Central mechanisms of odour object perception

Abstract

The stimulus complexity of naturally occurring odours presents unique challenges for central nervous systems that are aiming to internalize the external olfactory landscape. One mechanism by which the brain encodes perceptual representations of behaviourally relevant smells is through the synthesis of different olfactory inputs into a unified perceptual experience--an odour object. Recent evidence indicates that the identification, categorization and discrimination of olfactory stimuli rely on the formation and modulation of odour objects in the piriform cortex. Convergent findings from human and rodent models suggest that distributed piriform ensemble patterns of olfactory qualities and categories are crucial for maintaining the perceptual constancy of ecologically inconstant stimuli.

Figure 1. Anatomy of the human olfactory brain

a | A ventral view of the human brain in which the right anterior temporal lobe has been resected in the coronal plane to expose the limbic olfactory areas. The area that is outlined by a box in part a is magnified in part b following a second resection along the axial plane of the right temporal lobe (shown by the dashed line and scalpel). b | Afferent output from the olfactory bulb (OB) passes through the lateral olfactory tract (LOT) and projects monosynaptically to numerous regions, including the anterior olfactory nucleus (AON), olfactory tubercle (OTUB), anterior piriform cortex (APC), posterior piriform cortex (PPC), amygdala (AM) and entorhinal cortex (EC). Downstream relays include the hippocampus (HP) and the putative olfactory projection site in the human orbitofrontal cortex (OFC_olf) that has been identified on the basis of a neuroimaging meta-analysis. As noted in the inset, information is not transferred serially through this circuit. Monosynaptic projections from the lateral olfactory tract reach numerous downstream regions in parallel and these regions are then reciprocally interconnected (not shown). c | Schematic representation of the cellular organization of the piriform cortex. Pyramidal neurons are located in cell body layers II and III, and their apical dendrites project to molecular layer I. Layer I is subdivided into a superficial layer (Ia) that contains the sensory afferents from the olfactory bulb (shown in red) and a deeper layer (Ib) that contains the associative inputs from other areas of the primary olfactory cortex and higher-order areas (shown in blue). The majority of layer Ia afferents terminate in the APC, whereas the majority of layer Ib associative inputs terminate in posterior piriform cortex (PPC). Photographs in parts a and b prepared with the help of E. H. Bigio, Northwestern University Feinberg School of Medicine, USA.

Figure 2. Odorant feature synthesis

a | The d’Anjou pear produces 44 volatile components, 3 of which are depicted here: ethyl acetate, α-farnesene and butanol. Elemental processing in the anterior piriform cortex (APC) results in coding of odorant chemical identity (top right), whereas synthetic processing in the posterior piriform cortex (PPC) results in coding of odour object quality (bottom right)^,. b | Sequential presentation of odorants that contain the same functional group results in decreased, or cross-adapting, responses in the APC. The image (left) shows a statistical parametric map of functional MRI data from the APC after the sequential presentation, showing the cross-adapting effect. The time-course plots for signal change illustrate a significant main effect for repetition of functional group (left-hand graph) but not for repetition of perceptual quality (right-hand graph). c | In the PPC, cross-adaptation is elicited by the sequential presentation of odorants that contain similar perceptual qualities. The image (left) shows the statistical parametric map of fMRI data from the PPC after the sequential presentation. The time-course plots show no significant main effect for repetition of functional group (left-hand graph) but a significant effect for repetition of quality (right-hand graph). The red circles indicate the APC (b) and the PPC (c). * significant at P < 0.05. Parts b and c are modified, with permission, from REF. © (2006) Cell Press.

Figure 3. Odour-background segmentation

a | When considering pears hanging from a tree as an odour object, the olfactory features that arise from the leaves of the pear tree constitute the background stimulus. Prolonged exposure to this background stimulus induces sensory-specific habituation in the piriform cortex, thereby bringing the smell of pears to the foreground of perception. b | In a study performed in rodents, odorants ‘A’ and ‘B’ were presented individually or as a mixture (‘A + B’) on separate trials that lasted for 2 s (top part, left side). In a subsequent habituation phase, B was continuously presented for 40 s, followed by a presentation of the mixture for 2 s (top part, right side). In this presentation of the mixture, B constituted the background against which A was presented. During habituation to B, single-unit activity persisted in the olfactory bulb, showing a constant profile resembling that elicited by the 2-s presentation (middle part, right side), but in the anterior piriform cortex, the activity declined progressively during habituation to B (bottom part, right side). When A was presented together with B immediately after habituation, firing rates in the olfactory bulb were similar to those evoked by individual presentations of A + B (middle part, left side). By contrast, anterior piriform cortex firing rates in response to presentation of the mixture (bottom part, right side) were more similar to those evoked by A alone (bottom part, left side), reflecting the effective segregation of odorant A from the background (odorant B). Part b is modified, with permission, from REF. © (2006) The American Physiological Society.

