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  • Review Article
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Central mechanisms of odour object perception

Nature Reviews Neuroscience volume 11, pages 628–641 (2010)Cite this article

Subjects

Key Points

  • An object can be defined as a 'thing' that is presented to the senses. Thus, an odour object can be defined as a smell that is presented to the olfactory sense. Although the visual and olfactory systems have evolved under different ecological pressures, many of the basic principles underlying visual object perception hold for olfactory object perception.

  • Studies in which olfactory behavioural states and brain activity are monitored simultaneously in the same animal offer a direct way to relate odour object percepts to their underlying cortical signatures. These approaches, in combination with high-resolution functional MRI and multivariate statistical analysis, have advanced our understanding of odour object perception.

  • The human piriform cortex is situated at the junction of the frontal and temporal lobes and is the main recipient of afferent sensory input from the olfactory bulb. Its unique anatomy, physiology and connectivity suggest that this brain region is well-suited for encoding odour objects.

  • Recent data indicate that the piriform cortex is involved in key elements of odour object perception, including feature synthesis, figure–ground segregation, perceptual categorization and discrimination, and attentional selection. The chemical identity of an odour stimulus is encoded in the anterior piriform cortex, whereas the integrated perceptual representation of an odour object is encoded in posterior piriform cortex.

  • Categorical percepts of odour objects take the form of spatially dispersed patterns across the piriform cortex in the apparent absence of localized clusters of activity. These distributed ensemble representations may be crucial for the olfactory brain to execute content-addressable memory and pattern completion, in which object-specific patterns can be fully reconstituted from degraded or noisy odour inputs, helping to achieve perceptual constancy.

  • The principal neocortical projection area of the piriform cortex is the orbitofrontal cortex, which itself sends return projections to the piriform cortex. A plausible hypothesis of olfactory orbitofrontal function is that it provides a top-down signal that helps to resolve odour object representations in the piriform cortex, particularly under conditions of high stimulus uncertainty.

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.

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Figure 1: Anatomy of the human olfactory brain.
Figure 2: Odorant feature synthesis.
Figure 3: Odour-background segmentation.
Figure 4: Constancy and categorization of objects.
Figure 5: Odour object discrimination.
Figure 6: Olfactory attentional selection.

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Acknowledgements

The author would like to thank the members of the Gottfried Laboratory for helpful comments and suggestions. The author is supported by grants from the National Institute on Deafness and Other Communication Disorders, National Institutes of Health, USA.

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    Jay A. Gottfried

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Glossary

Odours

Perceived smells that emanate from an odorant or mixture of odorants.

Odorant

A chemical stimulus that is capable of evoking a smell. In terrestrial animals, most odorants are organic molecules of low molecular weight that can gain airborne access to the olfactory system.

Configural odour perception

The perception of an odour mixture that differs from the perception of the mixture elements; that is, the mixture configuration is perceived holistically rather than as the sum of its parts.

Elemental odour perception

The perception of an odour mixture that is the same as the perception of the summed mixture elements.

Chemotopy

The idea that information about odorant chemical composition is projected onto topographically ordered spatial maps in the olfactory brain.

2-deoxyglucose methods

A functional brain mapping technique that uses radioactive 2-[14C]deoxyglucose to measure local metabolic patterns of activity-dependent glucose uptake in the central nervous system.

Odour quality

The perceptual character of a smell, such as mintiness, that emanates from an odorous object, as opposed to other perceptual features of a smell, such as intensity or pleasantness.

Focal electrical stimulation

An electrophysiological technique that limits the extent of electrical stimulation to single axon fibres. This permits quantification of synaptic transmission at the level of individual synapses.

Respiratory entrainment

The time at which odorant-evoked neural activity, usually in the form of single-unit spike firing, is most prominent during a particular phase of the respiratory cycle.

Prepotent responses

Behavioural responses with the greatest ('most potent') tendencies of being evoked by given sensory stimuli — often innate, reflexive responses.

