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Top-down gain control of the auditory space map by gaze control circuitry in the barn owl

Nature volume 439, pages 336–339 (2006)Cite this article

Abstract

High-level circuits in the brain that control the direction of gaze are intimately linked with the control of visual spatial attention1,2,3,4,5. Immediately before an animal directs its gaze towards a stimulus, both psychophysical sensitivity to that visual stimulus and the responsiveness of high-order neurons in the cerebral cortex that represent the stimulus increase dramatically3,6,7. Equivalent effects on behavioural sensitivity and neuronal responsiveness to visual stimuli result from focal electrical microstimulation of gaze control centres in monkeys8,9,10,11. Whether the gaze control system modulates neuronal responsiveness in sensory modalities other than vision is unknown. Here we show that electrical microstimulation applied to gaze control circuitry in the forebrain of barn owls regulates the gain of midbrain auditory responses in an attention-like manner. When the forebrain circuit was activated, midbrain responses to auditory stimuli at the location encoded by the forebrain site were enhanced and spatial selectivity was sharpened. The same stimulation suppressed responses to auditory stimuli represented at other locations in the midbrain map. Such space-specific, top-down regulation of auditory responses by gaze control circuitry in the barn owl suggests that the central nervous system uses a common strategy for dynamically regulating sensory gain that applies across modalities, brain areas and classes of vertebrate species. This approach provides a path for discovering mechanisms that underlie top-down gain control in the central nervous system.

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Figure 1: Effect of electrical microstimulation in the AGF on auditory responses at an aligned site in the optic tectum.
Figure 2: Effect of AGF microstimulation on a non-aligned site in the optic tectum.
Figure 3: Summary of the effects of AGF microstimulation on auditory responses in the optic tectum.

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Acknowledgements

We thank J. Bergan, M. Cohen, K. Maczko, T. Moore and I. Witten for reviews of earlier versions of the manuscript, and P. Knudsen for technical assistance. This work was supported by grants from the National Institutes of Health (E.I.K.) and an NRSA postdoctoral fellowship (D.E.W.) Author Contributions D.E.W. and E.I.K. designed the experiment and co-wrote the paper. D.E.W. carried out the electrophysiological recordings and data analysis.

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  1. Department of Neurobiology, Stanford University, California, 94305, Stanford, USA

    Daniel E. Winkowski & Eric I. Knudsen

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  1. Daniel E. Winkowski
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Correspondence to Daniel E. Winkowski.

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Winkowski, D., Knudsen, E. Top-down gain control of the auditory space map by gaze control circuitry in the barn owl. Nature 439, 336–339 (2006). https://doi.org/10.1038/nature04411

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