Elsevier

Neuroscience

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

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

https://doi.org/10.1016/j.neuroscience.2010.02.013Get 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

References (72)

  • D. Lehmann et al.

    Spatial analysis of evoked potentials in man—a review

    Prog Neurobiol

    (1984)
  • C.M. Michel et al.

    EEG source imaging

    Clin Neurophysiol

    (2004)
  • C.M. Michel et al.

    Electric source imaging of human brain functions

    Brain Res Brain Res Rev

    (2001)
  • R.C. Oldfield

    The assessment and analysis of handedness: the Edinburgh inventory

    Neuropsychologia

    (1971)
  • J. Porter et al.

    Brain mechanisms for extracting spatial information from smell

    Neuron

    (2005)
  • E.T. Rolls et al.

    The orbitofrontal cortex and beyond: from affect to decision-making

    Prog Neurobiol

    (2008)
  • J.P. Royet et al.

    Functional neuroanatomy of different olfactory judgments

    Neuroimage

    (2001)
  • I. Savic et al.

    Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans

    Neuron

    (2001)
  • M.T. Shipley et al.

    Anatomical evidence for convergence of olfactory, gustatory, and visceral afferent pathways in mouse cerebral cortex

    Brain Res Bull

    (1984)
  • D.M. Small et al.

    Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans

    Neuron

    (2005)
  • L. Uva et al.

    Polysynaptic olfactory pathway to the ipsi- and contralateral entorhinal cortex mediated via the hippocampus

    Neuroscience

    (2005)
  • A. Welge-Lussen et al.

    Olfactory-induced brain activity in Parkinson's disease relates to the expression of event-related potentials: a functional magnetic resonance imaging study

    Neuroscience

    (2009)
  • D. Zumsteg et al.

    Source localization of mesial temporal interictal epileptiform discharges: correlation with intracranial foramen ovale electrode recordings

    Clin Neurophysiol

    (2005)
  • Y. Attal et al.

    Modeling and detecting deep brain activity with MEG and EEG

    Conf Proc IEEE Eng Med Biol Soc

    (2007)
  • R. Axel

    The molecular logic of smell

    Sci Am

    (1995)
  • F. Babiloni et al.

    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

    (2000)
  • S. Baillet et al.

    Electromagnetic brain mapping

    IEEE Signal Process Mag

    (2001)
  • S.T. Carmichael et al.

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

    J Comp Neurol

    (1994)
  • L.A. Dade et al.

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

    Brain

    (2002)
  • J.A. Gottfried

    Smell: central nervous processing

    Adv Otorhinolaryngol

    (2006)
  • R. Grave de Peralta Menendez et al.

    Noninvasive localization of electromagnetic epileptic activity. IMethod descriptions and simulations

    Brain Topogr

    (2001)
  • R. Grave de Peralta Menendez et al.

    Noninvasive estimation of local field potentials: methods and applications

  • L.B. Haberly

    Olfactory cortex

  • B. He et al.

    Cortical source imaging from scalp electroencephalograms

    Med Biol Eng Comput

    (1996)
  • R.S. Herz

    Scents of time

    Sciences

    (2000)
  • A. Holley et al.

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

    Ann N Y Acad Sci

    (1974)
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