Abstract
GABA-ergic interneurons provide diverse inhibitions that are essential for the operation of neuronal circuits in the neocortex. However, the mechanisms that control the functional organization of neocortical interneurons remain largely unknown. Here we show that developmental origins influence fine-scale synapse formation and microcircuit assembly of neocortical interneurons. Spatially clustered neocortical interneurons originating from low-titre retrovirus-infected radial glial progenitors in the embryonic medial ganglionic eminence and preoptic area preferentially develop electrical, but not chemical, synapses with each other. This lineage-related electrical coupling forms predominantly between the same interneuron subtype over an extended postnatal period and across a range of distances, and promotes action potential generation and synchronous firing. Interestingly, this selective electrical coupling relates to a coordinated inhibitory chemical synapse formation between sparsely labelled interneurons in clusters and the same nearby excitatory neurons. These results suggest a link between the lineage relationship of neocortical interneurons and their precise functional organization.
Highlights
We did not observe any obvious pattern of chemical synaptic connectivity or electrical coupling between FS/non-FS pairs that account for B40% sparsely labelled interneuron pairs
The electrical coupling between sparsely labelled interneuron pairs in clusters starts to form around P7–P10 and the rate continues to increase even after P22. These results suggest that there are two electrical coupling interneuron networks in the neocortex, a short distance network that is not related to the lineage relationship and forms within a narrow window of time, and a long distance network that is related to the lineage relationship and forms over a prolonged period of time
It is important to emphasize that this specific connectivity between inhibitory and excitatory neurons appears to depend on both lineage relationship and electrical coupling of inhibitory interneurons, as neither non-electrically coupled, sparsely labelled interneurons in clusters nor electrically coupled, non-clonally related interneurons exhibit this feature of synaptic connectivity
Summary
Our study uncovers specific synaptic connectivity between neocortical interneurons related to their development origin and demonstrates that this specificity is selective for electrical, but not chemical, synapses. We detected electrical and/or chemical synaptic connections between sparsely labelled interneurons in clusters.
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