Spatio–temporal dynamics of olfactory processing in the human brain: an event-related source imaging study

doi:10.1016/j.neuroscience.2010.02.013

Neuroscience

Volume 167, Issue 3, 19 May 2010, Pages 700-708

https://doi.org/10.1016/j.neuroscience.2010.02.013 Get rights and content

Abstract

Although brain structures involved in central nervous olfactory processing in humans have been well identified with functional neuroimaging, little is known about the temporal sequence of their activation. We recorded olfactory event-related potentials (ERP) to H₂S stimuli presented to the left and right nostril in 12 healthy subjects. Topographic and source analysis identified four distinct processing steps between 200 and 1000 ms. Activation started ipsilateral to the stimulated nostril in the mesial and lateral temporal cortex (amygdala, parahippocampal gyrus, superior temporal gyrus, insula). Subsequently, the corresponding structures on the contralateral side became involved, followed by frontal structures at the end of the activation period. Thus, based on EEG-related data, current results suggest that olfactory information in humans is processed first ipsilaterally to the stimulated nostril and then activates the major relays in olfactory information processing in both hemispheres. Most importantly, the currently described techniques allow the investigation of the spatial processing of olfactory information at a high temporal resolution.

Section snippets

Participants

Twelve normosmic healthy volunteers (six male; six female; median age: 30 years; age range: 22–46 years) were included in this study. All participants were right handed (Edinburgh Handedness Inventory (Oldfield, 1971)) and non-smokers. Prior to participation, subjects provided written informed consent. The study design had been approved by the Ethics Committee of the University Hospital of Geneva (Geneva, Switzerland) in agreement with the Declaration of Helsinki. Exclusion criteria were

Epicranial olfactory ERP mapping

Fig. 2 shows the grand-mean OERP response averaged over 12 healthy controls for both left and right nostril stimulation. Fig. 2A reveals the conventional ERP traces of the parietal electrode (Pz) referenced to the mean of the two mastoid electrodes (M1/M2), showing the expected N1 (Peak: 408 and 420 ms for the right and the left stimulation respectively) and P2–P3 components (Peak: 844 and 796 ms for the right and the left stimulation respectively) as described in previous literature (Kobal,

Discussion

The major finding of this study is that source localization analysis of high-density olfactory ERPs identified a clear temporal succession of central nervous olfactory processing. Olfactory information is first processed in mesial and lateral temporal brain structures ipsilaterally to the stimulated nostril, before it reaches contralateral temporal and finally frontal areas.

The olfactory ERP waveforms in the present study stand in line with a large body of literature on chemosensory ERPs and

Conclusion

In conclusion, the present research shows that olfactory information can be traced with high temporal and good spatial resolution not only at neocortical sites but also at the level of deep brain structures. This approach opens new avenues for the analysis of olfactory information processing. As a first result the present data indicate that olfactory information is processed mostly ipsilaterally to the stimulated nostril in humans and that the information is not stationary but seems to go back

Acknowledgments

This work was supported by a Fund of the Neuroscience Center of the University of Geneva to BNL, JSL and CMM. BNL was supported by a Grant of the Swiss National Fund for Scientific Research (SSMBS grant n° PASMA-119579/1). CMM was supported by the Swiss National Science Foundation (Grant No. 320030-111783. TH was supported by a grant from the Centre National de la Recherche Scientifique (European associated laboratory; EAL 549, CNRS-TUD). The Cartool software (//brainmapping.unige.ch/Cartool.htm

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Cognitive NeuroscienceResearch PaperSpatio–temporal dynamics of olfactory processing in the human brain: an event-related source imaging study

Abstract

Section snippets

Participants

Epicranial olfactory ERP mapping

Discussion

Conclusion

Acknowledgments

Modeling and detecting deep brain activity with MEG and EEG

Conf Proc IEEE Eng Med Biol Soc

The molecular logic of smell

Sci Am

High-resolution electro-encephalogram: source estimates of Laplacian-transformed somatosensory-evoked potentials using a realistic subject head model constructed from magnetic resonance images

Med Biol Eng Comput

Electromagnetic brain mapping

IEEE Signal Process Mag

Signal-to-noise ratio of chemosensory event-related potentials

Clin Neurophysiol

Event-related potentials of the brain and cognitive processes: approaches and applications

Neuropsychologia

Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey

J Comp Neurol

In vivo imaging of functional disruption, recovery and alteration in rat olfactory circuitry after lesion

Neuroimage

Olfactory learning: convergent findings from lesion and brain imaging studies in humans

Brain

Cognitive modulation of olfactory processing

Neuron

Smell: central nervous processing

Adv Otorhinolaryngol

The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception

Neuron

Noninvasive localization of electromagnetic epileptic activity. IMethod descriptions and simulations

Brain Topogr

Noninvasive estimation of local field potentials: methods and applications

Olfactory cortex

Cortical source imaging from scalp electroencephalograms

Med Biol Eng Comput

Scents of time

Sciences

Qualitative and quantitative discrimination in the frog olfactory receptors: analysis from electrophysiological data

Ann N Y Acad Sci

Olfactory event-related potentials

Chemosensory event-related potentials in patients with temporal lobe epilepsy

Epilepsia

Kallmann's syndrome and chemosensory evoked potentials

Eur Arch Otorhinolaryngol

Assessment of olfactory function

Adv Otorhinolaryngol

Neural transition from short-to long-term memory and the medial temporal lobe: a human evoked-potential study

Hippocampus

Early neuronal responses in right limbic structures mediate harmony incongruity processing in musical experts

Neuroimage

Odor recognition memory in humans: role of right temporal and orbitofrontal regions

Brain Cogn

Contribution of medial versus lateral temporal-lobe structures to human odour identification

Brain

Functional imaging of olfactory activation in the human brain

Odorants activate the human superior temporal sulcus

Neurosci Lett

Chemosensory function in patients with vagal nerve stimulators

J Clin Neurophysiol

Elektrophysiologische Untersuchungen des menschlichen Geruchssinns

Cerebral chemosensory evoked potentials elicited by chemical stimulation of the human olfactory and respiratory nasal mucosa

Electroencephalogr Clin Neurophysiol

Methodische Anmerkungen zur Gewinnung olfaktorischer EEG-Antworten des wachen Menschen (objektive Olfaktometrie)

Z EEG-EMG

Is there directional smelling?

Experientia

Neuroleptic-induced parkinsonism is associated with olfactory dysfunction

J Neurol

Noninvasive localization of electromagnetic epileptic activity. IIDemonstration of sublobar accuracy in patients with simultaneous surface and depth recordings

Brain Topogr

EEG microstates

Scholarpedia

Cognitive Neuroscience
Research Paper
Spatio–temporal dynamics of olfactory processing in the human brain: an event-related source imaging study