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Excitatory cortical neurons form fine-scale functional networks


The specificity of cortical neuron connections creates columns of functionally similar neurons spanning from the pia to the white matter1,2,3,4,5,6. Here we investigate whether there is an additional, finer level of specificity that creates subnetworks of excitatory neurons within functional columns. We tested for fine-scale specificity of connections to cortical layer 2/3 pyramidal neurons in rat visual cortex by using cross-correlation analyses of synaptic currents evoked by photostimulation. Recording simultaneously from adjacent layer 2/3 pyramidal cells, we find that when they are connected to each other (20% of all recorded pairs) they share common input from layer 4 and within layer 2/3. When adjacent layer 2/3 neurons are not connected to each other, they share very little (if any) common excitatory input from layers 4 and 2/3. In contrast, all layer 2/3 neurons share common excitatory input from layer 5 and inhibitory input from layers 2/3 and 4, regardless of whether they are connected to each other. Thus, excitatory connections from layer 4 to layer 2/3 and within layer 2/3 form fine-scale assemblies of selectively interconnected neurons; inhibitory connections and excitatory connections from layer 5 link neurons across these fine-scale subnetworks. Relatively independent subnetworks of excitatory neurons are therefore embedded within the larger-scale functional architecture; this allows neighbouring neurons to convey information more independently than suggested by previous descriptions of cortical circuitry.

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Figure 1: Cross-correlation analyses of photostimulation-evoked excitatory postsynaptic currents (EPSCs) simultaneously recorded in adjacent pairs of layer 2/3 pyramidal neurons.
Figure 2: Correlation probabilities for EPSCs and IPSCs in layer 2/3 pyramidal cell pairs.
Figure 3: Cross-correlation analyses of photostimulation-evoked inhibitory postsynaptic currents (IPSCs) simultaneously recorded in adjacent pairs of layer 2/3 pyramidal neurons.
Figure 4: Schematic diagram illustrating the organization of cortical connections proposed in this study.

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We are grateful for support from the National Institutes of Health. We thank Y. Komatsu and F. Briggs and members of the Callaway laboratory for discussions.

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Correspondence to Edward M. Callaway.

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The authors declare that they have no competing financial interests.

Supplementary information

Figure S1

Spatial resolution of photostimulation. (DOC 71 kb)

Figure S2

Timing of action potentials evoked by photostimulation. (DOC 111 kb)

Supplementary Data (DOC 31 kb)

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Yoshimura, Y., Dantzker, J. & Callaway, E. Excitatory cortical neurons form fine-scale functional networks. Nature 433, 868–873 (2005).

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