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A cortico-collicular circuit for orienting to shelter during escape

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Názov: A cortico-collicular circuit for orienting to shelter during escape
Autori: Dario Campagner, Ruben Vale, Yu Lin Tan, Panagiota Iordanidou, Oriol Pavón Arocas, Federico Claudi, A. Vanessa Stempel, Sepiedeh Keshavarzi, Rasmus S. Petersen, Troy W. Margrie, Tiago Branco
Zdroj: Campagner, D, Vale, R, Tan, Y L, Iordanidou, P, Pavón Arocas, O, Claudi, F, Stempel, A V, Keshavarzi, S, Petersen, R S, Margrie, T W & Branco, T 2023, 'A cortico-collicular circuit for orienting to shelter during escape', Nature, vol. 613, no. 7942, pp. 111-119. https://doi.org/10.1038/s41586-022-05553-9
Informácie o vydavateľovi: Springer Science and Business Media LLC, 2022.
Rok vydania: 2022
Predmety: Neurons, 0301 basic medicine, Superior Colliculi, 0303 health sciences, Time Factors, Escape Reaction/physiology, Spatial Navigation/physiology, Gyrus Cinguli/cytology, Gyrus Cinguli, Mice, 03 medical and health sciences, Escape Reaction, Predatory Behavior, Neural Pathways, Animals, Neurons/physiology, Goals, Superior Colliculi/cytology, Spatial Memory, Spatial Navigation
Popis: When faced with predatory threats, escape towards shelter is an adaptive action that offers long-term protection against the attacker. Animals rely on knowledge of safe locations in the environment to instinctively execute rapid shelter-directed escape actions1,2. Although previous work has identified neural mechanisms of escape initiation3,4, it is not known how the escape circuit incorporates spatial information to execute rapid flights along the most efficient route to shelter. Here we show that the mouse retrosplenial cortex (RSP) and superior colliculus (SC) form a circuit that encodes the shelter-direction vector and is specifically required for accurately orienting to shelter during escape. Shelter direction is encoded in RSP and SC neurons in egocentric coordinates and SC shelter-direction tuning depends on RSP activity. Inactivation of the RSP-SC pathway disrupts the orientation to shelter and causes escapes away from the optimal shelter-directed route, but does not lead to generic deficits in orientation or spatial navigation. We find that the RSP and SC are monosynaptically connected and form a feedforward lateral inhibition microcircuit that strongly drives the inhibitory collicular network because of higher RSP input convergence and synaptic integration efficiency in inhibitory SC neurons. This results in broad shelter-direction tuning in inhibitory SC neurons and sharply tuned excitatory SC neurons. These findings are recapitulated by a biologically constrained spiking network model in which RSP input to the local SC recurrent ring architecture generates a circular shelter-direction map. We propose that this RSP-SC circuit might be specialized for generating collicular representations of memorized spatial goals that are readily accessible to the motor system during escape, or more broadly, during navigation when the goal must be reached as fast as possible.
Druh dokumentu: Article
Jazyk: English
ISSN: 1476-4687
0028-0836
DOI: 10.1038/s41586-022-05553-9
Prístupová URL adresa: https://pubmed.ncbi.nlm.nih.gov/36544025
https://research.manchester.ac.uk/en/publications/eb6b2e93-33cf-404b-81f4-839c32ba137b
https://doi.org/10.1038/s41586-022-05553-9
https://www.mendeley.com/catalogue/f7451f7a-e1a3-3b72-875d-ac3064bc741f/
http://www.scopus.com/inward/record.url?scp=85144513756&partnerID=8YFLogxK
https://research.manchester.ac.uk/en/publications/eb6b2e93-33cf-404b-81f4-839c32ba137b
https://doi.org/10.1038/s41586-022-05553-9
https://discovery-pp.ucl.ac.uk/id/eprint/10162282/
Rights: Springer Nature TDM
Prístupové číslo: edsair.doi.dedup.....a6831cec1404a4a2908a03fe1b8e0b6b
Databáza: OpenAIRE
Popis
Abstrakt:When faced with predatory threats, escape towards shelter is an adaptive action that offers long-term protection against the attacker. Animals rely on knowledge of safe locations in the environment to instinctively execute rapid shelter-directed escape actions1,2. Although previous work has identified neural mechanisms of escape initiation3,4, it is not known how the escape circuit incorporates spatial information to execute rapid flights along the most efficient route to shelter. Here we show that the mouse retrosplenial cortex (RSP) and superior colliculus (SC) form a circuit that encodes the shelter-direction vector and is specifically required for accurately orienting to shelter during escape. Shelter direction is encoded in RSP and SC neurons in egocentric coordinates and SC shelter-direction tuning depends on RSP activity. Inactivation of the RSP-SC pathway disrupts the orientation to shelter and causes escapes away from the optimal shelter-directed route, but does not lead to generic deficits in orientation or spatial navigation. We find that the RSP and SC are monosynaptically connected and form a feedforward lateral inhibition microcircuit that strongly drives the inhibitory collicular network because of higher RSP input convergence and synaptic integration efficiency in inhibitory SC neurons. This results in broad shelter-direction tuning in inhibitory SC neurons and sharply tuned excitatory SC neurons. These findings are recapitulated by a biologically constrained spiking network model in which RSP input to the local SC recurrent ring architecture generates a circular shelter-direction map. We propose that this RSP-SC circuit might be specialized for generating collicular representations of memorized spatial goals that are readily accessible to the motor system during escape, or more broadly, during navigation when the goal must be reached as fast as possible.
ISSN:14764687
00280836
DOI:10.1038/s41586-022-05553-9