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In This Article

  • Summary
  • Abstract
  • Introduction
  • Protocol
  • Representative Results
  • Discussion
  • Acknowledgements
  • Materials
  • References
  • Reprints and Permissions

Summary

This paper describes using a breath-synchronized olfactometer to trigger single- and dual-coil transcranial magnetic stimulation (TMS) during odorant presentation synchronized to human nasal breathing. This combination allows us to objectively investigate how pleasant and unpleasant odors impact corticospinal excitability and brain-effective connectivity in a given individual.

Abstract

It is widely accepted that olfactory stimulation elicits motor behaviors, such as approaching pleasant odorants and avoiding unpleasant ones, in animals and humans. Recently, studies using electroencephalography and transcranial magnetic stimulation (TMS) have demonstrated a strong link between processing in the olfactory system and activity in the motor cortex in humans. To better understand the interactions between the olfactory and the motor systems and to overcome some of the previous methodological limitations, we developed a new method combining an olfactometer that synchronizes the random order presentation of odorants with different hedonic values and the TMS (single- and dual-coil) triggering with nasal breathing phases. This method allows probing the modulations of corticospinal excitability and effective ipsilateral connectivity between the dorsolateral prefrontal cortex and the primary motor cortex that could occur during pleasant and unpleasant odor perception. The application of this method will allow for objectively discriminating the pleasantness value of an odorant in a given participant, indicating the biological impact of the odorant on brain effective connectivity and excitability. In addition, this could pave the way for clinical investigations in patients with neurological or neuropsychiatric disorders who may exhibit odor hedonic alterations and maladaptive approach-avoidance behaviors.

Introduction

It is widely accepted that olfactory stimulation elicits automatic reactions and motor behaviors. For example, in humans, the existence of an avoidance motor response (leaning away from the odor source) occurring 500 ms after negative odor onset has been recently demonstrated1. By recording freely moving human participants exploring odors emanating from flasks, Chalençon et al. (2022) showed that motor behaviors (i.e., speed of approach to the nose and withdrawal of the flask containing the odorant) are closely linked to odor hedonics2. Moreover, a close link between processing in the olfactory system and activity i....

Protocol

All experimental procedures described in the following sections have been approved by an Ethics Committee (CPP Ile de France VII, Paris, France, protocol number 2022-A01967-36) in accordance with the Declaration of Helsinki. All participants provided written informed consent before study enrollment.

1. Participant recruitment

  1. Inclusion/exclusion criteria.
    1. Include adult (> 18 years) participants. Screen all participants for any contraindications to T.......

Representative Results

The representative data presented here reflect recordings from participants after completing the step-by-step protocol above to provide a preliminary insight into what we might expect.

Figure 2 shows an example of a representative participant's respiratory signals recorded with the olfactometer software. The expiratory and inspiratory phases are well detected when the thresholds are crossed. The odorant is triggered immediately after the expiration phase .......

Discussion

The protocol above describes a novel method combining the use of a breath-synchronized olfactometer with single- and dual-coil TMS to investigate changes in corticospinal excitability and effective connectivity depending on the hedonic value of the odorants. This setup will allow for objectively discriminating the pleasantness value of an odorant in a given participant, indicating the biological impact of the odorant on brain effective connectivity and reactivity. The critical steps in this protocol involve both TMS.......

Acknowledgements

This work was supported by the Fondation de France, Grant N°: 00123049/WB-2021-35902 (a grant received by J.B. and N.M.). The authors would like to thank the Fondation Pierre Deniker for its support (grant received by C.N.) and the staff of the Neuro-Immersion platform for their valuable help in designing the setup.

....

Materials

NameCompanyCatalog NumberComments
Acquisition board (8 channels) National InstrumentNI USB-6009 
Air compressorJun-Air Model6-15
Alcohol prep padsAny
Butyric acidSigma-AldrichB103500Negative odorant
Desktop computerDellLatitude 3520
EMG systemBiopac SystemMP150
Isoamyl acetateSigma-AldrichW205508Positive odorant
Nasal cannulaSEBAC FranceO1320
Programmable pulse generatorA.M.P.I Master-8
Surface electrodesKendall Medi-traceFS327
TMS coil (X2)MagStimD40 Alpha B.I. coil 
TMS machineMagStimBistim2
Tube 6 mm x 20 mRadiospare686-2671Pneumatic connection
USB-RS232Radiospare687-7806
U-shaped tubesVS technologiesVS110115

References

  1. Iravani, B., Schaefer, M., Wilson, D. A., Arshamian, A., Lundström, J. N. The human olfactory bulb processes odor valence representation and cues motor avoidance behavior. Proceedings of the National Academy of Sciences. 118 (42), e2101209118 (2021).
  2. Chalençon, L., Thevenet, M., Noury, N., Bensafi, M., Mandairon, N.

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OlfactometerBrain SimulationCorticospinal ExcitabilityEffective ConnectivityOlfactory motor InteractionsPleasant And Unpleasant OdorsTranscranial Magnetic Stimulation TMSNasal BreathingPsychiatric DisordersAutonomic PerceptionApproach avoidance Behaviors

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