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Dynamic shifts in the owl's auditory space map predict moving sound location

Abstract

The optic tectum of the barn owl contains a map of auditory space. We found that, in response to moving sounds, the locations of receptive fields that make up the map shifted toward the approaching sound. The magnitude of the receptive field shifts increased systematically with increasing stimulus velocity and, therefore, was appropriate to compensate for sensory and motor delays inherent to auditory orienting behavior. Thus, the auditory space map is not static, but shifts adaptively and dynamically in response to stimulus motion. We provide a computational model to account for these results. Because the model derives predictive responses from processes that are known to occur commonly in neural networks, we hypothesize that analogous predictive responses will be found to exist widely in the central nervous system. This hypothesis is consistent with perceptions of stimulus motion in humans for many sensory parameters.

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Figure 1: Predictive shifts in spatiotemporal receptive fields in response to stimulus motion (80 μs ITD per s) for a single optic tectum unit.
Figure 2: Predictive shifts in spatiotemporal receptive fields in response to stimulus motion for the population.
Figure 3: Predictive shifts of the leading and lagging edges of the receptive field measured at 80 μs ITD per s.
Figure 4: Receptive field shifts increase with stimulus velocity.
Figure 5: Computational model reproduces receptive field shifts.
Figure 6: Effects of an excitatory or inhibitory priming stimulus on responses to a subsequent test stimulus.

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Acknowledgements

We thank S. Baccus, R. Aldrich, A. Keuroghlian, D. Winkowski and K. Maczko for helpful comments on this paper, and P. Knudsen for technical assistance. I.B.W. and J.F.B. are recipients of National Science Foundation graduate research fellowships. J.F.B. is a recipient of a National Research Service Award. Support for the experiments came from the US National Institutes of Health.

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E.I.K., J.F.B. and I.B.W. conceived the experiments and wrote the paper. J.F.B. and I.B.W. performed the experiments. J.F.B. performed the data analysis and statistics. I.B.W. developed the computational model.

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Correspondence to Eric I Knudsen.

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The authors declare no competing financial interests.

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Witten, I., Bergan, J. & Knudsen, E. Dynamic shifts in the owl's auditory space map predict moving sound location. Nat Neurosci 9, 1439–1445 (2006). https://doi.org/10.1038/nn1781

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