A single-cell anatomical blueprint for intracortical information transfer from primary visual cortex

Abstract

The wiring diagram of the neocortex determines how information is processed across dozens of cortical areas. Each area communicates with multiple others via extensive long-range axonal projections^1–5, but the logic of inter-area information transfer remains unresolved. In sensory neocortex, previous work suggests that neurons typically innervate single cortical areas^3,5,6, implying that information is distributed via ensembles of dedicated pathways. Alternatively, single neurons could broadcast information to multiple cortical targets^6–9. Distinguishing between these models has been challenging because the projection patterns of only a few individual neurons have been reconstructed. Here we map the projection patterns of axonal arbors from 595 individual neurons in mouse primary visual cortex (V1) using two complementary methods: whole-brain fluorescence-based axonal tracing^10,11 and high-throughput DNA sequencing of genetically barcoded neurons (MAPseq)¹². Although our results confirm the existence of dedicated projections to certain cortical areas, we find these are the exception, and that the majority of V1 neurons broadcast information to multiple cortical targets. Furthermore, broadcasting cells do not project to all targets randomly, but rather comprise subpopulations that either avoid or preferentially innervate specific subsets of cortical areas. Our data argue against a model of dedicated lines of inter-areal information transfer via “one neuron – one target area” mapping. Instead, long-range communication between a sensory cortical area and its targets is based on a principle whereby individual neurons copy information to, and potentially coordinate activity across, specific subsets of cortical areas.