Orientation de l'attention visuelle par des stimulations chemosensorielles intra-nasales

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Thesis

Reference

Orientation de l'attention visuelle par des stimulations chemosensorielles intra-nasales

ISCHER, Matthieu

Abstract

Cette thèse décrit comment une odeur peut automatiquement orienter l'attention visuo-spatiale. En effet, i) il existe une banque commune de ressources attentionnelles partagées à travers les modalités sensorielles, ii) le système olfactif et trigéminal permettent aux humains de différencier une stimulation délivrée dans la narine gauche ou droite, et iii) les stimulations trigéminales sont particulièrement susceptibles de capter l'attention d'un individu.

Nous avons utilisé le dioxide de carbone (CO2) et l'eucalyptol comme indices exogènes intranasaux latéralisés dans une variante du paradigme d'indiçage spatial (tâche de Posner).

Nous avons fait varier l'intervalle de temps entre l'apparition de l'indice (l'amorce) et de la cible, appelée « Stimulus Onset Asyncrony » (SOA), dans chacune des sept études. Nous avons trouvé des effets d'amorçages avec un SOA de 610 ms pour l'eucalyptol, et avec un SOA de 680 ms et de 1160 ms pour le CO2. Les résultats suggèrent que le type de molécule utilisé pour l'amorçage pourrait influencer la fenêtre temporelle de l'apparition de l'effet.

ISCHER, Matthieu. Orientation de l'attention visuelle par des stimulations

chemosensorielles intra-nasales. Thèse de doctorat : Univ. Genève et Lausanne, 2018, no.

Neur. 221

DOI : 10.13097/archive-ouverte/unige:105936 URN : urn:nbn:ch:unige-1059368

Available at:

http://archive-ouverte.unige.ch/unige:105936

Disclaimer: layout of this document may differ from the published version.

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Faculté des sciences

DOCTORAT EN NEUROSCIENCES des Universités de Genève

et de Lausanne

CISA, UNIVERSITÉ DE GENÈVE FACULTÉ DES SCIENCES Professeur David Sander, directeur de thèse.

TITRE DE LA THÈSE

ORIENTATION DE L’ATTENTION VISUELLE PAR DES STIMULATIONS CHEMOSENSORIELLES INTRA-NASALES

THÈSE Présentée à la Faculté des Sciences de l’Université de Genève

pour obtenir le grade de Docteur en Neurosciences

par

Matthieu ISCHER

de Onex [Genève]

Thèse N° 221 Genève

Editeur ou imprimeur : Université de Genève 2017

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Ischer, M., Baron, N., Mermoud, C., Cayeux, I., Porcherot, C., Sander, D., & Delplanque, S. (2014). How incorporation of scents could enhance immersive virtual experiences. Frontiers in Psychology, 5, 736. doi:10.3389/fpsyg.2014.00736

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Acknowledgements

Je voudrais remercier sincèrement un grand nombre de personnes qui ont contribué à ce travail car il n'aurait pas été possible de finir cette thèse sans leur soutien et leur aide. Les quatres dernières années ont été très enrichissantes et j’ai eu la chance d’être entouré par des collègues et amis solidaires et généreux.

Je tiens d'abord à remercier mes superviseurs; Docteur Sylvain Delplanque et Professeur David Sander pour m'avoir accueilli et me permettre de réaliser cette thèse avec leur soutien. Merci d’avoir partagé vos nombreuses idées avec moi, nos discussions m'ont beaucoup stimulé. David et Sylvain, merci de m'avoir donné accès à cette incroyable opportunité, et d’être restés disponibles et enthousiastes en toutes circonstances pour me guider tout au long de ces années.

Merci pour vos implications, vos encouragements constants et la clarté de vos explications, cela m'a énormément aidé. Merci également de m'avoir inclus pleinement et de m'avoir donné accès à votre laboratoire.

Je voudrais aussi spécialement remercier Sylvain pour sa contribution essentielle à ce travail de thèse. Sylvain, merci beaucoup de m'avoir patiemment présenté au merveilleux monde de l'olfaction, aux mystères de la psychophysiologie et de l'écriture scientifique. Merci pour ton soutien indéfectible, tes critiques attentionnées, tes commentaires réfléchis et ton enseignement;

ils ont été essentiels à mon doctorat.

Je voudrais remercier le Docteur Christian Margot, le Docteur Basile Landis et le Professeur Johannes Frasnelli pour avoir accepté d'être membres du jury, et le Professeur Sophie Schwartz pour avoir accepté de le présider. Christian, je te remercie sincèrement pour la qualité des échanges que nous avons eus et la pertinence de tes commentaires lors de l'examen théorique.

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Merci pour tes explications fascinantes sur la chimie organique des odeurs et tes conseils pour le choix des odeurs. Johannes, merci d'avoir accepté de venir à Genève. Basile, merci beaucoup d'avoir partagé avec moi une partie de tes vastes connaissances pour mieux appréhender les troubles du système olfactif et leurs répercussions, et pour ta contribution théorique lors de mon examen.

Je remercie également le département Recherche et Développement de Firmenich, en particulier le Docteur Isabelle Cayeux, le Docteur Christelle Porcherot, Nadine Gaudreau, Alain Hugon et le Docteur Maria Inés Velazco, pour leur gentillesse et leur disponibilité. Isabelle, Christelle, Nadine, merci pour vos conseils et vos réponses à mes questions, ainsi que pour votre aide lors de la préparation des odeurs. Merci à Alain Hugon pour avoir développé l'olfactomètre, cet outil de travail incroyable, et à Maria Ines pour avoir rendu possible cette collaboration.

Je tiens également à remercier tous mes collègues et amis au Campus Biotech, Unimail ainsi qu'à l'extérieur de l'Université de Genève: Alain, Alexia, Aleks, Alison, Arnaud, Bruno, Carole, Cristina, Christian, Christopher, Coralie, Corrado, Cyrielle , Cyrille, Danny, Daniela, Damien, David, Didier, Fabien, Frédérique, Gaëlle, Giada, Guillaume, Heather, James, Jérôme, Jean, Julien, Katia, Katja, Konnie, Kim, Leo, Lia , Lore, Luca, Marc, Marcello, Massimo, Mohammad, Mohsen, Naëm, Olouf, Régine, Sascha, Simon, Soheil, Steffi, Stéphanie, Swann, Ulf, Ulrike, Tobias et Wiebke.

Un remerciement spécial aux membres du E3 Lab pour m'avoir accueilli dans ma nouvelle

«maison» pendant toutes mes années de doctorat (et même avant), et à Mme M. Hawkins, Mme K. Lopez et le Docteur C. Steinberger pour leur aide avec la grammaire anglaise et les corrections de syntaxe. Merci à Alexandra, Andrea, Aline, Chiara, Eva, Géraldine, Patricia,

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Ryan, Tiffany, Vanessa et Yoann pour le mélange quotidien de fun et de science, Christophe et Sylvain pour leurs prouesses informatiques, Rémi et Ben pour leurs clarifications statistiques, Marion pour sa bonne humeur et son efficacité.

Enfin, je remercie ma famille et surtout mes parents et mon frère pour leur affection, leur présence et le soutien moral qu'ils m'ont toujours apporté tout au long de ma vie. Leur présence a beaucoup contribué à la réussite de ce travail.

