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Distinct neural mechanisms construct classical versus extraclassical inhibitory surrounds in an inhibitory nucleus in the midbrain attention network

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  • Hannah M. Schryver

    (Johns Hopkins University
    Currently, Allen Institute)

  • Shreesh P. Mysore

    (Johns Hopkins University
    Johns Hopkins School of Medicine
    Johns Hopkins University)

Abstract

Inhibitory neurons in the midbrain spatial attention network, called isthmi pars magnocellularis (Imc), control stimulus selection by the sensorimotor and attentional hub, the optic tectum (OT). Here, we investigate in the barn owl how classical as well as extraclassical (global) inhibitory surrounds of Imc receptive fields (RFs), fundamental units of Imc computational function, are constructed. We find that focal, reversible blockade of GABAergic input onto Imc neurons disconnects their extraclassical inhibitory surrounds, but leaves intact their classical inhibitory surrounds. Subsequently, with paired recordings and iontophoresis, first at spatially aligned site-pairs in Imc and OT, and then, at mutually distant site-pairs within Imc, we demonstrate that classical inhibitory surrounds of Imc RFs are inherited from OT, but their extraclassical inhibitory surrounds are constructed within Imc. These results reveal key design principles of the midbrain spatial attention circuit and highlight the critical importance of competitive interactions within Imc for its operation.

Suggested Citation

  • Hannah M. Schryver & Shreesh P. Mysore, 2023. "Distinct neural mechanisms construct classical versus extraclassical inhibitory surrounds in an inhibitory nucleus in the midbrain attention network," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39073-5
    DOI: 10.1038/s41467-023-39073-5
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    References listed on IDEAS

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    1. Nagaraj R. Mahajan & Shreesh P. Mysore, 2022. "Donut-like organization of inhibition underlies categorical neural responses in the midbrain," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
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