Inhibitory Units: An Organizing Nidus for Feature-Selective Sub-Networks in Area V1

Sensory stimuli are encoded by the joint firing of neuronal groups composed of pyramidal cells and interneurons, rather than single isolated neurons (Uhlhaas et al, 2009, Buzsaki, 2010). However, the principles by which these groups are organized to encode information remain poorly understood. A leading hypothesis is that similarly tuned pyramidal cells that preferentially connect to each other may form multi-cellular encoding units yoked to a similar purpose. The existence of such groups would be reflected on the profile of spontaneous events observed in neocortical networks. We used 2-photon calcium imaging to study spontaneous population-burst events in layer 2/3 of mouse area V1 during postnatal maturation (postnatal day 8–52). Throughout the period examined both size and duration of spontaneously occurring population-bursts formed scale-free distributions obeying a power law. The same was true for the degree of “functional connectivity,” a measure of pairwise synchrony across cells. These observations are consistent with a hierarchical small-world-net architecture, characterized by groups of cells with high local connectivity (“small worlds”, cliques) connected to each other via a restricted number of “hub” cells” (Bonifazi et al., 2009, Sporns, 2011, Luce & Perry, 1949). To identify candidate “small world” groups we searched for cells whose calcium events had a consistent temporal relationship to events recorded from local inhibitory interneurons. This was guided by the intuition that groups of neurons whose synchronous firing represents a “temporally coherent computational unit” (or feature) ought to be inhibited together. This strategy allowed us to identify clusters of pyramidal neurons whose firing is temporally “linked” to one or more local interneurons. These “small-world” clusters did not remain static, during postnatal development: both cluster size and overlap with other clusters decreased over time as pyramidal neurons became progressively more selective, “linking” to fewer neighboring interneurons. Notably, pyramidal neurons in a cluster show higher tuning function similarity than expected with each other and with their “linked” interneurons. Our findings suggest that spontaneous population events in the visual cortex are shaped by “small-world” networks of pyramidal neurons that share functional properties and work in concert with one or more local interneurons. We argue that such groups represent a fundamental neocortical unit of computation at the population level.