From molecule to mind: an integrative perspective on odor intensity

doi:10.1016/j.tins.2014.05.005

Trends in Neurosciences

Volume 37, Issue 8, August 2014, Pages 443-454

https://doi.org/10.1016/j.tins.2014.05.005 Get rights and content

Highlights

•
Olfaction lacks a working model of odor-intensity coding.
•
Neural correlates of varying odor concentration lead to simplistic models.
•
New models are needed that predict intensity across odors, in mixtures, and after adaptation.

A fundamental problem in systems neuroscience is mapping the physical properties of a stimulus to perceptual characteristics. In vision, wavelength translates into color; in audition, frequency translates into pitch. Although odorant concentration is a key feature of olfactory stimuli, we do not know how concentration is translated into perceived intensity by the olfactory system. A variety of neural responses at several levels of processing have been reported to vary with odorant concentration, suggesting specific coding models. However, it remains unclear which, if any, of these phenomena underlie the perception of odor intensity. Here, we provide an overview of current models at different stages of olfactory processing, and identify promising avenues for future research.

Section snippets

Deciphering the neural code for odor intensity

‘I want to create a cologne that smells like a whisper. It’ll be for all the secret admirers out there.’ Jarod Kintz

Some odors whisper like a secret admirer, others blare like a megaphone. How does the brain encode such a broad spectrum of olfactory intensities? Most research in the field has focused on concentration, rather than intensity. Whereas the intensity of an odorant is clearly related to its concentration [1], odorant concentration also correlates with odor valence [2] and quality [3]

Intensity–concentration relation

Empirically, the perceived intensity of an odorant is a monotonic, sigmoidal function of the logarithm of odorant concentration, although most early observations captured only the linear portion over a middle range of concentrations. In fact, many odorants fail to attain sufficiently high vapor concentrations to saturate the psychophysical function [7], so linear [8] and exponential [9] functions can indeed approximate the intensity–concentration function. However, a comparison of models found

Predicting odor intensity from chemical structure

There is currently no general model predicting the psychophysical intensity function from chemical structure. Certain physicochemical properties of molecules tend to be associated with high-potency odorants, such as high volatility and intermediate water-lipid partitioning, but odor intensity still spans several orders of magnitude for compounds with similar volatility and hydrophobicity.

General models have emerged for a special case of the psychophysical function relating concentration to

Neural encoding: predicting odor intensity from spike patterns

Chemical signals detected by olfactory receptors (OR) in OSNs are transformed into sequences of action potentials or spikes relayed to the brain. Spikes are digital signals whose number, timing, and distribution across neural assemblies contain all of the stimulus information available to the nervous system. A variety of schemes have been proposed for spike encoding of odor intensity at different stages in the olfactory pathway, based on observing changes in neural activity as a function of

Odor intensity from cortical activation

To date, few studies have directly assessed the central neural network responsible for the processing of perceived odor intensity or odor concentration. A major reason for this dearth of knowledge is the aforementioned inherently confounding co-dependency between the three perceptual odor dimensions: intensity, valence, and quality. This interdependence among dimensions renders the task of isolating cognitive processing of intensity perception inherently difficult. Nonetheless, increased

How quickly is intensity computed?

In land-based vertebrates, olfactory perception begins with the inhalation (sniffing) of odorous air into the nasal cavity. A sniff begins with a stimulus-independent inhalation, but is rapidly modulated in response to sniff content. Sniffs of different odorant concentrations are uniform for the first 160–260 ms following sniff onset, but then diverge such that sniffs of a concentrated odorant will have a smaller volume than sniffs of a diluted odorant [73]. This relation is sufficiently robust

Concluding remarks

Most olfactory stimuli encountered in nature are complex mixtures of odorant molecules. When the intensities of the component odorants are known, what is the intensity of the mixture? The intensity of an odorant mixture is rarely a simple linear sum of the intensities of individual components [108], but as noted above, nonlinear models, such as the Hill equation, are often a better fit to the concentration–intensity relation. Thus, mixture interactions that deviate from a linear sum of

Acknowledgments

J.D.M. is supported by National Institutes of Health (NIH) grant DC013339. J.N.L. is supported by the Knut and Alice Wallenberg Foundation (KAW 2012.0141). J.R. is supported by NIH grant DC009613. G.L. is supported by NIH grant DC04208.

Glossary

Amodal neural network: a network that is not primarily dedicated to the processing of information from a specific sensory modality, such as vision, audition, or olfaction.
GCaMP2 imaging: GCaMP2 is a genetically encoded reporter protein whose fluorescence increases as intracellular calcium levels rise when neurons fire action potentials. In the olfactory system, mouse strains expressing GCaMP2 in OSNs, and in mitral/tufted cells, have been used to map patterns of glomerular activity encoding

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Trends in Neurosciences

ReviewFrom molecule to mind: an integrative perspective on odor intensity

Highlights

Section snippets

Deciphering the neural code for odor intensity

Intensity–concentration relation

Predicting odor intensity from chemical structure

Neural encoding: predicting odor intensity from spike patterns

Odor intensity from cortical activation

How quickly is intensity computed?

Concluding remarks

Acknowledgments

Glossary

Curr. Biol.

Neuropsychologia

Biophys. J.

Biophys. J.

Biosystems

Cell

Neuron

Neuron

Neuron

Trends Neurosci.

Neuron

Trends Neurosci.

Cell Rep.

Neuron

Neuron

Neuron

Mol. Cell. Neurosci.

Neuron

Neuron

Neuroscience

Electroencephalogr. Clin. Neurophysiol.

Neuroscience

Neuron

Neuron

Physiol. Behav.

Exp. Neurol.

Modelling the human olfactory stimulus-response function

Chem. Senses

Odor pleasantness and intensity: a single dimension?

J. Exp. Psychol.

Concentration-dependent changes of perceived odor quality

Chem. Senses

Selective olfactory deficits in case H.M

Brain

Odor intensity and pleasantness for a diverse set of odorants

Percept. Psychophysiol.

Elemente der Psychophysik

On the psychophysical law

Psychol. Rev.

Limitations in the use of odor activity values to determine important odorants in foods

An algorithm for 353 odor detection thresholds in humans

Chem. Senses

Quantitative structure-activity relationships (QSARs) for odor thresholds of volatile organic compounds (VOCs)

Indoor Air

Genetic variation in a human odorant receptor alters odour perception

Nature

Odor intensity: differences in the exponent of the psychophysical function

Percept. Psychophys.

Patch-clamp studies of isolated mouse olfactory receptor neurons

J. Gen. Physiol.

Adaptation of the odour-induced response in frog olfactory receptor cells

J. Physiol.

Quantitative stimulation of frog olfactory receptors

J. Neurophysiol.

Origin of basal activity in mammalian olfactory receptor neurons

J. Gen. Physiol.

Peripheral odor coding in the rat and frog: quality and intensity specification

J. Neurosci.

Olfactory receptor neuron responses coding for rapid odour sampling

J. Physiol.

A large-scale analysis of odor coding in the olfactory epithelium

J. Neurosci.

Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb

J. Neurosci.

Odorant receptor expression defines functional units in the mouse olfactory system

J. Neurosci.

Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice

Review
From molecule to mind: an integrative perspective on odor intensity