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1. Abstract

Almost all perceived volatile compounds stimulate both the main olfactory system and the trigeminal system. Through these systems, it is possible to orient intentionally oneself by spatially localizing an odor, but whether a scent can automatically orient visuospatial attention remains unknown. Yet, i) there is a common pool of attentional resources shared across sensory modalities, ii) olfactory and trigeminal systems enable humans to differentiate between a stimulation delivered to the left or the right nostril, and iii) trigeminal stimulations can send alert signals and can thus be considered relevant stimuli, which are particularly prone to capture an individual’s attention. We used carbon dioxide (CO2) and eucalyptol as intranasal lateralized exogenous cues in a variant of a visuospatial cueing paradigm, the Posner task. We varied the delay between the start of the cue and the target, called stimulus-onset asynchrony (SOA), in each of the seven studies. In the Posner task with exogenous orienting of attention, trials are called valid trials when cues appear at the targets’ locations, whereas they are called invalid trials when they appear at the opposite side of the targets’ locations. As predicted, an intermodal effect was observed: reaction times in valid trials were faster than invalid trials. We found that the length of the SOA is crucial in showing this effect. Indeed, we found a cueing effect of the eucalyptol with an SOA of 610 ms. The cueing effect of the CO2 occurs with a SOA of 680 ms and of 1180 ms. Results suggest that the type of stimulant might influence the time window of the cueing effect.

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1. Résumé

Presque tous les composés volatils perçus stimulent à la fois le système olfactif principal et le système trigéminal. Grâce à ces systèmes, il est possible de s'orienter intentionnellement en localisant spatialement une odeur, mais on ignore si une odeur peut automatiquement orienter l'attention visuo-spatiale. Pourtant, i) il existe une banque commune de ressources attentionnelles partagées à travers les modalités sensorielles, ii) le système olfactif et trigéminal permettent aux humains de différencier une stimulation délivrée dans la narine gauche ou droite, et iii) les stimulations trigéminales peuvent envoyer des signaux d'alertes et sont donc considérées comme des stimuli pertinents, qui sont particulièrement susceptibles de capter l'attention d'un individu. Nous avons utilisé le dioxide de carbone (CO2) et l'eucalyptol comme indices exogènes intranasaux latéralisés dans une variante du paradigme d’indiçage spatial (tâche de Posner). Nous avons fait varier l’intervalle de temps entre l’apparition de l’indice (l’amorce) et de la cible, appelée « Stimulus Onset Asyncrony » (SOA), dans chacune des sept études. Dans la tâche de Posner avec une orientation exogène de l'attention (les amorces n’aident pas les participants), les essais sont appelés des essais valides lorsque les amorces apparaissent aux emplacements des cibles, alors qu'ils sont appelés des essais invalides lorsqu'ils apparaissent du côté opposé des emplacements des cibles. Afin de s’assurer que les mouvements oculaires et la respiration du participant n’interfèrent pas avec notre tâche, nous avons enregistré l’activité éléctro-occulographique liée aux saccades latérales des yeux et le rythme respiratoire. De plus, nous nous sommes assuré que notre olfactomètre pouvait délivrer intra-nasalement nos stimulations chémosensorielles de manière fiable, reproductible, avec une grande précision temporelle, sans que d’autres stimulations soient perçues par les participants.

Finalement, nous avons contrôlé que les participants percevaient correctement les stimulations de CO2 et d’eucalyptol dans la narine gauche et la narine droite en réalisant, au préalable, une tache de détection des stimuli latéralisés. Comme prévu, un effet intermodal a été observé: les

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temps de réaction dans les essais valides étaient plus rapides que les essais invalides. Nous avons constaté que la durée du SOA est cruciale pour révéler cet effet. Effectivement, nous avons trouvé un effet d’amorçage de l'eucalyptol avec un SOA de 610 ms. L'effet d’amorçage du CO2 s’est produit avec un SOA de 680 ms et de 1180 ms. Les résultats suggèrent que le type de molécule utilisé pour l’amorçage pourrait influencer la fenêtre temporelle de l’apparition de l'effet. L’orientation de l’attention visuelle par des stimulation trigéminales pourrait fournir un nouvel outil aux cliniciens pour restaurer l’équilibre attentionnel entre le champs visuel gauche et droite chez des patients souffrant d’héminégligence. L’entrainement de l’orientation attentionnel vers le coté négligé par l’administration de stimulations trigéminales pourrait même aider les patients chroniques grâce à une mise en scène de leurs tâches de tous les jours en réalité virtuel.

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2. Introduction

Recently, researchers discovered that humans can orient themselves with olfactory stimulations by scent-tracking (Porter et al., 2007). Indeed, participants were able to follow a scented track with only the olfactory system, and they were performing better at it with practice and inter- nostril comparisons. This discovery showed that humans can voluntarily localize an odorant source by actively moving their nose around it. However, whether or not an odor can automatically orient human in the environment under immobile conditions remains unknown.

Of all the senses, the chemosensory ones are the most spread through the animal kingdom. Even simple cell organisms, such as bacteria, possess a sensory system to detect chemical molecules.

In humans, the chemosensory systems contribute actively to the everyday life, e.g. in the regulation of the food intake, in the social and affective life. They also play a defensive role in detecting toxic substances and in giving us the opportunity to react rapidly with adaptive behavior, such as running away.

However, volatile chemicals are usually invisible and thus are not perceived as clearly as classical salient stimuli, such as sparkling lights or screams. Moreover, the human ability to lateralize volatile chemicals seems reduced by the short distance between the nostrils.

Nevertheless, the trigeminal system shares some interesting properties with the olfactory system, such as short neuron connections to the thalamus and the brain stem, and a high potential for capturing individual attention. Furthermore, its ability to rapidly detect and to discern which nostril is stimulated under immobile conditions makes the trigeminal system the ideal candidate to answer to our specific question: is there a covert lateralized automatic orienting of attention after a lateralized intranasal trigeminal stimulation? In order to answer this specific question, the lateralized intranasal trigeminal stimulation that should orient attention must be uninformative (exogenous), meaning that they do not help the participant in

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his task. This statement guarantees the automaticity of the attentional effect. In order to investigate the first process of attentional orienting (covert attention), the gaze of the participants has to be directed straight in front of them during the experiments to ensure that no eye saccades are involved.

The theoretical introduction of the thesis is divided into two major parts. In the first one, we will examine the trigeminal system according to different aspects; the types of signals that are incorporated, how they are incorporated, and the ensuing psychological and physiological effects. Key points will be highlighted such as the fact that the trigeminal system reaches the thalamus, a consciousness and alertness regulator, with only one relay station between the neurons with receptors in the outside world and in the thalamus. These connections are made by two types of nerve fibers, C-fibers and Adelta-fibers, which produce two different kinds of feelings. The trigeminal receptor activated by the stimulant and the concentration of the stimulant influence the type of activated fibers. The choice of CO2 as a pure or almost pure trigeminal stimulant and eucalyptol as a strong pleasant trigeminal stimulation for our experiments will be detailed. Psychological responses, such as improvement of alertness, and physiological responses, such as coughing, will be enumerated to emphasize the role of the trigeminal system as an alert system. The interactions between the olfactory and the trigeminal system will then be presented. Different solutions will be presented to distinguish between the olfactory and the trigeminal systems, such as the ability without movements to lateralize trigeminal stimulations but not olfactory stimulations.

