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Top-down laminar organization of the excitatory network in motor cortex

Abstract

Cortical layering is a hallmark of the mammalian neocortex and a major determinant of local synaptic circuit organization in sensory systems. In motor cortex, the laminar organization of cortical circuits has not been resolved, although their input-output operations are crucial for motor control. Here, we developed a general approach for estimating layer-specific connectivity in cortical circuits and applied it to mouse motor cortex. From these data we computed a laminar presynaptic → postsynaptic connectivity matrix, Wpost,pre, revealing a complement of stereotypic pathways dominated by layer 2 outflow to deeper layers. Network modeling predicted, and experiments with disinhibited slices confirmed, that stimuli targeting upper, but not lower, cortical layers effectively evoked network-wide events. Thus, in motor cortex, descending excitation from a preamplifier-like network of upper-layer neurons drives output neurons in lower layers. Our analysis provides a quantitative wiring-diagram framework for further investigation of the excitatory networks mediating cortical mechanisms of motor control.

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Figure 1: Experimental approach.
Figure 2: Synaptic input and output in the local circuit.
Figure 3: Network activity in simulated circuits and disinhibited slices.
Figure 4: Wiring diagrams.

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Acknowledgements

We thank W. Kath, A. Stepanyants, K. Svoboda, M. Tresch, and J. Waters for comments and suggestions. We appreciate funding support provided through grants from the Whitehall Foundation, Simons Foundation and Rett Syndrome Research Foundation (G.M.G.S.).

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Contributions

Experiments were conducted by N.W., L.W., J.Y. and G.M.G.S., and simulations by S.A.S. and G.M.G.S. All authors participated in data analysis and interpretation. G.M.G.S. supervised the project and drafted the manuscript.

Corresponding author

Correspondence to Gordon M G Shepherd.

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The authors declare no competing financial interests.

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Weiler, N., Wood, L., Yu, J. et al. Top-down laminar organization of the excitatory network in motor cortex. Nat Neurosci 11, 360–366 (2008). https://doi.org/10.1038/nn2049

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