Intracortical circuits of pyramidal neurons reflect their long-range axonal targets

Abstract

The cerebral cortex is often viewed as a sparsely connected network of neurons. Using quadruple whole-cell recordings, Solange Brown and Shaul Hestrin have now tested for synaptic connections among heterogeneous populations of cortical excitatory cells — pyramidal neurons. Their results reveal highly connected local circuits of neurons, each reflecting the neurons' long-range projections to a different brain region. The findings illustrate a diversity of dense cortical microcircuitry associated with the variety of information streams that produce our repertoire of behaviours and internal states. Using quadruple whole-cell recordings, this study tested for synaptic connections among heterogeneous populations of cortical excitatory cells (pyramidal neurons), and found highly connected local circuits of neurons, each reflecting the neurons' long-range projections to a different brain region. The findings illustrate a diversity of dense cortical microcircuitry associated with the variety of information streams that produce our repertoire of behaviours and internal states. Cortical columns generate separate streams of information that are distributed to numerous cortical and subcortical brain regions1. We asked whether local intracortical circuits reflect these different processing streams by testing whether the intracortical connectivity among pyramidal neurons reflects their long-range axonal targets. We recorded simultaneously from up to four retrogradely labelled pyramidal neurons that projected to the superior colliculus, the contralateral striatum or the contralateral cortex to assess their synaptic connectivity. Here we show that the probability of synaptic connection depends on the functional identities of both the presynaptic and postsynaptic neurons. We first found that the frequency of monosynaptic connections among corticostriatal pyramidal neurons is significantly higher than among corticocortical or corticotectal pyramidal neurons. We then show that the probability of feed-forward connections from corticocortical neurons to corticotectal neurons is approximately three- to fourfold higher than the probability of monosynaptic connections among corticocortical or corticotectal cells. Moreover, we found that the average axodendritic overlap of the presynaptic and postsynaptic pyramidal neurons could not fully explain the differences in connection probability that we observed. The selective synaptic interactions we describe demonstrate that the organization of local networks of pyramidal cells reflects the long-range targets of both the presynaptic and postsynaptic neurons.