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A disinhibitory microcircuit for associative fear learning in the auditory cortex

Author

Listed:
  • Johannes J. Letzkus

    (Friedrich Miescher Institute for Biomedical Research)

  • Steffen B. E. Wolff

    (Friedrich Miescher Institute for Biomedical Research
    University of Basel)

  • Elisabeth M. M. Meyer

    (Friedrich Miescher Institute for Biomedical Research
    University of Basel)

  • Philip Tovote

    (Friedrich Miescher Institute for Biomedical Research)

  • Julien Courtin

    (INSERM U862, Neurocentre Magendie)

  • Cyril Herry

    (INSERM U862, Neurocentre Magendie)

  • Andreas Lüthi

    (Friedrich Miescher Institute for Biomedical Research)

Abstract

Learning causes a change in how information is processed by neuronal circuits. Whereas synaptic plasticity, an important cellular mechanism, has been studied in great detail, we know much less about how learning is implemented at the level of neuronal circuits and, in particular, how interactions between distinct types of neurons within local networks contribute to the process of learning. Here we show that acquisition of associative fear memories depends on the recruitment of a disinhibitory microcircuit in the mouse auditory cortex. Fear-conditioning-associated disinhibition in auditory cortex is driven by foot-shock-mediated cholinergic activation of layer 1 interneurons, in turn generating inhibition of layer 2/3 parvalbumin-positive interneurons. Importantly, pharmacological or optogenetic block of pyramidal neuron disinhibition abolishes fear learning. Together, these data demonstrate that stimulus convergence in the auditory cortex is necessary for associative fear learning to complex tones, define the circuit elements mediating this convergence and suggest that layer-1-mediated disinhibition is an important mechanism underlying learning and information processing in neocortical circuits.

Suggested Citation

  • Johannes J. Letzkus & Steffen B. E. Wolff & Elisabeth M. M. Meyer & Philip Tovote & Julien Courtin & Cyril Herry & Andreas Lüthi, 2011. "A disinhibitory microcircuit for associative fear learning in the auditory cortex," Nature, Nature, vol. 480(7377), pages 331-335, December.
  • Handle: RePEc:nat:nature:v:480:y:2011:i:7377:d:10.1038_nature10674
    DOI: 10.1038/nature10674
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    Citations

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    Cited by:

    1. Athina Tzovara & Christoph W Korn & Dominik R Bach, 2018. "Human Pavlovian fear conditioning conforms to probabilistic learning," PLOS Computational Biology, Public Library of Science, vol. 14(8), pages 1-21, August.
    2. Xu Zhan & Chao Chen & Longgang Niu & Xinran Du & Ying Lei & Rui Dan & Zhao-Wen Wang & Ping Liu, 2023. "Locomotion modulates olfactory learning through proprioception in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    3. Allen P. F. Chen & Jeffrey M. Malgady & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Joshua L. Plotkin & Shaoyu Ge & Qiaojie Xiong, 2022. "Nigrostriatal dopamine pathway regulates auditory discrimination behavior," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Matteo Farinella & Daniel T Ruedt & Padraig Gleeson & Frederic Lanore & R Angus Silver, 2014. "Glutamate-Bound NMDARs Arising from In Vivo-like Network Activity Extend Spatio-temporal Integration in a L5 Cortical Pyramidal Cell Model," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-21, April.
    5. Katherine C. Wood & Christopher F. Angeloni & Karmi Oxman & Claudia Clopath & Maria N. Geffen, 2022. "Neuronal activity in sensory cortex predicts the specificity of learning in mice," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Yanmei Liu & Jiahe Zhang & Zhishan Jiang & Meiling Qin & Min Xu & Siyu Zhang & Guofen Ma, 2024. "Organization of corticocortical and thalamocortical top-down inputs in the primary visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Angeliki Damilou & Linbi Cai & Ali Özgür Argunşah & Shuting Han & George Kanatouris & Maria Karatsoli & Olivia Hanley & Lorenzo Gesuita & Sepp Kollmorgen & Fritjof Helmchen & Theofanis Karayannis, 2024. "Developmental Cajal-Retzius cell death contributes to the maturation of layer 1 cortical inhibition and somatosensory processing," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Shiva Farashahi & Alireza Soltani, 2021. "Computational mechanisms of distributed value representations and mixed learning strategies," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    9. Robert Legenstein & Wolfgang Maass, 2014. "Ensembles of Spiking Neurons with Noise Support Optimal Probabilistic Inference in a Dynamically Changing Environment," PLOS Computational Biology, Public Library of Science, vol. 10(10), pages 1-27, October.
    10. Allen P. F. Chen & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Shaoyu Ge & Qiaojie Xiong, 2023. "Nigrostriatal dopamine modulates the striatal-amygdala pathway in auditory fear conditioning," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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