A blanket of inhibition: functional inferences from dense inhibitory connectivity

Abstract

The function of neocortical interneurons is still unclear, and, as often happens, one may be able to draw functional insights from considering the structure. In this spirit we describe recent structural results and discuss their potential functional implications. Most GABAergic interneurons innervate nearby pyramidal neurons very densely and without any apparent specificity, as if they were extending a 'blanket of inhibition', contacting pyramidal neurons often in an overlapping fashion. While subtypes of interneurons specifically target subcellular compartments of pyramidal cells, and they also target different layers selectively, they appear to treat all neighboring pyramidal cells the same and innervate them massively. We explore the functional implications and temporal properties of dense, overlapping inhibition by four interneuron populations.

Figure 1

Blanket inhibition by the different subtypes of interneurons. (a) Early blanket inhibition by PVs. (b) Early Blanket inhibition by ChCs. Right panel shows early activation of ChCs compared to PCs after layer 1 stimulation (copied with permission from [4]). (c) Late blanket inhibition by SOMs. (d) Slow blanket inhibition by NGFCs. Inset: Gray trace represents total inhibitory current while blue is a GABA_B receptor component and red is the difference. Green triangles represent PCs, and circles in each panel represent INs projecting to PCs. Traces shown in (a), (c), and (d) represent responses of PCs to IN inputs.

Figure 2

Functional roles of INs. (a) Lateral inhibition. (b) Input normalization. (c) INs decorrelate PC spiking. (d) Inhibitory trail reduces response to a second input. Lightning symbols indicate input along arrows. (ii) Simple temporal effect. Green triangles represent PCs and red circles represent INs. (ii) example of spatio-temporal effect. Here circles represent modules containing both INs and PCs, and arrows the spread of excitation; because of the inhibitory trail stimulation of a pathway at t₁, shortly before stimulation of another path at t₂ blocks the progress of the latter activity at the red cross and directs it instead to the blue direction.

Figure 3

Hole in inhibitory blanket. Orange cell represents a VIP disinhibiting a network through inhibition of a SOM. Green triangles represent PCs, and a light blue circles SOMs.