Recurrent cortical circuits implement concentration-invariant odor coding

Abstract

Animals rely on olfaction to find food, attract mates, and avoid predators. To support these behaviors, they must be able to identify odors across different odorant concentrations. The neural circuit operations that implement this concentration invariance remain unclear. We found that despite concentration-dependence in the olfactory bulb (OB), representations of odor identity were preserved downstream, in the piriform cortex (PCx). The OB cells responding earliest after inhalation drove robust responses in sparse subsets of PCx neurons. Recurrent collateral connections broadcast their activation across the PCx, recruiting global feedback inhibition that rapidly truncated and suppressed cortical activity for the remainder of the sniff, discounting the impact of slower, concentration-dependent OB inputs. Eliminating recurrent collateral output amplified PCx odor responses rendered the cortex steeply concentration-dependent and abolished concentration-invariant identity decoding.

Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception

“…Both the spatial identity or temporal latencies of glomeruli activated in the pattern may be perceptually meaningful (6,7), but the relative importance of each is unknown. It is also unclear what forms a perceptually-meaningful combination of glomerular activation: ordered sequences aligned relative to each other (10)(11)(12), sequences aligned to sniff rhythm (6,7,13,14), or the earliest activated subset of glomeruli within a sniff rhythm (15,16).…”

Robust odor coding across states in piriform cortex requires recurrent circuitry: evidence for pattern completion in an associative network

“…3, a and d). Thus, PCx could over-represent early inputs to produce a stable output 37 . Indeed, robust PCx responses had shorter latencies ( Fig.…”

“…To test this prediction, we injected conditional viral vectors to express tetanus toxin (AAV-DIO-GFP-TeLC) into PCx of emx1-Cre mice to express TeLC in all PCx excitatory neurons ( Fig. 4l), effectively converting PCx into a pure feedforward circuit driven by OB 37 . We then obtained simultaneous bilateral recordings from TeLC-infected and contralateral control PCx hemispheres before and during anesthesia.…”

“…4n). Because TeLC expression interferes with all PCx output, including strong feedback projections from PCx to OB inhibitory neurons, OB responses ipsilateral to TeLC-PCx can be substantially enhanced 37 , and may no longer present degraded input to PCx under anesthesia. Indeed, awake and anesthetized responses in OB ipsilateral to TeLC-PCx were decoded with equivalent accuracy, whereas simultaneous recordings from contralateral OB degraded under anesthesia ( Supplementary Fig.…”

“…1m). Previously, we identified complementary recurrent circuit mechanisms through which PCx transforms varying concentration-dependent OB input odor to form stable odor identity representations 37 . These results are consistent with a primary role for PCx in stable odor coding despite varying input.…”