The distributed circuit within the piriform cortex makes odor discrimination robust

Abstract

Distributed circuits wherein connections between subcircuit components seem randomly distributed are common to the olfactory circuit, hippocampus, and cerebellum. In such circuits, activation patterns seem random too, showing no detectable spatial preference, and contrast with regions that have topographic connections between subcircuits and topographic activation patterns. Quantitative studies of topographic circuits in the neocortex have yielded common principles of organization. Whether distributed circuits share similar principles of organization is unknown because similar quantitative information is missing and understanding the way they encode information remains a challenge. We addressed these needs by providing a quantitative description of the mouse piriform cortex, a paleocortical distributed circuit that subserves olfaction. The quantitative information provided two insights. First, with a nearly parameter-free model of the olfactory circuit, we show that the piriform cortex robustly maintains odor information and discrimination ability present in the olfactory bulb. Second, the paleocortex is quantitatively different from the neocortex: it has a lower surface area density, which decreases from the anterior to posterior paleocortex contrasting with the uniform neuronal density of the neocortex. These insights might also apply to other distributed circuits.

Circuit-specific dendritic development in the piriform cortex

“…We assumed that upon odor exposure a maximum of 70 active synapses can arrive at a single neuronal dendrite. Following recent experimental measurements (Srinivasan and Stevens 2018), we considered 3700 glomeruli, 9.7x10⁷ synapses between all glomeruli and all layer 2 neurons and a total of 41000 layer 2 neurons. Hence, we dealt with an average 9.7x10⁷ / 41000 = 2366 synapses between all glomeruli and one neuron.…”

“…The average total dendritic branch length (1800 µm) was constant for all neurons. We estimated the layer 1a input density based on a recent comprehensive quantitative description of mouse piriform cortex (Srinivasan and Stevens 2018). Based on Srinivasan and Stevens, we extrapolated that the whole population of activated glomeruli would therefore activate 70 synapses on a layer 2b neuron, which we defined as the upper limit of coincident inputs.…”

“…These sensory-input sharing neighboring neurons have a high degree of local connectivity. In contrast, the PCx is a distributed, non-topographic circuit, where both the representation of sensory space and the recurrent connectivity are unpredictable and dispersed (Srinivasan and Stevens 2018). This diffuse organization of the palaeocortical PCx is likely to reflect the primordial structure of sensory cortices prior to the evolution of isocortex in synapsids and later mammals (Fournier et al 2015).…”

“…Functionally, the aPCx synthesizes the segregated peripheral input into odor objects and identifies them (Wilson and Sullivan 2011). Unlike topographically organized neocortical sensory systems, afferent sensory and recurrent connectivity in the aPCx lack any apparent spatial structure and are therefore non-topographical (Srinivasan and Stevens 2018).…”

Regenerative Failure Following Rat Neonatal Chorda Tympani Transection is Associated with Geniculate Ganglion Cell Loss and Terminal Field Plasticity in the Nucleus of the Solitary Tract

“…Sollars, unpublished observations), total ganglion cell counts were assessed. Since each neuron appeared on multiple sections, a soma was counted only when the nucleolus was clearly visible (Konigsmark, 1970;Miller et al, 1978;Srinivasan & Stevens, 2018). Cell counts were compared between the right (CTX) and left (intact) ganglia.…”