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A new cellular mechanism for coupling inputs arriving at different cortical layers

Author

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  • Matthew E. Larkum

    (Abt. Zellphysiologie, Max-Planck-Institut für Medizinische Forschung)

  • J. Julius Zhu

    (Abt. Zellphysiologie, Max-Planck-Institut für Medizinische Forschung)

  • Bert Sakmann

    (Abt. Zellphysiologie, Max-Planck-Institut für Medizinische Forschung)

Abstract

Pyramidal neurons in layer 5 of the neocortex of the brain extend their axons and dendrites into all layers. They are also unusual in having both an axonal and a dendritic zone for the initiation of action potentials1,2,3,4,5,6. Distal dendritic inputs, which normally appear greatly attenuated at the axon, must cross a high threshold at the dendritic initiation zone to evoke calcium action potentials1,7 but can then generate bursts of axonal action potentials. Here we show that a single back-propagating sodium action potential generated in the axon8 facilitates the initiation of these calcium action potentials when it coincides with distal dendritic input within a time window of several milliseconds. Inhibitory dendritic input can selectively block the initiation of dendritic calcium action potentials, preventing bursts of axonal action potentials. Thus, excitatory and inhibitory postsynaptic potentials arising in the distal dendrites can exert significantly greater control over action potential initiation in the axon than would be expected from their electrotonically isolated locations. The coincidence of a single back-propagating action potential with a subthreshold distal excitatory postsynaptic potential to evoke a burst of axonal action potentials represents a new mechanism by which the main cortical output neurons can associate inputs arriving at different cortical layers.

Suggested Citation

  • Matthew E. Larkum & J. Julius Zhu & Bert Sakmann, 1999. "A new cellular mechanism for coupling inputs arriving at different cortical layers," Nature, Nature, vol. 398(6725), pages 338-341, March.
  • Handle: RePEc:nat:nature:v:398:y:1999:i:6725:d:10.1038_18686
    DOI: 10.1038/18686
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    Cited by:

    1. Giuseppe Chindemi & Marwan Abdellah & Oren Amsalem & Ruth Benavides-Piccione & Vincent Delattre & Michael Doron & András Ecker & Aurélien T. Jaquier & James King & Pramod Kumbhar & Caitlin Monney & Ro, 2022. "A calcium-based plasticity model for predicting long-term potentiation and depression in the neocortex," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Etay Hay & Sean Hill & Felix Schürmann & Henry Markram & Idan Segev, 2011. "Models of Neocortical Layer 5b Pyramidal Cells Capturing a Wide Range of Dendritic and Perisomatic Active Properties," PLOS Computational Biology, Public Library of Science, vol. 7(7), pages 1-18, July.
    3. 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.
    4. Jan C. Frankowski & Alexa Tierno & Shreya Pavani & Quincy Cao & David C. Lyon & Robert F. Hunt, 2022. "Brain-wide reconstruction of inhibitory circuits after traumatic brain injury," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Oren Amsalem & Hidehiko Inagaki & Jianing Yu & Karel Svoboda & Ran Darshan, 2024. "Sub-threshold neuronal activity and the dynamical regime of cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Arjun A. Bhaskaran & Théo Gauvrit & Yukti Vyas & Guillaume Bony & Melanie Ginger & Andreas Frick, 2023. "Endogenous noise of neocortical neurons correlates with atypical sensory response variability in the Fmr1−/y mouse model of autism," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Brandon R. Munn & Eli J. Müller & Vicente Medel & Sharon L. Naismith & Joseph T. Lizier & Robert D. Sanders & James M. Shine, 2023. "Neuronal connected burst cascades bridge macroscale adaptive signatures across arousal states," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Pierre Yger & Kenneth D Harris, 2013. "The Convallis Rule for Unsupervised Learning in Cortical Networks," PLOS Computational Biology, Public Library of Science, vol. 9(10), pages 1-16, October.
    9. Shan Shen & Xiaolong Jiang & Federico Scala & Jiakun Fu & Paul Fahey & Dmitry Kobak & Zhenghuan Tan & Na Zhou & Jacob Reimer & Fabian Sinz & Andreas S. Tolias, 2022. "Distinct organization of two cortico-cortical feedback pathways," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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