Figure 4. Constancy and categorization of objects

a | Despite differences in odour, colour, size, shape and texture, all of the objects shown belong to the category ‘pears’. In the piriform cortex, distributed ensemble patterns of odour-evoked activity provide a mechanism for perceptual pattern completion of partial, fragmented or non-canonical stimulus inputs. This allows the distinction of one object from a group of objects of the same category — for example, the distinction of the small Seckel pear (S) from a group of pears. b | Data from a human subject, presented on a flattened cortical map of the left posterior piriform cortex (PPC), showing that odorants that differ in perceptual quality evoke distributed and overlapping but unique functional MRI activity patterns in this structure (top part). Considerable response overlap was observed at the level of individual voxels, suggesting that odorants that differ in perceived quality might activate the same voxel. However, at the multi-voxel level, qualitatively distinct odorants evoked unique ensemble patterns of activity. From a dataset of 3 minty, 3 woody, and 3 citrus odorants, 2 ‘distance’ matrices were generated: a 9-by-9 imaging matrix composed of the multi-voxel fMRI signal correlation in the PPC for every odorant pair and a 9-by-9 perceptual matrix composed of perceived differences (reported by the subject) in odour quality between every odorant pair. Multidimensional scaling projections of these distance matrices onto a common three-dimensional space (bottom part) demonstrated robust spatial correspondence between the projected PPC imaging map (shown by filled circles) and the projected perceptual map (shown by open circles). A, anterior; L, lateral; M, medial; P, posterior. c | In the rodent anterior piriform cortex (APC), virtual ensemble activity patterns for a 10-odorant mixture (10c) were highly correlated with similar mixtures from which 1 component was removed (10c – 1). These pattern correlations progressively decreased as more odorants were either removed (10c – 2, 10c – 3) or replaced (10c R1, 10c R2, 10c R3) in the mixture (shown by blue bars). This was not observed in the mitral and tufted cell ensembles (shown by green bars). d | A 2-choice odour discrimination test shows that rats make many more errors when trying to distinguish between 10c and 10c – 1 (pattern completion) than when trying to tell apart 10c from 10c – 2, 10c – 3, and 10c R1 (pattern separation). This finding is in agreement with the pattern correlations that are depicted in part c. Part b is modified, with permission, from REF. © (2009) Macmillan Publishers Ltd. All rights reserved. Parts c and d are modified, with permission, from REF. © (2008) Macmillan Publishers Ltd. All rights reserved.

Figure 5. Odour object discrimination

a | Perceptual learning. Two varieties of pears, the d’Anjou and the Comice, have similar smells (left part). The ability to discriminate between the two can increase after prolonged exposure to their odours or after aversive learning (middle and right parts). This is an example of learning-induced perceptual plasticity in humans. b | In a functional MRI study of olfactory perceptual learning in humans, prolonged exposure to one odorant enhanced perceptual differentiation among qualitatively related odorants. After continuous delivery of a floral odorant for 3.5 min, the ratings of odour quality dissimilarity given by subjects increased between floral odorants (left part, shown in red) but not between minty odorants (left part, shown in purple), demonstrating the category-specificity of these learning effects. In the same subjects, experience-dependent changes were observed in the right posterior piriform cortex (PPC) (right part), with greater differences in mean fMRI activity in response to floral odours pre-exposure (PRE) compared with post-exposure (POST), showing how perceptual experience can modulate neural representations of odour quality. c | In an olfactory fMRI study of aversive learning, subjects smelled two odour enantiomers, or mirror-image molecules, before and after an aversive conditioning session in which one of the two enantiomers (the conditioned stimulus, CS) was repeatedly paired with a mild electric shock (the unconditioned stimulus). After conditioning, there was an improvement in perceptual discrimination between the previously indistinguishable enantiomers (CS+) (left part, shown by blue bars) but this was not the case for a control pair of odour enantiomers (CS−) (left part, shown by orange bars). Aversive learning was also associated with a reorganization of fMRI ensemble activity patterns in the PPC specifically for the enantiomer pair that was used during conditioning. The grids depict odorant pairwise activation differences at each PPC voxel, with bolder colors indicating greater differences in activation per voxel (right part). Voxels are arranged in columns from top left to bottom right of each grid, in ascending order of signal intensity for the conditioned stimulus before conditioning. Part b is modified, with permission, from REF. © (2006) Cell Press. Part c is modified, with permission, from REF. © (2008) American Association for the Advancement of Science.

Figure 6. Olfactory attentional selection

a | The olfactory system may be confronted with many different odorous objects simultaneously, such as an array of different fruit smells at a market (left part). Attentional mechanisms provide a dynamic way of selecting among these competing alternatives, bringing one odour object to the perceptual foreground (right part) in accordance with physiological needs and motivational states. b | In a functional MRI study in humans, participants were presented with a bimodal olfactory–auditory stimulus and asked to attend to the odour or to the tone. Odorant-evoked activity in the temporal piriform cortex (PirT; roughly approximating to the posterior piriform cortex [PPC]) was not affected by the attentional state, whereas activity in the frontal piriform cortex (PirF; roughly approximating the anterior piriform cortex [APC]) was attention-dependent and more pronounced when the subjects were paying attention to odour instead of tone. c | Odour attention enhances fMRI network coherence along the olfactory transthalamic pathway. The coupling between the PPC and mediodorsal thalamus (MD), and between the mediodorsal thalamus and orbitofrontal cortex (OFC) was strengthened as a result of directing attention to a smell. This effect was specific to forward connections (that is, connections from the MD to the OFC, rather than from the OFC to the MD), and to the indirect trans-thalamic pathway (compared to the direct pathway between the APC and the OFC). Thick arrows indicate forward pathway connections that were strengthened during odour versus tone attention. Thin arrows indicate other forward and backward connections that were not affected by attentional manipulation. The key (top right of the image) indicates anterior (Ant), posterior (Post), superior (Sup)-inferior (Inf), right and left axes of the brain image. Part b is modified from REF. © (2005) Macmillan Publishers Ltd. All rights reserved. Part c modified, with permission, from REF. © (2008) Society for Neuroscience.