Letter | Published:

Nonlinear dendritic integration of sensory and motor input during an active sensing task

Nature volume 492, pages 247251 (13 December 2012) | Download Citation

Abstract

Active dendrites provide neurons with powerful processing capabilities. However, little is known about the role of neuronal dendrites in behaviourally related circuit computations. Here we report that a novel global dendritic nonlinearity is involved in the integration of sensory and motor information within layer 5 pyramidal neurons during an active sensing behaviour. Layer 5 pyramidal neurons possess elaborate dendritic arborizations that receive functionally distinct inputs, each targeted to spatially separate regions1,2. At the cellular level, coincident input from these segregated pathways initiates regenerative dendritic electrical events that produce bursts of action potential output3,4 and circuits featuring this powerful dendritic nonlinearity can implement computations based on input correlation5. To examine this in vivo we recorded dendritic activity in layer 5 pyramidal neurons in the barrel cortex using two-photon calcium imaging in mice performing an object-localization task. Large-amplitude, global calcium signals were observed throughout the apical tuft dendrites when active touch occurred at particular object locations or whisker angles. Such global calcium signals are produced by dendritic plateau potentials that require both vibrissal sensory input and primary motor cortex activity. These data provide direct evidence of nonlinear dendritic processing of correlated sensory and motor information in the mammalian neocortex during active sensation.

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Acknowledgements

We thank L. Tian and L. Looger for GCaMP3 constructs; J. Chandrashekar, N. Ryba and C. Zuker for GCaMP3 transgenic mice; W. Denk for comments on the manuscript; N. Clack, G. Myers, T. Zhao, V. Iyer, S. Peron and S. Drukmann for help with software and analysis; and L. Petreanu for help with experimental apparatus. S.R.W. is supported by the Australian research council (FT100100502) and Australian National Health and Medical Research Council (APP1004575).

Author information

Author notes

    • Daniel Huber
    •  & Daniel H. O’Connor

    Present addresses: Department of Basic Neurosciences, University of Geneva, CH-1211 Geneva, Switzerland (D.H.); Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA (D.H.O.).

Affiliations

  1. Howard Hughes Medical Institute, Janelia Farm Research Campus, Ashburn, Virginia 20147, USA

    • Ning-long Xu
    • , Mark T. Harnett
    • , Daniel Huber
    • , Daniel H. O’Connor
    • , Karel Svoboda
    •  & Jeffrey C. Magee
  2. Queensland Brain Institute, The University of Queensland, St Lucia, Queensland 4072, Australia

    • Stephen R. Williams

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Contributions

N.-L.X., K.S. and J.C.M. conceived the project and designed the experiments. N.-L.X. performed all behavioural and chronic imaging experiments, and data analysis. M.T.H. and S.R.W. carried out all in vitro experiments. J.C.M. performed in vivo dendritic recording experiments. D.H., D.H.O. and K.S. designed behavioural apparatus and whisker data-analysis code. N.-L.X. and J.C.M. wrote the paper with comments from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jeffrey C. Magee.

Supplementary information

PDF files

  1. 1.

    Supplementary Figures

    This file contains Supplementary Figures 1-12.

Videos

  1. 1.

    Active touch evoked global dendritic calcium signals

    This video shows synchronized two-photon image frames (left) and high-speed whisker video tracking frames of whisker trajectory (right). Dendritic ROIs belonging to the same neuron were outlined and overlaid on the two-photon images. The pole position is indicated by the gray circle on the right panel, the color changing to red indicates when the pole rose into the whisker plane.

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DOI

https://doi.org/10.1038/nature11601

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