In the second part, we will explore the likelihood of trigeminal stimulations of orienting visual spatial attention as do visual cues. First, the concept of spatial visual attention will be defined and explained. Second, the original cueing task (the Posner task) with visual cues and targets will be presented. Third, the concept of a common pool of attentional resources shared between senses (called modalities) will be presented.

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Few characteristics were required to answer to our research question. Firstly, to have a natural automatic cueing, the cues must be peripheral (presented on both sides of participants).

Secondly, the cues have to be salient and pertinent. Thirdly, the delay between the cue onset and the target onset has to be adapted to chemosensory cues. While the first two key points may be satisfied with the trigeminal cues, the third point is almost completely unknown. This is the case because it is extremely complicated and rare to have the possibility to deliver odors with adequate precision. A perfect control of a modern olfactometer is necessary to respect the key points of a Posner task with chemosensory cues. The chemosensory stimulations and the air have to be delivered precisely without giving any other clues or distractions. Indeed, the timing of the cue delivery has to be extremely accurate, with similar flow to both nostrils during and between stimulations, with constant trigeminal concentration for every puff during the whole experiment but without polluting the environment, or contaminating the delivery system. A few attempts to cue spatial attention with intranasal chemosensory stimulation failed to discover a cueing effect that clearly affects behaviors. However, all these previously presented points suggest that this topic deserves a more extensive investigation and our hypothesis will be presented at the end of the theoretical introduction.

2.1 Sensing the outside world

Even if five senses are generally recognized in human nature, there are many more senses. The type of stimuli encoded by the brain usually categorizes the sensory systems. Visual perception is the ability of the cortex to respond to light within the visible spectrum. The resulting perception is known as visual perception, eyesight, sight or vision. The various physiological components involved in vision are referred to collectively as the visual system. The ability to detect mechanical pressure or distortion is a part of the sensory nervous system. The sensory receptors are mechanoreceptors. They are present in glabrous skin, in hairy skin and in hair cells. The ability to detect the thermal properties of the surrounding environment as well as of

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one’s own body is done by thermally-sensitive neurons which are present in many different parts of the human body such as the skin, muscles, brain, spinal cord, and viscera (Filingeri, 2016). These neurons provide information regarding thermal conditions and modulate autonomic thermal responses such as increased sweating. In the peripheral nervous system, cold-sensitive receptors are present in larger numbers than warm-sensitive thermoreceptors, while in the central pathways this relation is inverted.

The ability to perceive chemicals relies on three different sensory systems: the olfactory system, the gustatory system, and the trigeminal system. Whereas gustation perceives molecules in solutions, the olfactory and trigeminal systems detect volatile molecules in the environment.

Almost all odorants activate both the olfactory and the trigeminal systems (Frasnelli, Hummel, Berg, Huang, & Doty, 2011) however a higher odorant concentration is needed to activate the trigeminal system (Abraham, Sanchez-Moreno, Cometto-Muniz, & Cain, 2007; Kleemann et al., 2009).

The activation of the trigeminal system is dependent on the chemical properties of the odorant that vary from low trigeminal to high trigeminal. This is called the “trigeminality” of the molecule (Frasnelli, Hummel, et al., 2011).

2.2 The trigeminal system

The trigeminal system is poly-modal; it allows the perception of temperature, pH, chemical substances and mechanical pressure (Latorre, Brauchi, Orta, Zaelzer, & Vargas, 2007; Viana, 2011). Distinct from the olfactory system, the trigeminal system innervates the nasal cavity as well as the eye. We will focus on the chemical perception of the trigeminal system.

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2.2.1 The receptors

In humans, the chemical activation of the trigeminal system is mainly made through one of the three transient receptor potential (TRP) channel families: TRPV (vanilloid), TRPM (melastatin), and TRPA (ankyrin) (Frasnelli & Manescu, 2017; Nilius & Owsianik, 2011;

Venkatachalam & Montell, 2007). The TRPV channels present in the trigeminal system are TRPV1, TRPV2, and TRPV3. Only TRPM8 and TRPA1 are expressed in the trigeminal system from the TRPM and the TRPA channel families (Frasnelli & Manescu, 2017; Viana, 2011).

These ion channels are activated by changes in membrane voltage, temperature, or ligand binding depending on their architecture and subsequently transduce this information into conformational changes that open channel pores (Paulsen, Armache, Gao, Cheng, & Julius, 2015). These channels are constituted by six transmembrane domains containing a pore. The opening of channels generates a graded transduction current. This induces a depolarization and then a firing of an action potential. It has been showed that the regions involved in the binding of TRPV1 agonist are different from the regions involved in the temperature activation.

Moreover, it is suggested that the module sensing the temperature is different from the module sensing the voltage (Latorre et al., 2007). Receptors are present in sensory neurons of mucosal epithelium, and in the skin. Whereas TRPV1 is only expressed in nociceptive neurons, TRPM8 is expressed in both the nociceptive and the non-nociceptive neurons. Thus, different channel families exist and a small diversity of chemical receptors can specifically activate the trigeminal system.

2.2.2 Neuroanatomy of the trigeminal system

The trigeminal nerve (cranial nerve V) is the largest cranial nerve. It has three major branches:

the ophthalmic nerve, the maxillary nerve, and the mandibular nerve. Each branch innervates a

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different zone (Figure 1). The ophthalmic nerve and the maxillary nerve innervate the nasal mucosa while the maxillary nerve and the mandibular nerve innervate the oral mucosa.

Figure 1: Schema of the innervation of the nasal cavity. From http://www.rahulgladwin.com retrieved 22.08.2017.

The three branches converge in the trigeminal ganglion where the cell bodies of the neurons are situated (Figure 2). From there, neurons project to the trigeminal nucleus. They make synaptic connections with second order neurons in the trigeminal nucleus then project to the thalamus, which is a regulator for consciousness and alertness. From the medial thalamic nuclei, neurons project to the somatosensory cortex. Note that only three series of neurons are solicited for transmission of the information from the lumen of the nasal cavity to the somatosensory cortex, and that the somatotopic information is preserved throughout the pathway.

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Figure 2: Schema of the pathway triggered by a trigeminal stimulus. A: Receptors of trigeminal neurons are in the epithelium of the nasal cavity (brown). B: The trigeminal ganglion (grey). C:

Trigeminal nucleus with the first relay station (1) in the brain stem (blue). D: Thalamus (green) with the second relay station (2). E: Somatosensory regions of the cortex (orange) are connected to third-

order neurons (3). From Frasnelli & Manescu (2017).

The type of stimulation and the location of the mucosa stimulated are important. The anterior portion of the nasal cavity is more responsive to CO2 stimulation and not to mechanosensory stimulation (Frasnelli, Heilmann, & Hummel, 2004). Trigeminal receptors for chemical detection might be more numerous in this area (Scheibe, Schmidt, & Hummel, 2012).

