Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity

Abstract

Excitatory cortical neurons form fine-scale networks of precisely interconnected neurons. Here we tested whether inhibitory cortical neurons in rat visual cortex might also be connected with fine-scale specificity. Using paired intracellular recordings and cross-correlation analyses of photostimulation-evoked synaptic currents, we found that fast-spiking interneurons preferentially connected to neighboring pyramids that provided them with reciprocal excitation. Furthermore, they shared common fine-scale excitatory input with neighboring pyramidal neurons only when the two cells were reciprocally connected, and not when there was no connection or a one-way, inhibitory-to-excitatory connection. Adapting inhibitory neurons shared little or no common input with neighboring pyramids, regardless of their direct connectivity. We conclude that inhibitory connections and also excitatory connections to inhibitory neurons can both be precise on a fine scale. Furthermore, fine-scale specificity depends on the type of inhibitory neuron and on direct connectivity between neighboring pyramidal-inhibitory neuron pairs.

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Figure 1: Direct connections between layer 2/3 inhibitory neuron–pyramidal neuron pairs.
Figure 2: Cross-correlation analyses of photostimulation-evoked EPSCs simultaneously recorded in adjacent layer 2/3 neuron pairs consisting of one pyramidal neuron and one fast-spiking inhibitory neuron (FS).
Figure 3: Correlation probabilities for EPSCs measured simultaneously in fast-spiking interneuron–pyramidal neuron pairs.
Figure 4: Cross-correlation analyses of photostimulation-evoked EPSCs simultaneously recorded in adjacent layer 2/3 neuron pairs consisting of one pyramidal neuron and one adapting inhibitory neuron (AD).
Figure 5: Correlation probabilities for EPSCs measured simultaneously in adapting interneuron–pyramidal neuron pairs.

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Acknowledgements

Supported by grants from the US National Institutes of Health (MH063912, EY010742) and from the Japanese Ministry of Education, Culture, Science, Sports and Technology (17023026, 17500208). We thank Y. Komatsu and H. Sato for discussions.

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Correspondence to Edward M Callaway.

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The authors declare no competing financial interests.

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Supplementary Fig. 1

Organization of cortical connections revealed by this study and incorporating data from a previous study. (PDF 580 kb)

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Yoshimura, Y., Callaway, E. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat Neurosci 8, 1552–1559 (2005). https://doi.org/10.1038/nn1565

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