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Stimulus-driven competition in a cholinergic midbrain nucleus

Abstract

The mechanisms by which the brain selects a particular stimulus as the next target for gaze are poorly understood. A cholinergic nucleus in the owl's midbrain exhibits functional properties that suggest its role in bottom-up stimulus selection. Neurons in the nucleus isthmi pars parvocellularis (Ipc) responded to wide ranges of visual and auditory features, but they were not tuned to particular values of those features. Instead, they encoded the relative strengths of stimuli across the entirety of space. Many neurons exhibited switch-like properties, abruptly increasing their responses to a stimulus in their receptive field when it became the strongest stimulus. This information propagates directly to the optic tectum, a structure involved in gaze control and stimulus selection, as periodic (25–50 Hz) bursts of cholinergic activity. The functional properties of Ipc neurons resembled those of a salience map, a core component in computational models for spatial attention and gaze control.

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Figure 1: Feature and modality independence of stimulus competition for a single nonswitch-like Ipc unit.
Figure 2: Effect of a competing looming stimulus on unit responses to a looming stimulus.
Figure 3: Effect of the strength of the Sin stimulus on switch value.
Figure 4: Global stimulus competition in the Ipc.
Figure 5: Periodicity of bursting responses of Ipc units.

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Acknowledgements

We thank P. Knudsen for technical support, C. Goddard and S. Devarajan for helpful discussions and T. Moore, B. Noudoost and N. Steinmets for reviewing the manuscript. This work was supported by grants from the US National Institutes of Health (R01 EY019179) to E.I.K.

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A.A., S.P.M. and E.I.K. designed the experiments and formulated the analysis. A.A. performed the experiments and data analysis. E.I.K. wrote the paper.

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Correspondence to Ali Asadollahi.

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The authors declare no competing financial interests.

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Supplementary Figures 1–5 and Supplementary Table 1 (PDF 644 kb)

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Asadollahi, A., Mysore, S. & Knudsen, E. Stimulus-driven competition in a cholinergic midbrain nucleus. Nat Neurosci 13, 889–895 (2010). https://doi.org/10.1038/nn.2573

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