Scaling of Topologically Similar Functional Modules Defines Mouse Primary Auditory and Somatosensory Microcircuitry

Abstract

Mapping the flow of activity through neocortical microcircuits provides key insights into the underlying circuit architecture. Using a comparative analysis we determined the extent to which the dynamics of microcircuits in mouse primary somatosensory barrel field (S1BF) and auditory (A1) neocortex generalize. We imaged the simultaneous dynamics of up to 1126 neurons spanning multiple columns and layers using high-speed multiphoton imaging. The temporal progression and reliability of reactivation of circuit events in both regions suggested common underlying cortical design features. We used circuit activity flow to generate functional connectivity maps, or graphs, to test the microcircuit hypothesis within a functional framework. S1BF and A1 present a useful test of the postulate as both regions map sensory input anatomically, but each area appears organized according to different design principles. We projected the functional topologies into anatomical space and found benchmarks of organization that had been previously described using physiology and anatomical methods, consistent with a close mapping between anatomy and functional dynamics. By comparing graphs representing activity flow we found that each region is similarly organized as highlighted by hallmarks of small world, scale free, and hierarchical modular topologies. Models of prototypical functional circuits from each area of cortex were sufficient to recapitulate experimentally observed circuit activity. Convergence to common behavior by these models was accomplished using preferential attachment to scale from an auditory up to a somatosensory circuit. These functional data imply that the microcircuit hypothesis be framed as scalable principles of neocortical circuit design.

Spontaneous activations follow a common developmental course across primary sensory areas in mouse neocortex

“…Spontaneous circuit events began as local recruitments of spatially contiguous neighborhoods of on the order of 5% of cells and then expanded on PND 9 to include global activations of up to 80% of the cells, spread over the whole field of view. Finally, after PND 14 events became sparse, still drawing from the whole field of view but recruiting only 25 Ϯ 11% of the cells per event, as reported previously (Sadovsky and MacLean 2013).…”

“…It is known that functional graphs describing the activity structure of adolescent cortex show a high degree of modularity compared with matched Erdłos-Rényi random graphs (Sadovsky and MacLean 2013). Whether this is also true prior to adolescence is unknown, as is the developmental trajectory of functional modularity.…”

“…Graphs reflecting the single-frame time-lagged activity correlation between cell pairs were constructed as described in Sadovsky and MacLean (2013). The element-wise inverses of the adjacency matrices of these graphs defined the functional distance matrices used to compute shortest internode path distances.…”

Multineuronal activity patterns identify selective synaptic connections under realistic experimental constraints

“…Isolating activity within a single input context (trials with the same input projection topology), 36 Ϯ 0.98% of model neurons were never active. With the inclusion of many input contexts over the entire simulation, only 14.5% of model neurons were inactive, recapitulating experimental data (Sadovsky and MacLean 2013). Naturally, unresponsive neurons, which do not participate in propagating circuit activity, do not give rise to functional relationships.…”

“…Nevertheless, correlation has been shown to indicate an enhanced likelihood that neurons are synaptically connected (Ko et al 2011). A select fraction of pairwise spike timing relationships are highly reliable (Sadovsky and MacLean 2013) and do not arise by chance. These strong statistical dependencies may be particularly informative of the underlying synaptic connections that produce them.…”