Moreover, the chemosensitive afferent innervation of the nasal epithelium is constituted by two major nerve fibers; unmyelinated C-fibers and myelinated Adelta-fibers (Anton & Peppel, 1991;

Sekizawa & Tsubone, 1994). The perception of pain and warmth is mediated by C-fibers (Mackenzie, Burke, Skuse, & Lethlean, 1975; Sinclair & Hinshaw, 1950; Torebjörk & Hallin, 1970). Stinging and sharp sensations are mediated by Adelta-fibers (Mackenzie et al., 1975;

Torebjörk & Hallin, 1973). Differential activation of Adelta-fibers or C-fibers is concentration dependent (Hummel, Livermore, Hummel, & Kobal, 1992).

In the next chapter, the regions engaged by the trigeminal nerve will be presented.

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2.2.3 Cerebral structures of the trigeminal system

The regions activated by stimuli other than chemicals are the inferior portions of the postcentral gyrus in the somatosensory cortex for the maxillary nerve and the superior regions in the central sulcus for the mandibular nerve. To investigate the additional cerebral structures activated by trigeminal chemicals, three approaches can be used.

Firstly, one can use a pure or almost pure trigeminal stimulant like CO2 or capsaicin (Cain, 1976; Coates, 2001; Husner et al., 2006). Both of these stimulants are painful for participants.

Moreover, capsaicin has little or no vapor pressure. The molecule is much larger than CO2, it does not fly as an aerosol without water vapor, and is therefore difficult to use in experiments with volatile chemosensory stimuli. There are no purer trigeminal stimuli available and most of olfactory stimuli stimulate also the trigeminal system, thereby the distinction between the cerebral structures involved in trigeminal and olfactory perception has been rarely done. Thus, most of the literature on the cerebral structures activated by the human trigeminal system use CO2 (Savic, Gulyás, & Berglund, 2002). Research showed that CO2 stimuli activate small nociceptive fibers, including Adelta-fibers (Steen, Reeh, Anton, & Handwerker, 1992; Thürauf, Friedel, Hummel, & Kobal, 1991). CO2 stimulation engages (additionally to the somatosensory regions) the insula, the orbitofrontal cortex, and the piriform cortex, brain regions that are usually considered olfactory and gustatory regions (Albrecht et al., 2010).

Secondly, one can examine the trigeminal system of patients who have lost the sense of olfaction (anosmic patients). However, the assessment of their normality can be difficult.

Additionally, trigeminal information is not processed the same way when the olfactory system is not working anymore (Frasnelli & Hummel, 2007).

Thirdly, one can perform a subtraction of a bimodal brain activity (trigeminal and olfactory activity) with the brain activity of a unimodal activity (olfactory activity). With this technique,

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a significant recruitment of the right insular and bilateral cingulate cortices for iso-amyl-acetate (odor similar to banana or pear), was shown (Lombion et al., 2009). This approach carries risks because some confusion can occur, underdetermining the identification of which region is activated by the trigeminal component of the odor and which region is activated by the olfactory component of the odor.

Thus, it is safer to work with CO2 when studying the cerebral structure involved in the chemical response of the trigeminal system even though it can be unpleasant for participants.

2.2.4 Trigeminal stimulations

Many different stimulations activate the trigeminal system, e.g. thermal, electrical, and chemical. Mechanical stimulations such as air puffs produce trigeminal stimulation (Iannilli, Del Gratta, Gerber, Romani, & Hummel, 2008). Mechanical, painful and thermal perceptions are well known because they are the main sensations created by the trigeminal system.

However, researchers discovered recently the specific chemical stimulation of the trigeminal system. Indeed, TRPV1 (Caterina et al., 1997) and TRPV3 receptors (Xu, Delling, Jun, &

Clapham, 2006) are heat-triggered whereas TRPM8 (McKemy, Neuhausser, & Julius, 2002) and TRPA1 receptors (Bandell et al., 2004; Jordt et al., 2004) are triggered by cold. A temperature of 17°C or below activates TRPA1 (Story et al., 2003). TRPM8 is directly activated by temperatures below 28°C (McKemy et al., 2002). Voltage can also activate trigeminal neurons. Actually, a pH under 6 makes the protons activate TRPV1 at room temperature (Latorre et al., 2007). Thus, TRPV1 is suggested to be involved in inflammatory pain since tissue acidification is induced by ischemia and inflammation.

In addition, many chemicals stimulate the trigeminal system. The detection of many chemicals may have a protective function for predators (informing them of potential poisons) and a defensive function for plants that even use it to deter against predators. Oral chemoperception

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explains the effects of the coolness of peppermint, the warmness of chilli peppers, the tingle of carbonated drinks, and the irritation of nicotine (Table 1). Humans have developed a liking for trigeminal foods, beverages, and spices. Indeed, a large variety of plant-derived natural food stimulates the trigeminal system (Viana, 2011).

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Table 1. Plant-derived trigeminal stimulants from Viana, 2010. Abbreviations are used for the name of trigeminal receptors: V1 for TRPV1, A1 for TRPA1, V2 for TRPV2, V3 for TRPV3, and M8 for TRPM8. The symbol > indicates that the receptor on the left responds more to, or has a higher affinity for, the trigeminal stimulant.

The fact that chemicals produce cold or warm feelings suggests an evolution of the trigeminal system in detecting chemicals that could harm individuals. Accidental transposition of olfactory receptor genes near to a sequence of DNA regulating the expression of a trigeminal receptor during transmission of the genome might have allowed the expression of olfactory receptors in the trigeminal system, which still produces the thermal sensation. This genetic modification

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that gives new tools to organisms through evolution, was observed in the mouse (Dietschi et al., 2017).

Thus, the trigeminal nerves convey stimulations classified with different physical properties.

Various types of trigeminal stimulations can stimulate similar receptors and thereby elicit sensations.

2.2.5 Trigeminal sensations

The sensory part of the trigeminal system provides mainly proprioception, pain, and temperature perception of the face. In this section, we will investigate the sensations triggered by chemical activations.

In 1978, it was shown that anosmics were able to feel a limited spectrum of sensations such as burning, warmth, coolness, or itching through the trigeminal system (Doty et al., 1978). For decades, it was believed that the activation of the trigeminal system was initiated by nonspecific interactions between the chemical compounds of the odors and the endings of the trigeminal nerve. However, the identification of trigeminal receptors showed that the trigeminal activation is specific to the interaction between molecules and receptors (Bandell et al., 2004; Caterina et al., 1997; McKemy et al., 2002; Xu et al., 2006). The activation of the trigeminal system may produce many sensations, such as pain, pungency, sharpness, astringency, scratching, tickling, prickling, sneezing, burning, warmth, stinging, or coldness (Frasnelli, Albrecht, Bryant, &

Lundström, 2011; Laska, Distel, & Hudson, 1997).

The sensations elicited by three molecules that mainly activate three different trigeminal receptors (TRPM8, TRPV1 and TRPA1) were investigated (Filiou, Lepore, Bryant, Lundström,

& Frasnelli, 2015). Principal Component Analysis¹ has shown that these trigeminal activations

1 The Principal Component Analysis (PCA) is a statistical test that determines which variables called principal components explain the best the variation of result values (Wold, Esbensen, & Geladi, 1987).

