identical stimuli were used to test adaptation in the lateral shell of the central nucleus of the inferior colliculus (ICCls), which provides input directly to the ICX. Compared with ICX adaptation, adaptation in the ICCls was substantially weaker, shorter lasting, and far more frequency specific, suggesting that part of the adaptation observed in the ICX was attributable to processes resident to the ICX. The sharp tuning of ICX neurons to space, along with their broad tuning to frequency, allows ICX adaptation to preserve a representation of stimulus location, regardless of the frequency content of the sound. The ICX is known to be a site of visually guided auditory map plasticity. ICX adaptation could play a role in this cross-modal plasticity by providing a short-term memory of the representation of auditory localization cues that could be compared with later-arriving, visual–spatial information from bimodal stimuli.


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