Tuning specificity

The idea that the response activity (or 'tuning') of a given neuron is specific for a particular range of stimulus inputs. This tuning may be highly specific and 'narrow' (or non-specific and 'broad').

Olfactory valence

The appetitive or aversive nature of an olfactory stimulus.

Anosmia

Complete loss of the sense of smell, typically caused by trauma, infection or nasal–sinus disease, but often arising without an identifiable cause.

fMRI cross-adaptation

A paradigm based on the concept that sequential presentation of stimuli that share a particular feature, such as olfactory quality, causes response decline (or adaptation) in neural populations that are sensitive to that feature.

Figure–ground segmentation

The ability to discriminate, or segment, foreground details from background distracters. It is also referred to as figure–ground separation or segregation and is a necessary aspect of object perception.

Go/No-go task

In this classic discrimination task, animal or human subjects are required to make a response ('go') when presented with a particular stimulus cue and to withhold a response ('no-go') when presented with a different one.

Intraglomerular feedback inhibition

An important mechanism of synaptic inhibition in the olfactory bulb glomerulus, in which GABA (γ-aminobutyric acid)-ergic interneurons send direct inhibitory projections back to the same odour-activated mitral or tufted cells, forming a disynaptic feedback arc.

Cortical flattening algorithm

A computational method for unfolding a three-dimensional image of the brain into a flattened two-dimensional cortical sheet, making it easier to visualise topographical patterns of functional activity. These algorithms have been widely applied in retinotopic mapping of the primary visual cortex.

Multivariate fMRI analysis

A method of functional MRI data analysis designed to preserve activity-dependent signal change at the level of individual voxels and that allows the characterization of multi-voxel, pattern-based information within a brain region of interest.

Voxel-wise pattern

An ensemble pattern of functional MRI activity distributed spatially across a set of voxels.

Univariate fMRI analysis

A method of functional MRI data analysis in which data are spatially averaged and smoothed across trials, voxels and subjects, and that yields a mean estimate of peak fMRI activity for a given region of interest.

Pattern completion

A concept that is pertinent to content-addressable memory and in which an object-specific pattern representation can be fully reconstituted, or 'completed', from an incomplete stimulus input, helping to achieve perceptual constancy.

Virtual ensembles of single-unit activity

An analytical method that pools single-unit responses from different cells and different subjects into a virtual ensemble of a spatially distributed activity.

Pattern separation

The opposite of pattern completion. Learning and experience can induce a divergence, or 'separation', of object-specific pattern representations that were formerly overlapping, helping to enhance perceptual discrimination.

Perceptual learning

An increase in sensory acuity following a period of perceptual training that may or may not be explicit. The perceptual enhancement is relatively specific for the types of sensory stimuli that were encountered during initial learning.

Aversive conditioning

A type of associative learning paradigm in which a previously innocuous stimulus acquires behavioural salience after being repetitively paired with an aversive event such as an electric shock.

fMRI effective connectivity

A technique that is used to compute the causal links, or 'effects', that one brain region exerts on another, based on functional MRI data sets.

Signal fidelity

In the context of neural information processing and transformation, this term refers to how closely an output signal or representation corresponds to the input.

Content-addressable memory

A computationally robust form of associative memory that effectively functions as a reference table that allows the retrieval of specific memories in response to a particular smell.

Object coding

The neurobiological processes by which perceptually relevant information about an object is encoded or represented in the brain.

Diffusion-tensor imaging

An MRI technique that provides a three-dimensional image of water diffusion in the brain. As water diffuses more readily along the axis of myelinated nerve-fibre tracts, this method can be used to obtain a non-invasive estimate of anatomical connectivity between brain areas.

Transcranial magnetic stimulation

A method that involves applying local magnetic stimulation at the scalp to induce electrical excitation of the underlying cortical areas and their projections. The technique can be used to study cortical excitability and reorganization, as well as to disrupt or enhance activity in specific brain regions.

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Gottfried, J. Central mechanisms of odour object perception. Nat Rev Neurosci 11, 628–641 (2010). https://doi.org/10.1038/nrn2883

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