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could be described by 4 characteristics on the 12 trigeminal descriptors studied. The 4 main descriptors were “intensity”, “warmth”, “pain”, and “cold”. Filiou and al. (2015) suggest that painful, prickly, ticklish, and scratchy sensations constitute the nociceptive aspect of the trigeminal percept. However, other trigeminal receptors such as TRPV2, TRPV3, or KCNK, which can be found in plants (Viana, 2011) haven’t been included into the investigation. Thus, more qualifiers will be integrated in the next paragraph in order to give an exhaustive point of view.

The sensation of warmth is produced by the activation of the receptor TRPV1 and TRPV3 while the sensation of cold is produced by the activation of the receptor TRPM8. Trigeminal receptor TRPV1, specifically activated by capsaicin (Caterina et al., 1997) and camphor (Xu, Blair, &

Clapham, 2005; Xu et al., 2006), elicits burning, stinging, and tickling sensations. Camphor increases the perceived intensity of the cutaneous sensation produced during arm heating and cooling (Green, 1990). Ingredients, such as cinnamon that contains cinnamaldehyde, specifically stimulates TRPA1 (Bandell et al., 2004). In 2002, the menthol receptor was cloned and it was proposed that its function was to transduce cold stimuli in the somatosensory system (McKemy et al., 2002). The sensation of coldness is mainly produced by the activation of TRPM8 in sensory nerve fibers (Bautista et al., 2007). The unique perception of the Szechuan peppercorns is described as “tingling and numbing”, “mild electric shock”, or as having a “pins and needles” effect (Bautista et al., 2008). KCNK channels trigger this effect.

These sensations can trigger different responses. In the next chapter, some of the different human responses will be presented.

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2.2.6 Human responses to trigeminal stimulations 2.2.6.1 Psychological

Many odors that stimulate the olfactory and trigeminal system (Doty et al., 1978; Von Békésy, 1964) have been used as ambient odors to test their potential effects on human behavior.

Peppermint odor can improve performance, vigilance, alertness, and enhance memory (M.

Moss, Hewitt, Moss, & Wesnes, 2008; Warm, Dember, & Parasuraman, 1991). Warm et al., (1991) suggest that exposure to peppermint may serve as an effective supplementary stimulation in tasks demanding close attention for prolonged periods. Odors such as pyridine and lavender improve simple reaction time performance after a visual stimulus (Millot, Brand,

& Morand, 2002). However, when the task involved more cognitive resources², the lavender odor decreased participants’ attentional speed, contrary to rosemary odor (M. Moss, Cook, Wesnes, & Duckett, 2003). Moreover, bimodal odors such as the allyl isothiocyanate can enhance the effect of visual distractors and slow down the response times of participants to visual targets (Michael, Jacquot, Millot, & Brand, 2003). Michael et al. (2003) conclude that odors modulate the attentional system’s responsiveness to visual objects.

Thus, the complexity of the task and the type of odor has a critical effect on human behavior and the trigeminal sense may influence processes implicated in attention.

2.2.6.2 Physiological

The intensities of the stimuli appear to be decisive in the type of sensation that is elicited and thus in the type of fibers that are activated. For example, nicotine produces a burning sensation at a certain concentration and starts to produce stinging with a higher concentration. In addition,

2 Moss et al., 2003 used three different tasks to measure the speed of attention: a simple reaction time task (participants had to press a button, when they saw “yes” was displayed on the screen), a digit vigilance task (participants had to press a button when the number in the center of the screen matched a constant number on the right), and a choice reaction time task (participants had to press on one button when “yes”, and another when “no”, were displayed on the screen).

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burning and stinging appear to follow a different time course; stinging starts almost immediately after stimulation while the first pain sensation starts after several seconds (Hummel et al., 1992). Indeed, burning starts after several seconds while a stinging sensation starts almost immediately after the stimulation. The two sensations reach their maximum intensity at different times (Hummel, Gruber, Pauli, & Kobal, 1994). Furthermore, the overall intensity appears to be dependent on the length of the interval between two stimulations. When the interval is ≤ 3 s, the burning painful sensation increases but when it is at a long enough interval (> 20 s for CO2 stimuli), the intensity of the stinging sensations decreases with each successive stimulus. These differences are certainly due to the type of stimulated fibers that have been previously described.

The Szechuan pepper has been found to have anaesthetic properties. This unique property is produced by hydroxyl-alpha-sanshool that inhibits pH-sensitive background potassium channels (KCNK), which excite trigeminal neurons (Bautista et al., 2008). Like Szechuan pepper, eugenol can also have anaesthetic properties that can weaken its trigeminal perception, which can impair the capacity of localizing the presence of the odor in the nostrils.

Additionally, the intranasal trigeminal system triggers physiological reflexes automatically.

The stimulation of C-fibers releases a neuropeptide that can produce glandular secretion, tissue swelling, and facilitates mast cell degranulation (Stjärne, Lundblad, Änggård, Hökfelt, &

Lundberg, 1989). Tissue swelling diminishes luminal size, thereby increasing nasal airway resistance and the work of nasal breathing. Thus, the airflow obstruction reduces the risk of further inhaling dangerous molecules. The ingestion of hot or spicy food can trigger nasal secretion and even lacrimal secretion, depending on the individual and the strength of the stimuli (Shusterman & Murphy, 2007). Through its connections to the brain stem, the intranasal trigeminal system can trigger reflex sneezing, coughing, gagging, and vomiting. At the same time, it also influences the vasoconstrictor system reflexes (Baraniuk & Merck, 2009).

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2.2.6.3 The cumulative effect

In the main olfactory system, rapid repetitive stimulations lead to a reduction of the intensity of the perception, called the habituation effect. In contrast, a rapid repetitive painful stimulation of the trigeminal system leads to an increase of the intensity of the stimulation perceived, accompanied by a painful sensation (Hummel et al., 1994). This increase of the painful sensations, called the cumulative effect, may be due to the central nervous summation of the input created by stimulation of C-fiber afferents. Indeed, a rapid electrical, mechanical, or thermal stimulus to the foot or the hand can generate two successive sensations of pain. The first pain, related to Adelta-fibers, is followed about 1 s later by the second pain related to the C- fiber. To resume, the second pain is undeterred by the partial suppression of the trigeminal sensory exercise. In comparison, this summation effect does not appear to affect the Adelta-fibers due to their adaptability to sustained painful stimulations (Adriaensen, Gybels, Handwerker, &

Van Hees, 1983; Sumino & Dubner, 1981). It is important to note that concerning desensitization, the sensation produced by Adelta-fibers is less noticeable when compared to similar processes in C-fibers (Adriaensen, Gybels, Handwerker, & Van Hees, 1984;

Handwerker, Anton, & Reeh, 1987). This suggests that an eventual decrease in Adelta-fibers sensation, after repetitive stimulation, may be due to both peripheral adaptation and/or habituation (Price, Hu, Dubner, & Gracely, 1977).

All these effects produced by trigeminal exposure are useful for different purposes; in the next chapter, different theories will be presented.

2.2.7 Trigeminal functions

The trigeminal nerve innervates the mandibular muscle, which produces the chewing motion but we will focus more on its role related to chemical perception. The main functions of the trigeminal system are the monitoring of the nasal mucosal environment. This system detects

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and clears inhaled harmful substances. It has four missions. First, the immediate secretion of protective mucus, which dilutes injurious inhalants and protects sensitive tissues. Second, coughing and sneezing as protective automatic reactions to expel noxious substances. Third, diminish the breathing rhythms (Walker et al., 2001) to reduce inhalation of toxic substances.

