Mixture Coding and Segmentation in the Anterior Piriform Cortex

Abstract

Coding of odorous stimuli has been mostly studied using single isolated stimuli. However, a single sniff of air in a natural environment is likely to introduce airborne chemicals emitted by multiple objects into the nose. The olfactory system is therefore faced with the task of segmenting odor mixtures to identify objects in the presence of rich and often unpredictable backgrounds. The piriform cortex is thought to be the site of object recognition and scene segmentation, yet the nature of its responses to odorant mixtures is largely unknown. In this study, we asked two related questions. (1) How are mixtures represented in the piriform cortex? And (2) Can the identity of individual mixture components be read out from mixture representations in the piriform cortex? To answer these questions, we recorded single unit activity in the piriform cortex of naïve mice while sequentially presenting single odorants and their mixtures. We find that a normalization model explains mixture responses well, both at the single neuron, and at the population level. Additionally, we show that mixture components can be identified from piriform cortical activity by pooling responses of a small population of neurons-in many cases a single neuron is sufficient. These results indicate that piriform cortical representations are well suited to perform figure-background segmentation without the need for learning.

What the odor is not: Estimation by elimination

“…Recurrent inhibition allows local solutions to this inversion problem when it is well-defined if we choose so that (𝕀 − p ) = ŜS . These criteria relate feed-forward weights to the sensing matrix recalling [18, 63], and balance the network unit by unit, compensating feed-forward excitation by recurrent inhibition. Since these constraints relate individual readouts (rows of Ŝ ) and odorants (columns of S ), solutions for different pairs can be spliced to construct feedforward and recurrent weight matrices.…”

“…Then, at steady state, active units satisfy (I p)r =ŜSc (7) where rows of the odor vector c and columns of the sensing matrix S have been restricted to present odorants. This readout can directly represent odorants (r = c) if (I p) 1Ŝ = S 1 , an explicit decoding of the sort considered in [63]. Such an inversion of a rectangular matrix is generally ill-defined because S andŜ will have rank less than the number of concentrations to estimate when there are fewer receptors than odorants.…”

State-dependent representations of mixtures by the olfactory bulb

“…In particular, suppressive interactions become dominant among large responses due to saturation ( Mathis et al, 2016 ). This pattern is observed at many stages of olfactory processing, including in the OB ( Economo et al, 2016 ; Fletcher, 2011 ) and anterior piriform cortex ( Penker et al, 2020 ), but it depends on the complexity of mixtures, as well as odorant choices ( Fletcher, 2011 ; Gupta et al, 2015 ; Rokni and Murthy, 2014 ; Tabor et al, 2004 ). We therefore characterised the property of binary mixture summation using our odour set.…”

“…In one test, these sums, with added noise, were passed through SVMs that had been trained with single odour responses. In another test, the linearly summed responses with noise were transformed with a normalising function ( Mathis et al, 2016 ; Penker et al, 2020 ), which adds sublinearity in an amplitude-dependent manner ( Figure 7B ; see Materials and methods). Then, these signals were passed through the same SVMs to assess how discriminable the activity patterns were.…”

“…In addition to the interactions at the periphery, there are many forms of nonlinear summation at multiple stages of olfactory processing, including the saturation of neural responses ( Firestein et al, 1993 ; Wachowiak and Cohen, 2001 ) and inhibitory interactions within the olfactory bulb (OB) ( Economo et al, 2016 ). Widespread suppressive interactions are also observed in downstream areas, including the piriform cortex ( Penker et al, 2020 ; Stettler and Axel, 2009 ).…”