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Journal Article

Inhibitory top-down projections from zona incerta mediate neocortical memory

MPS-Authors

Schroeder ,  Anna
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;
Institute for Physiology, Faculty of Medicine, University of Freiburg, 79108 Freiburg, Germany;

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Schuman,  Erin M.       
Synaptic Plasticity Department, Max Planck Institute for Brain Research, Max Planck Society;

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Citation

Schroeder, A., Pardi, M. B., Keijser, J., Dalmay, T., Groisman, A. I., Schuman, E. M., et al. (2023). Inhibitory top-down projections from zona incerta mediate neocortical memory. Neuron. doi:10.1016/j.neuron.2022.12.010.


Cite as: https://hdl.handle.net/21.11116/0000-000C-26BF-3
Abstract
Top-down projections convey a family of signals encoding previous experiences and current aims to the sensory neocortex, where they converge with external bottom-up information to enable perception and memory. Whereas top-down control has been attributed to excitatory pathways, the existence, connectivity, and information content of inhibitory top-down projections remain elusive. Here, we combine synaptic two-photon calcium imaging, circuit mapping, cortex-dependent learning, and chemogenetics in mice to identify GABAergic afferents from the subthalamic zona incerta as a major source of top-down input to the neocortex. Incertocortical transmission undergoes robust plasticity during learning that improves information transfer and mediates behavioral memory. Unlike excitatory pathways, incertocortical afferents form a disinhibitory circuit that encodes learned top-down relevance in a bidirectional manner where the rapid appearance of negative responses serves as the main driver of changes in stimulus representation. Our results therefore reveal the distinctive contribution of long-range (dis)inhibitory afferents to the computational flexibility of neocortical circuits.