Fourth, the olfactory system with the intranasal trigeminal system monitors inhaled air for composition and quality (Doty et al., 1978) in order to inform individuals of potential dangers.

Thus, trigeminal functions defined the trigeminal system as a monitoring system, which could alert. The trigeminal system shares some of its functions with the olfactory system.

2.2.8 Interaction between olfaction and the trigeminal system

Disentangling the trigeminal stimulation from the olfaction is a difficult task. Indeed, there are many interactions between olfaction and the trigeminal system because of their common neuroanatomy and functions.

Odorant mixture of trigeminal and olfactory stimulation recruits more brain areas than pure olfactory stimuli or almost pure trigeminal stimuli. These brain regions, such as the anterior orbitofrontal cortex, are specialized in mixture processing (Boyle, Djordjevic, Olsson, Lundström, & Jones-Gotman, 2008). Co-stimulation with an olfactory stimulus increases arousal responses to trigeminal stimulations (Stuck, Baja, Lenz, Herr, & Heiser, 2011).

Additionally, cold perception is enhanced if both the mainly trigeminal molecule and the mainly olfactory molecules are delivered at the same time but in different nostrils, whereas intensity, warm and painful dimension are enhanced if the mixture is presented in both nostrils. Olfactory dysfunction impairs the lateralization score. The greater is the duration of the olfactory dysfunction, the lower is the lateralization score (Kendal-Reed, Walker, Morgan, LaMacchio,

& Lutz, 1998). The observation of patients with acquired anosmia within two years compared to patients with acquired anosmia within a time longer that two year showed a difference in the

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trigeminal event-related potential amplitudes. Indeed, the latter group elicited bigger trigeminal event-related potential amplitudes compared to the patients with recently acquired anosmia.

This suggested a cross-modal plasticity that would increase trigeminal sensitivity over time in compensation for the complete loss of olfactory function.

Even if the trigeminal system has many interactions with the olfactory system, different evaluations of the trigeminal system can be done.

2.2.9 Investigation of the trigeminal system 2.2.9.1 Brain imaging

Researchers used functional MRI to explore sensory processing, including trigeminal processing. They discovered that chemosensory trigeminal stimulation activates brain regions partly similar than somatosensory stimulation, such as brain stem (Albrecht et al., 2010), thalamus (Iannilli et al., 2008), SI/SII (Iannilli, Gerber, Frasnelli, & Hummel, 2007) and anterior cingulate (Albrecht et al., 2010). However, trigeminal stimulant also engaged olfactory area such as the piriform, the orbitofrontal and the insular cortex.

2.2.9.2 Electroencephalography

Two electroencephalographic (EEG) techniques allow the objective recording of the activation of the trigeminal system because they are less dependent on the participant’s collaboration than on brain imaging techniques. The first EEG technique is called trigeminal event-related potentials and the second one is called negative mucosal potential. The latter technique is relatively free from olfactory interference because the measurement is directly made by an electrode placed on the respiratory mucosa (Ottoson, 1955). The negative mucosal potential is a negative wave around 1000 ms after the stimulation (Frasnelli & Hummel, 2007). The amplitude of the wave increases with the sensitivity of the neural mucosa (Scheibe, Zahnert,

& Hummel, 2006). The event-related potential technique requires electrodes on the scalp

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(Kobal, 1981) that record a global signal from several cortical neurons. The advantage of this technique is the very high temporal resolution. Central and parietal electrodes usually produce the largest positive peak and the largest negative peak, respectively 200 ms and 400 ms after the trigeminal stimulation (Frasnelli, Lötsch, & Hummel, 2003; Kobal, Hummel, & Van Toller, 1992).

2.2.9.3 Behavioral method

Because almost all the trigeminal stimulants first activate the olfactory system, a psychophysical method was invented to try to test the performance of the trigeminal system (Von Skramlik, 1925). This method uses multiple monorhinal stimulations and participants under immobile conditions. Indeed, participants perform almost randomly when they have to indicate the side stimulated only by the olfactory system without head motions (Frasnelli, Ariza, Collignon, & Lepore, 2010; Kleemann et al., 2009; Kobal, Van Toller, & Hummel, 1989;

Wysocki, Cowart, & Radil, 2003) or if the stimulation is too short (Frasnelli, Robert, &

Steffener, 2017). Doubtlessly, the more the substance stimulates the trigeminal system, the more participants discriminate left to right intranasal stimulation (Frasnelli, Hummel, et al., 2011; Hummel, Futschik, Frasnelli, & Huttenbrink, 2003; Kobal et al., 1989; Porter, Anand, Johnson, Khan, & Sobel, 2005; Von Békésy, 1964; Wudarczyk et al., 2016). This technique, which is based on the ability to better lateralize trigeminal monorhinal stimulation for a given number of trial, estimates the trigeminality of a substance and the trigeminal capability of a subject with the ratio of correct responses. It is especially useful when trying to identify individuals with reduced sensitivity (Frasnelli, Hummel, et al., 2011; Hummel et al., 2003).

Olfactory clinics generally use eucalyptol (when an olfactory stimulation is not a problem) because of its strong “fresh” trigeminality (TRPM8’s receptor), and the general agreeable sensation produced widely appreciated by individuals. A solution to distinguish between different levels of normal sensitivity is to reduce the time of exposure of the participant to the

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trigeminal stimuli (Frasnelli & Manescu, 2017). Actually, the time of exposure of the participant is as crucial as the participant breathing behavior. In breathing behavior, three different techniques are used. Firstly, the participant has to sniff (Frasnelli, Charbonneau, Collignon, & Lepore, 2009) but it is almost impossible to control precisely the duration of the sniff and thus the number of molecules over time that will be integrated by the trigeminal system (Wise, Zhao, & Wysocki, 2009). Secondly, the delivery of the molecule can be done directly in the nostril during normal breathing but a careful observation of the breathing rhythms has to be performed in order to control the stimulus volume. A deep breath in (or out) when the stimulus reaches the nostril could considerably weaken the stimulation (Frasnelli et al., 2009). Thirdly, the stimulation can be sent in the nostril when the participant holds their breath. This protocol allows a perfect control of the trigeminal stimulant volume and concentration into the nose but the delivery cannot be too long in order not to disturb normal respiration processes.

Thus, the trigeminal system can give a rapid lateralization information when the stimulant is presented in the right or left nostril (Kobal et al., 1989). This lateralization of trigeminal stimulations could possibly influence attention.

Summary of this part

In sum, we examined the trigeminal system to determine its potential to influence spatial attention and many arguments are encouraging. Indeed, the ophthalmic nerve and the maxillary nerve from the trigeminal system monitor the nasal cavity and can send fast alert signals to brain regions implicated in alertness through C-fibers and Adelta-fibers depending on the stimulations. These latter can stimulate different trigeminal receptors and produce completely different sensations from irritation (CO2) to freshness (eucalyptol). CO2 is the most tested trigeminal stimulation in research because it is a rare pure trigeminal stimulant. Thus, a lot of our knowledge about intranasal trigeminal brain processing is based on TRPA1 activation.

