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Neuron. 2019 Oct 23;104(2):385-401.e3. doi: 10.1016/j.neuron.2019.06.028. Epub 2019 Jul 29.

Precise Long-Range Microcircuit-to-Microcircuit Communication Connects the Frontal and Sensory Cortices in the Mammalian Brain.

Author information

1
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USA; IDG/McGovern Institute for Brain Research, Tsinghua-Peking Joint Center for Life Sciences, Beijing Frontier Research Center of Biological Structures, School of Life Sciences, Tsinghua University, Beijing 100084, China.
2
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USA.
3
University Hospital Cologne, CECAD Research Centre, Joseph-Stelzmann-Str. 26, 50931 Cologne, Germany.
4
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USA; IDG/McGovern Institute for Brain Research, Tsinghua-Peking Joint Center for Life Sciences, Beijing Frontier Research Center of Biological Structures, School of Life Sciences, Tsinghua University, Beijing 100084, China. Electronic address: shis@mskcc.org.

Abstract

The frontal area of the cerebral cortex provides long-range inputs to sensory areas to modulate neuronal activity and information processing. These long-range circuits are crucial for accurate sensory perception and complex behavioral control; however, little is known about their precise circuit organization. Here we specifically identified the presynaptic input neurons to individual excitatory neuron clones as a unit that constitutes functional microcircuits in the mouse sensory cortex. Interestingly, the long-range input neurons in the frontal but not contralateral sensory area are spatially organized into discrete vertical clusters and preferentially form synapses with each other over nearby non-input neurons. Moreover, the assembly of distant presynaptic microcircuits in the frontal area depends on the selective synaptic communication of excitatory neuron clones in the sensory area that provide inputs to the frontal area. These findings suggest that highly precise long-range reciprocal microcircuit-to-microcircuit communication mediates frontal-sensory area interactions in the mammalian cortex.

KEYWORDS:

columnar microcircuit; cortical circuit; excitatory neuron clone; in utero retroviral labeling; long-range circuit; quadruple whole-cell recording; rabies virus tracing; top-down modulation

PMID:
31371111
PMCID:
PMC6813886
[Available on 2020-10-23]
DOI:
10.1016/j.neuron.2019.06.028

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