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

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


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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Mapping
  • Frontal Lobe / cytology
  • Frontal Lobe / physiology*
  • Mice
  • Motor Cortex / cytology
  • Motor Cortex / physiology*
  • Neural Pathways / physiology
  • Neural Stem Cells
  • Neuroanatomical Tract-Tracing Techniques
  • Neurons / physiology*
  • Somatosensory Cortex / cytology
  • Somatosensory Cortex / physiology*
  • Synapses