Eucalyptol is the most used stimulant in clinics because of its strong trigeminality and its

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appreciation by people. Many interactions exist between the olfactory and the trigeminal system but the ability of the trigeminal system to perceive and send instantly lateralized information to the brain is unique. Thus, intranasal trigeminal lateralized stimulus gives lateralized information, which could possess intrinsically the value of an alert signal, and orient attention.

2.3 Attention

The trigeminal alert signal could naturally capture attention. Indeed, processed pertinent information tends to capture attention but it is not that simple. The better the odor is detected, the greater are the probabilities to capture attention. This detection depends on the vapor pressure of the odor (the quantity of molecules emitted in the air) and on the detection threshold of the individual. The olfactory perception varies depending of the environment. The perception, which is the representation build by the consciousness, may vary depending of the interest or the training of the individuals. The sensibility to an odor increases with repetitive exposure. An individual’s familiarity with an odor influences the perception of it and the initial odor persist for a certain period of time.

Nevertheless, how attention can be captured by stimuli has been studied for a long time.

Concerning olfaction, one of the leads to follow was already brought by Edward T. Hall, who suggested that each sense is linked to a type of distance between people. Sight is the public distance, the distance between unknown people, and which allows them to exchange general information. Audition is the social distance, which allows communicating, sharing with others.

Touch and taste are the senses of the intimate distance. This is the distance of whisper, caress and confidence. The olfactory sense is situated between the social distance and the intimate distance, it is the personal distance. It is the distance of chat, of the relationship between friends, of experience, and of emotions sharing.

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In this second part of the theoretical part of the thesis, we will define attention and more specifically spatial visual attention and present how to study it operationally. Then, we will describe different critical aspects relevant to orienting attention with chemosensory cues, review the studies about orientation of attention with chemosensory stimulations, and present the technical challenges relative to chemosensory cueing that we will have to tackle.

“Attention is the behavioral and cognitive process of selectively concentrating on a specific information, to possess it vividly in mind, while ignoring other perceivable information”

(Anderson, 2005). It allows humans to adapt to the environment of everyday life that constantly stimulates its senses.

Attention can be allocated by attending to a location in the periphery without moving one’s gaze toward it (covert attention) or by directing one’s gaze toward an area (overt attention). The attentional deployment of covert attention is faster than overt attention and can be done simultaneously to more than one location. Visual covert attention is suggested to be a mechanism for quickly scanning the field of view for interesting locations. Because it is the first process to help monitoring the environment that subsequently can motivate eye movements, we will focus in this thesis on covert attention (Carrasco, 2011).

One fundamental aspect of the orientation of attention is the saliency of the stimulation. Indeed, the capture of attention is composed of two stimuli in quick succession. The first stimulus, which may orient the spatial attention, is the cue. The second one is the target, which usually requires a quick response of the participant. Various leads have been investigated to know what stimuli have a high power of spatial attentional capture (Theeuwes, 2004). Emotional stimuli have rapidly become a potential candidate to orient spatial attention (Carretié, 2014). Certainly, emotions modulate many cognitive processes, guide behavior and signal the presence of important events in the environment (Sander, Grandjean, & Scherer, 2005). It has been shown that when various stimuli compete for an access to the limited attentional resources of a person,

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a bias toward emotional stimuli allows efficient detection of these events and fast preparation of adaptive responses (Pourtois, Schettino, & Vuilleumier, 2013).

Another fundamental aspect in attention is to determine how visual selection is oriented. The characteristics of the stimulus that catch the attention make the difference between the two classes of attention. On one hand, if a salient and unattended stimulus captures attention and makes it aware of its presence, it is “explicit attentional capture” and the allocation of attention is exogenously oriented. Participants must not fail to detect the cueing stimulus; otherwise it is not “explicit attentional capture”. The orienting is controlled through external processes. On the other hand, a salient and irrelevant stimulus that affects performance of another task is

“implicit attentional capture” and the allocation of attention is captured endogenously. The orienting is controlled through internal processes. For example, the main difference between endogenous and exogenous cueing in spatial attention is that exogenous tasks need cues that are close location to the target (Prime, McDonald, Green, & Ward, 2008; Spence, 2010) while endogenous tasks can use central cues (as arrow pointing where the target should appear). Some phenomenon such as “inattentional blindness” can occur with the attentional capture. Typically, if participants are focused on something, they may fail to notice salient and distinctive objects (Simons, 2000). The attentional class of attention influences temporal aspects of processing.

Temporal attention can be investigated by cueing a location, then presenting rapidly two succinct visual stimuli at the attended location, or not, and asking participants to describe as quick as possible the first visual stimuli. If attention is cued endogenously, participants are less accurate when the cueing is valid, whereas if attention is cued exogenously, participants are more accurate when cueing is valid (Hein, Rolke, & Ulrich, 2006). The other form of attention is spatial attention that involves orienting attention to a location in space. Orienting is a natural and primitive function, e.g. heliotropism in plants as a function of orienting their leaves in function of the light. In humans, the numbers and the complexity of systems exploded, and so

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did the capacity of orienting senses toward or away from the signal sources in the environment.

Whereas the efficiency and rapidity supplied by automatic control of orienting would be important for predation and defence, voluntary control of orienting has certainly been crucial for evolutionary development. The recall of previous experiences stocked in the memory can be important in finding desirable food, objects or mates. Cognitive sciences try to understand how humans orient themselves with their limited resources in a world full of rapid stimuli.

2.3.1 Spatial visual attention

In this thesis, we will focus on how attention works on spatial visual attention, e.g. on how cueing one location at a time can influence the detection of a visual following stimulus. One of researchers goals is the transformation of complex phenomena into simpler mental operations that can be related to neural systems. Thus, Posner (1980) decided to investigate detection of simple sensory events with the idea that luminance increments in dark fields would facilitate the understanding of how spatial visual attention works. His study of attention divided it in three components: alertness, selectivity and processing capacity. In tasks that researchers design to study attention, the ability to develop and maintain an optimal sensitivity to environmental stimulation is investigated when participants receive a signal to prepare themselves at different intervals. The first component, alertness, must be developed rapidly and maintained over a relatively short period during this time waiting before a reaction time task. The second component of attention is the ability to select information from one source or one kind rather than another. This component was classically investigated in giving clues to the participants about what he has to look for. The third component, the processing capacity, is related to the idea of a limited central processing capacity. It is observed that when participants have to handle many tasks at the same time; they perform worst even if they do their best.

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2.3.1.1 The cueing Posner task

Posner et al. (1978), wanted to know if shifts in covert attention exist. Tasks based on participants response time have been created to investigate the covert orienting by measuring the efficiency of detecting events that appear at different spatial locations (Posner, Nissen, &

Ogden, 1978). If the efficiency of detecting an event was changed by orienting attention, it would prove that the line of attention would be separated from the gaze. Thus, Posner and al.

