Molecular programs guiding arealization of descending cortical pathways

Nature. 2024 Oct;634(8034):644-651. doi: 10.1038/s41586-024-07895-y. Epub 2024 Sep 11.

Abstract

Layer 5 extratelencephalic (ET) neurons are present across neocortical areas and send axons to multiple subcortical targets1-6. Two cardinal subtypes exist7,8: (1) Slco2a1-expressing neurons (ETdist), which predominate in the motor cortex and project distally to the pons, medulla and spinal cord; and (2) Nprs1- or Hpgd-expressing neurons (ETprox), which predominate in the visual cortex and project more proximally to the pons and thalamus. An understanding of how area-specific ETdist and ETprox emerge during development is important because they are critical for fine motor skills and are susceptible to spinal cord injury and amyotrophic lateral sclerosis9-12. Here, using cross-areal mapping of axonal projections in the mouse neocortex, we identify the subtype-specific developmental dynamics of ET neurons. Whereas subsets of ETprox emerge by pruning of ETdist axons, others emerge de novo. We outline corresponding subtype-specific developmental transcriptional programs using single-nucleus sequencing. Leveraging these findings, we use postnatal in vivo knockdown of subtype-specific transcription factors to reprogram ET neuron connectivity towards more proximal targets. Together, these results show the functional transcriptional programs driving ET neuron diversity and uncover cell subtype-specific gene regulatory networks that can be manipulated to direct target specificity in motor corticofugal pathways.

MeSH terms

  • Animals
  • Axons / metabolism
  • Female
  • Gene Expression Regulation, Developmental
  • Male
  • Mice
  • Motor Cortex / cytology
  • Motor Cortex / metabolism
  • Neocortex* / anatomy & histology
  • Neocortex* / cytology
  • Neocortex* / metabolism
  • Neural Pathways*
  • Neurons* / cytology
  • Neurons* / metabolism
  • Single-Cell Gene Expression Analysis
  • Transcription Factors / metabolism

Substances

  • Transcription Factors