Abstract
Author SummaryMany natural and engineered networks contain recurring patterns of local connectivity. Although these so-called network motifs are thought to have functional significance, direct tests of the idea that network topology reflects function remain scarce. We have performed such a test in the area of mammalian neocortex that is devoted to the sensory representation of touch. To this end, we equipped inhibitory interneurons in the mouse with light-activated ion channels that allowed us to stimulate interneuron activity optically and record light-evoked inhibitory currents in their postsynaptic partners, thereby revealing maps of connectivity. We find that excitatory pyramidal cells in layer 2/3 of primary somatosensory cortex receive inhibition from GABAergic interneurons located in different cortical layers, with a characteristic balance of inhibitory connections from deep and superficial layers. Trimming the whiskers to remove sensory input in adult animals alters this balance—inhibitory connections from deep cortical layers are depleted, while inhibitory connections from superficial layers are augmented. These changes revert when the whiskers regrow, restoring the original balance between wiring motifs. This see-saw relationship between deep and superficial inhibition demonstrates that mature cortical circuits adapt to functional change by selectively altering specific network motifs.
Highlights
Neocortex has a similar multilayered histology throughout [1,2], and different cortical areas are able to adapt, depending on their inputs, to the normal function of other regions [3]
A recent survey of inhibitory-toexcitatory wiring patterns in primary motor (M1), somatosensory (S1), and visual cortex (V1) of the mouse uncovered 25 interlaminar connection motifs common to all three regions [5]. Whereas most of these motifs were found at comparable frequencies in all cortical areas, the abundance of four motifs varied widely: ascending inhibition from layer 5B (L5B) to layer 2/3 (L2/3) and L4, as well as from L6 to L5B, was prominent in primary visual cortex (V1) and primary somatosensory cortex (S1), but not in primary motor cortex (M1); descending inhibition from L4 to L5A featured notably in S1
In agreement with recent observations in visual cortex [6,7,8,9], we found that sensory deprivation of adult barrel cortex induced changes in inhibitory circuits
Summary
Neocortex has a similar multilayered histology throughout [1,2], and different cortical areas are able to adapt, depending on their inputs, to the normal function of other regions [3] This versatility may reflect the existence of a ‘‘canonical’’ information-processing architecture, underpinned by stereotyped patterns of excitatory connectivity [2,4]. A recent survey of inhibitory-toexcitatory wiring patterns in primary motor (M1), somatosensory (S1), and visual cortex (V1) of the mouse uncovered 25 interlaminar connection motifs common to all three regions [5] Whereas most of these motifs were found at comparable frequencies in all cortical areas, the abundance of four motifs varied widely: ascending inhibition from layer 5B (L5B) to L2/3 and L4, as well as from L6 to L5B, was prominent in V1 and S1, but not in M1; descending inhibition from L4 to L5A featured notably in S1. These motifs may represent adaptations of a common blueprint to region-specific information-processing demands
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