The role of piriform associative connections in odor categorization

Abstract

Distributed neural activity patterns are widely proposed to underlie object identification and categorization in the brain. In the olfactory domain, pattern-based representations of odor objects are encoded in piriform cortex. This region receives both afferent and associative inputs, though their relative contributions to odor perception are poorly understood. Here, we combined a placebo-controlled pharmacological fMRI paradigm with multivariate pattern analyses to test the role of associative connections in sustaining olfactory categorical representations. Administration of baclofen, a GABA(B) agonist known to attenuate piriform associative inputs, interfered with within-category pattern separation in piriform cortex, and the magnitude of this drug-induced change predicted perceptual alterations in fine-odor discrimination performance. Comparatively, baclofen reduced pattern separation between odor categories in orbitofrontal cortex, and impeded within-category generalization in hippocampus. Our findings suggest that odor categorization is a dynamic process concurrently engaging stimulus discrimination and generalization at different stages of olfactory information processing, and highlight the importance of associative networks in maintaining categorical boundaries.DOI: http://dx.doi.org/10.7554/eLife.13732.001

Characterizing functional pathways of the human olfactory system

“…In our study, we found a clear differentiation between the functional connectivity patterns of human frontal and temporal piriform subdivisions, suggesting these two areas play different roles in olfactory processing in the human brain (Albrecht et al, 2010; Bao et al, 2016; Bensafi et al, 2007; Howard et al, 2009; Plailly et al, 2012; Porter et al, 2005; Zelano et al, 2005). This distinction between frontal and temporal piriform cortices was robust, surviving across k values and hemispheres.…”

Cell-Type-Specific Whole-Brain Direct Inputs to the Anterior and Posterior Piriform Cortex

“…In addition, we also noted that over half of the ipsilateral OLF inputs to the PPC came from the ipsilateral APC. A previous study demonstrated that by using the GABA(B) receptor agonist to attenuate PC associational inputs, pattern separation of within-category odors is interfered within the PPC (Bao et al, 2016), meaning that the neural activities in the PC, especially the PPC, may strongly be affected by their associational connections. It could be speculated that the PPC may be in higher associative functions.…”

“…The APC and PPC play different roles in olfactory processing including odor response and learning (Litaudon et al, 2003;Gottfried et al, 2006;Kadohisa and Wilson, 2006;Calu et al, 2007). For instance, the APC encodes odor identity and anticipation, and can be activated not only by odor stimuli but also by odor associated values or contextual cues (Zinyuk et al, 2001;Gottfried et al, 2006;Kadohisa and Wilson, 2006;Roesch et al, 2007); whereas the PPC seems to encode more associated information for it to be activated in tasks that require encoding of odor similarity or odor quality (Kadohisa and Wilson, 2006;Calu et al, 2007;Howard et al, 2009;Zelano et al, 2011;Bao et al, 2016;Grau-Perales et al, 2019). In addition, accumulating evidence from research has also revealed distinct susceptibilities of different PC subareas to seizure generation (Loscher and Ebert, 1996;Ekstrand et al, 2001;Yang et al, 2006;Vismer et al, 2015).…”

A Systematic Framework for Olfactory Bulb Signal Transformations

“…Similarly, the current form of the inhibitory learning rule forestalls manifold learning; its more sophisticated replacement may require expansion of the network to include the feedback loop between MOB and PCx, which in the biological system supersedes intrinsic MOB gamma with slightly slower (beta band) coherent oscillations between these two structures (Cenier et al, 2009 ; Frederick et al, 2016 ). Indeed, existing efforts to study the neuroscience of odor categorization have focused on the PCx and its associated limbic regions (Bao et al, 2016 ; Qu et al, 2016 ), and analogous studies in insects also suggest that categorical processing incorporates plasticity in peripheral networks together with higher-order olfactory structures (Locatelli et al, 2016 ; Strube-Bloss and Rossler, 2018 ). Finally, the rules by which adult-generated interneurons are incorporated into the neuromorphic network also are simplified, privileging strict categorization over similarity-dependent generalization processes.…”