(1980) imagined a setup in which participants would respond in pressing a button as fast as possible after the presentation of a detection stimulus (a target stimulus) while the gaze is monitored with electrooculography. In this way, they could test if participants detect more rapidly the target when they knew where the stimulus would appear, even if no movements of eyes were observed. Three conditions were designed: 1) neutral, 2) valid trials, and 3) invalid trials (Figure 3). A neutral trial was a non-informative plus sign as a cue followed by a detection stimulus to the left or the right. A valid trial had an arrow as a cue, showing the side where the target stimulus is going to appear. An invalid trial was made of an arrow as a cue, showing the opposite side of the location of the target. This design gave the opportunity to calculate the cueing effect and distinguish both the benefits and the cost of it.

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Figure 3: Original task of Posner: valid (cued) and invalid (uncued) trials. The SOA (Stimuli Onset Asynchrony) is the time between the cue onset to the target onset. From Klein, 2000.

The cueing effect or the facilitation effect is the difference between average reaction time of valid and invalid trial. It reflects the strength of the spatial orientation by the cue and it is constituted by benefits and costs. Benefits are calculated by the difference between the reaction time for neutral trial and the reaction time when the attention is cued to the place in space where the stimulus occurs (i.e a valid trial). Benefits reflect at what point the participant’s spatial attention was efficiently cued. However, the difference of reaction time between neutral trial and invalid trial determined the cost, thereby; it represents how long it took to re-orientate your attention from the uncorrected cue to the target. Different variants of the task were explored (letter vs digit or higher vs lower than the cue) and they discovered that the more the task is difficult, the less is the overall effect (Posner, 1980).

Classically, this unimodal Posner task with visual stimuli as cues and targets has been used (Shulman, Remington, & Mclean, 1979) but an increasing number of studies started to

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investigate the capabilities to orient and report attention with different modalities and across- modalities.

At first, experimental research focused on simple cueing such as luminance increments. Later, in the 1990’s, they tested the negative emotion of fear with the use of fearful faces or anger faces as cues (Mogg & Bradley, 1998; Vuilleumier, Armony, Driver, & Dolan, 2001). More broad threatening stimuli were then investigated on individuals with and without anxiety (Bar- Haim, Lamy, Pergamin, Bakermans-Kranenburg, & Van Ijzendoorn, 2007). Recently, studies expanded the investigation of attentional biases to rewarding stimuli (Brosch, Sander, Pourtois,

& Scherer, 2008; Pool, Brosch, Delplanque, & Sander, 2016). Their studies have shown that the spatial cueing effect is affected by various stimuli.

2.3.1.2 Common pool of attentional resources between modalities

Since the seventies, the idea of a limited capacity of attention has been brought to the front of the scene. Human senses are usually exposed to multiple stimuli at the same time that cannot be processed at the same time (Desimone & Duncan, 1995). Dividing attention between two objects almost always results in poorer performance than focusing attention on one (Kastner, De Weerd, Desimone, & Ungerleider, 1998). Moreover, attentional capacity is weakened when two different modalities are targeted (Duncan, Martens, & Ward, 1997). Nevertheless, the attentional orientation can be cued by a stimulus that will influence the integration of a following stimulus. For example, spatial informative clues, given by audio and tactile cues influence the reaction time of audio and tactile targets (Lloyd, Merat, McGlone, & Spence, 2003), audio cues can influence participant’s reaction time to olfactory or audition targets (Spence, Kettenmann, Kobal, & McGlone, 2001; Spence, McGlone, Kettenmann, & Kobal, 2001), and visual cues can influence participant’s reaction time to olfactory or tactile targets (Spence, Kettenmann, Kobal, & McGlone, 2000).

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Thus, spatial attention can be oriented by stimuli in one modality that the integration of following stimuli in another modality. Other aspects of the spatial cueing task such as the cue modality and the SOA will be discussed in the next section.

2.3.1.3 Modality and timing

Additionally, the cueing modality and the timing are critical aspects that go together (Spence, 2010). The most critical time is the delay between the start of the cue and the start of the target, which is named stimulus onset asynchrony (SOA). This SOA is typically varied during the experiment to avoid automatic answers from participants. Plotting reaction time versus SOA (Figure 4), it can be seen that for some values of SOA, the cueing effect disappear or is reversed.

This reversed effect is called the inhibition of return (Klein, 2000). For visual cues, the attention orientation occurs with a SOA from 0 to ~100 ms, disappear with a SOA from ~100 to ~300 ms and the inhibition of return effect appears with a SOA from ~300 to ~500 and ~2400 ms (Palanica & Itier, 2015).

Figure 4: Typical results of Posner task of reaction time on SOA (ms). From Klein, 2000. Black dots are valid trial averages and white dots are invalid trial averages.

For audio cues, the inhibition of return effect appears later with a SOA of around 1150 ms (Lloyd & McGloneF, 2000). Indeed, audio and visual stimuli have different speeds of

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integration (Millot et al., 2002) and chemosensory related processes of integration are known to be slow (Bensafi, Rouby, Farget, Vigouroux, & Holley, 2002; Boesveldt, Frasnelli, Gordon,

& Lundström, 2010; Croy, Krone, Walker, & Hummel, 2015; Demattè, Sanabria, & Spence, 2009). In the next section, only exogenous cueing tasks with peripheral chemosensory cues will be examined.

2.3.1.4 Chemosensory cueing in Posner tasks

Since exogenous cueing reflects an automatic natural way of orientation and can be interpreted as an adaptive tool from an evolutionary point of view, we will focus on studies with modified Posner tasks that are cued exogenously with chemosensory stimulations. In one study, the Posner task was adapted with chemosensory stimulations as cues and audio stimulations as targets (La Buissonnière-Ariza, Frasnelli, Collignon, & Lepore, 2012). La Buissonnière-Ariza et al. (2012) used phenyl ethyl alcohol (odor similar to rose, which is an almost pure olfactory stimulant) as the olfactory stimulus, eucalyptol as the chemosensory stimulus, air puffs for the somatosensory stimulus and nothing at all for the control stimulus (2L/min in each nostril).

Participants were asked to hold their breath from just before the cue until to after their response.

The cues were delivered 600 ms before the lateralized audio target. Participants had to respond as fast and as accurately as possible by pressing one of two buttons in order to indicate the side of the audio target. All cueing conditions enhanced the responding abilities of participants, but no effect depending on the validity of trials (cueing effect) was observed.

Then, another adapted Posner task was used with phenyl ethyl alcoho diluted at 3/40 for 1500 ms, as the cue, delivered in a heated humidified airflow at ~7L/min with visual stimulation as targets (Moessnang, Finkelmeyer, Vossen, Schneider, & Habel, 2011). Participants were asked to breathe through their mouth. The control condition was made of distilled water. The visual targets appeared after 500 ms of the olfactory cue, and for 1000 ms (Figure 5). Participants had to answer as fast and as accurately as possible, indicating on which side the target, a

Orientation de l&#039;attention visuelle par des stimulations chemosensorielles intra-nasales

Thesis

Reference

Orientation de l'attention visuelle par des stimulations chemosensorielles intra-nasales

Faculté des sciences

ORIENTATION DE L’ATTENTION VISUELLE PAR DES STIMULATIONS CHEMOSENSORIELLES INTRA-NASALES

Matthieu ISCHER

Acknowledgements

Table of Contents

1. Abstract

1. Résumé

2. Introduction

2.1 Sensing the outside world

2.2 The trigeminal system

2.3 Attention

Orientation de l'attention visuelle par des stimulations chemosensorielles intra-nasales