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

Abstract

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.

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Figure 1: Different frequencies of monosynaptic connections between corticotectal, corticostriatal or corticocortical neurons.
Figure 2: The probability of connection depends on the identities of the presynaptic and the postsynaptic pyramidal cell types.
Figure 3: The average axonal and dendritic architecture alone cannot explain differences in the connection probability.

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Acknowledgements

We thank J. Li and S. Pak for technical assistance. This work was supported by National Institutes of Health grants to S.P.B and to S.H.

Author Contributions S.P.B. and S.H. designed the experiments. S.P.B. collected the data and S.P.B. and S.H. performed the analyses. S.P.B. and S.H. wrote the paper.

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Correspondence to Shaul Hestrin.

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Brown, S., Hestrin, S. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457, 1133–1136 (2009). https://doi.org/10.1038/nature07658

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