Cortical Layer 6b Persistent Subplate Neurons Reciprocally Connect Sensorimotor Areas and Inversely Reflect Somatosensory Engagement

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Abstract

Persistent subplate neurons in layer 6b (L6b) of the cerebral cortex have long been assumed to be a passive remnant of early development. Recent findings are challenging this concept, but the functional role of L6b remains mysterious. A large group of L6b neurons express Connective Tissue Growth Factor (Ctgf). Here, we mapped L6b Ctgf neurons throughout the cortex and found the highest density in primary sensorimotor areas. Cortical L6b Ctgf projections are ipsilaterally restricted and origin-site specific, with notable reciprocity, whereas innervation of the thalamus is modality-matched. L6b Ctgf neurons are electrically diverse and form excitatory synapses with both pyramidal cells and interneurons. In freely moving mice, these neurons are highly active and have prominent task-specific and temporally locked responses to external stimuli. These responses are dominated by paradoxical population silencing with escalating task engagement. Thus, L6b Ctgf neurons may keep cortical ensembles in a state of alertness and available to process cognate stimuli.

HIGHLIGHTS

  • L6b Ctgf neurons form origin-and layer-specific ipsilateral cortical connections.

  • Electrically heterogeneous L6b Ctgf neurons excite multiple classes of cortical neurons.

  • Barrel cortex L6b Ctgf neurons are highly active in freely moving mice.

  • Somatosensory exploration paradoxically silences active barrel cortex L6b Ctgf neurons.

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