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The organization of intracortical connections by layer and cell class in the mouse brain

Julie A. Harris, Stefan Mihalas, Karla E. Hirokawa, Jennifer D. Whitesell, Joseph E. Knox, Amy Bernard, Phillip Bohn, Shiella Caldejon, Linzy Casal, Andrew Cho, David Feng, Nathalie Gaudreault, Charles R. Gerfen, Nile Graddis, Peter A. Groblewski, Alex Henry, Anh Ho, Robert Howard, Leonard Kuan, Jerome Lecoq, Jennifer Luviano, Stephen McConoghy, Marty T. Mortrud, Maitham Naeemi, Lydia Ng, Seung W. Oh, Benjamin Ouellette, Staci A. Sorensen, Wayne Wakeman, Quanxin Wang, Ali Williford, John W. Phillips, Allan Jones, Christof Koch, Hongkui Zeng
doi: https://doi.org/10.1101/292961
Julie A. Harris
1Allen Institute for Brain Science
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  • For correspondence: julieha@alleninstitute.org
Stefan Mihalas
1Allen Institute for Brain Science
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Karla E. Hirokawa
1Allen Institute for Brain Science
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Jennifer D. Whitesell
1Allen Institute for Brain Science
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Joseph E. Knox
1Allen Institute for Brain Science
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Amy Bernard
1Allen Institute for Brain Science
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Phillip Bohn
1Allen Institute for Brain Science
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Shiella Caldejon
1Allen Institute for Brain Science
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Linzy Casal
1Allen Institute for Brain Science
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Andrew Cho
1Allen Institute for Brain Science
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David Feng
1Allen Institute for Brain Science
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Nathalie Gaudreault
1Allen Institute for Brain Science
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Charles R. Gerfen
2Laboratory of Systems Neuroscience, National Institute of Mental Health
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Nile Graddis
1Allen Institute for Brain Science
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Peter A. Groblewski
1Allen Institute for Brain Science
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Alex Henry
1Allen Institute for Brain Science
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Anh Ho
1Allen Institute for Brain Science
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Robert Howard
1Allen Institute for Brain Science
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Leonard Kuan
1Allen Institute for Brain Science
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Jerome Lecoq
1Allen Institute for Brain Science
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Jennifer Luviano
1Allen Institute for Brain Science
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Stephen McConoghy
1Allen Institute for Brain Science
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Marty T. Mortrud
1Allen Institute for Brain Science
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Maitham Naeemi
1Allen Institute for Brain Science
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Lydia Ng
1Allen Institute for Brain Science
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Seung W. Oh
1Allen Institute for Brain Science
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Benjamin Ouellette
1Allen Institute for Brain Science
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Staci A. Sorensen
1Allen Institute for Brain Science
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Wayne Wakeman
1Allen Institute for Brain Science
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Quanxin Wang
1Allen Institute for Brain Science
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Ali Williford
1Allen Institute for Brain Science
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John W. Phillips
1Allen Institute for Brain Science
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Allan Jones
1Allen Institute for Brain Science
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Christof Koch
1Allen Institute for Brain Science
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Hongkui Zeng
1Allen Institute for Brain Science
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Abstract

The mammalian cortex is a laminar structure composed of many cell types densely interconnected in complex ways. Recent systematic efforts to map the mouse mesoscale connectome provide comprehensive projection data on interareal connections, but not at the level of specific cell classes or layers within cortical areas. We present here a significant expansion of the Allen Mouse Brain Connectivity Atlas, with ∼1,000 new axonal projection mapping experiments across nearly all isocortical areas in 49 Cre driver lines. Using 13 lines selective for cortical layer-specific projection neuron classes, we identify the differential contribution of each layer/class to the overall intracortical connectivity patterns. We find layer 5 (L5) projection neurons account for essentially all intracortical outputs. L2/3, L4, and L6 neurons contact a subset of the L5 cortical targets. We also describe the most common axon lamination patterns in cortical targets. Most patterns are consistent with previous anatomical rules used to determine hierarchical position between cortical areas (feedforward, feedback), with notable exceptions. While diverse target lamination patterns arise from every source layer/class, L2/3 and L4 neurons are primarily associated with feedforward type projection patterns and L6 with feedback. L5 has both feedforward and feedback projection patterns. Finally, network analyses revealed a modular organization of the intracortical connectome. By labeling interareal and intermodule connections as feedforward or feedback, we present an integrated view of the intracortical connectome as a hierarchical network.

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Posted April 18, 2018.
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The organization of intracortical connections by layer and cell class in the mouse brain
Julie A. Harris, Stefan Mihalas, Karla E. Hirokawa, Jennifer D. Whitesell, Joseph E. Knox, Amy Bernard, Phillip Bohn, Shiella Caldejon, Linzy Casal, Andrew Cho, David Feng, Nathalie Gaudreault, Charles R. Gerfen, Nile Graddis, Peter A. Groblewski, Alex Henry, Anh Ho, Robert Howard, Leonard Kuan, Jerome Lecoq, Jennifer Luviano, Stephen McConoghy, Marty T. Mortrud, Maitham Naeemi, Lydia Ng, Seung W. Oh, Benjamin Ouellette, Staci A. Sorensen, Wayne Wakeman, Quanxin Wang, Ali Williford, John W. Phillips, Allan Jones, Christof Koch, Hongkui Zeng
bioRxiv 292961; doi: https://doi.org/10.1101/292961
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The organization of intracortical connections by layer and cell class in the mouse brain
Julie A. Harris, Stefan Mihalas, Karla E. Hirokawa, Jennifer D. Whitesell, Joseph E. Knox, Amy Bernard, Phillip Bohn, Shiella Caldejon, Linzy Casal, Andrew Cho, David Feng, Nathalie Gaudreault, Charles R. Gerfen, Nile Graddis, Peter A. Groblewski, Alex Henry, Anh Ho, Robert Howard, Leonard Kuan, Jerome Lecoq, Jennifer Luviano, Stephen McConoghy, Marty T. Mortrud, Maitham Naeemi, Lydia Ng, Seung W. Oh, Benjamin Ouellette, Staci A. Sorensen, Wayne Wakeman, Quanxin Wang, Ali Williford, John W. Phillips, Allan Jones, Christof Koch, Hongkui Zeng
bioRxiv 292961; doi: https://doi.org/10.1101/292961

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