Localisation of unilateral nasal stimuli across sensory systems

doi:10.1016/j.neulet.2010.04.074

Neuroscience Letters

Volume 478, Issue 2, 5 July 2010, Pages 102-106

https://doi.org/10.1016/j.neulet.2010.04.074 Get rights and content

Abstract

Odor stimuli presented to one nostril can only be localised if they additionally activate the trigeminal nerve's chemosensitive fibers. In this study we aimed to investigate characteristics in the localisation of unilateral trigeminal, olfactory and somatosensory nasal stimuli. We compared the ability of healthy young subjects to localise monorhinally presented (a) pure olfactory stimuli (phenyl ethyl alcohol), (b) mixed olfactory trigeminal stimuli (eucalyptol), and (c) somatosensory stimuli (air puffs). As expected, subjects could localise the air puffs and eucalyptol, but could not phenyl ethyl alcohol. Interestingly, we observed a significant correlation between localisation performance for eucalyptol and phenyl ethyl alcohol but not between the ability to localise somatosensory and trigeminal or olfactory stimuli. These observations show that on a behavioural level, the trigeminal chemosensory system is more intimately connected to the olfactory system than to the somatosensory system despite the fact that anatomically its information is conveyed via same nerve as the latter. Furthermore, they show that the trigeminal chemosensory system should therefore be considered a self-confined contributor to chemosensory perception.

References (49)

J. Albrecht et al.
The neuronal correlates of intranasal trigeminal function—an ALE metaanalysis of human functional brain imaging data
Brain Res. Rev.
(2010)
D. Bowers et al.
Pseudoneglect: effects of hemispace on a tactile line bisection task
Neuropsychologia
(1980)
J.L. Bradshaw et al.
Bisecting rods and lines: effects of horizontal and vertical posture on left-side underestimation by normal subjects
Neuropsychologia
(1985)
J.L. Bradshaw et al.
Head and body space to left and right, front and rear. II. Visuotactual and kinesthetic studies and left-side underestimation
Neuropsychologia
(1983)
R.L. Doty et al.
Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans
Physiol. Behav.
(1978)
A. Dufour et al.
Rightward shift of the auditory subjective straight ahead in right- and left-handed subjects
Neuropsychologia
(2007)
J. Frasnelli et al.
Responsiveness of human nasal mucosa to trigeminal stimuli depends on the site of stimulation
Neurosci. Lett.
(2004)
J. Frasnelli et al.
Chemosensory specific reduction of trigeminal sensitivity in subjects with olfactory dysfunction
Neuroscience
(2006)
T. Hummel et al.
Effects of olfactory function, age, and gender on trigeminally mediated sensations: a study based on the lateralization of chemosensory stimuli
Toxicol. Lett.
(2003)
E. Iannilli et al.
Trigeminal activation using chemical, electrical, and mechanical stimuli
Pain
(2008)

E Iannilli et al.

Intranasal trigeminal function in subjects with and without an intact sense of smell

Brain Res.

(2007)

M. Jones-Gotman et al.

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

Brain Cogn.

(1993)

A.M. Kleemann et al.

Trigeminal perception is necessary to localize odors

Physiol. Behav.

(2009)

J. Lewald

Gender-specific hemispheric asymmetry in auditory space perception

Brain Res. Cogn. Brain Res.

(2004)

L. Liu et al.

Capsaicin, acid and heat-evoked currents in rat trigeminal ganglion neurons: relationship to functional VR1 receptors

Physiol. Behav.

(2000)

A Livermore et al.

Chemosensory event-related potentials in the investigation of interactions between the olfactory and the somatosensory (trigeminal) systems

Electroencephalogr. Clin. Neurophysiol.

(1992)

R.A. Schneider et al.

Dependency of olfactory localization on non-olfactory cues

Physiol. Behav.

(1967)

J.C. Stevens et al.

Aging and the perception of nasal irritation

Physiol. Behav.

(1986)

J.C. Stevens et al.

Reduction of odor and nasal pungency associated with aging

Neurobiol. Aging

(1982)

H.J. Behrendt et al.

Characterization of the mouse cold-menthol receptor TRPM8 and vanilloid receptor type-1 VR1 using a fluorometric imaging plate reader (FLIPR) assay

Br. J. Pharmacol.

(2004)

J.A. Boyle et al.

Cerebral activation to intranasal chemosensory trigeminal stimulation

Chem. Senses

(2007)

J.A. Boyle et al.

On the trigeminal percept of androstenone and its implications on the rate of specific anosmia

J. Neurobiol.

(2006)

W.S. Cain et al.

Olfactory sensitivity: reliability, generality, and association with aging

J. Exp. Psychol.

(1991)

W.S Cain et al.

Interaction between chemoreceptive modalities of odour and irritation

Nature

(1980)

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Trigeminal stimulation is required for neural representations of bimodal odor localization: A time-resolved multivariate EEG and fNIRS study
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Whereas neural representations of spatial information are commonly studied in vision, olfactory stimuli might also be able to create such representations via the trigeminal system. We explored in two independent multi-method electroencephalography–functional near-infrared spectroscopy (EEG+fNIRS) experiments (n1=18, n2=14) if monorhinal odor stimuli can evoke spatial representations in the brain. We tested whether this representation depends on trigeminal properties of the stimulus, and if the retention in short-term memory follows the “sensorimotor recruitment theory”, using multivariate representational similarity analysis (RSA). We demonstrate that the delta frequency band up to 5 Hz across the scull entail spatial information of which nostril has been stimulated. Delta frequencies were localized in a network involving primary and secondary olfactory, motor-sensory and occipital regions. RSA on fNIRS data showed that monorhinal stimulations evoke neuronal representations in motor-sensory regions and that this representation is kept stable beyond the time of perception. These effects were no longer valid when the odor stimulus did not sufficiently stimulate the trigeminal nerve as well. Our results are first evidence that the trigeminal system can create spatial representations of bimodal odors in the brain and that these representations follow similar principles as the other sensory systems.
Assessment of direct knowledge of the human olfactory system
2020, Experimental Neurology
Citation Excerpt :
The pars externa is thought to be involved in olfactory lateralization in rodents (Esquivelzeta Rabell et al., 2017; Kikuta et al., 2010). Its absence in humans may account for poor human performance in lateralizing olfactory stimuli with no trigeminal component (Frasnelli et al., 2010; Frasnelli et al., 2008; Kobal and Hummel, 1992; Moessnang et al., 2011; Porter et al., 2005; Radil and Wysocki, 1998; Sorokowski et al., 2019; Wysocki et al., 2003). Rodent studies suggest a potential role for the AON in odor object formation (Aqrabawi and Kim, 2018; Haberly, 2001), and human resting functional connectivity data support this hypothesis (Zhou et al., 2019a).
Human olfactory lateralization requires trigeminal activation
2014, NeuroImage
Citation Excerpt :
Frasnelli et al. published two studies showing that humans on average lack olfactory lateralization ability (Frasnelli et al., 2010), irrespective whether stimuli are actively sniffed or passively applied (Frasnelli et al., 2009). However, their data also indicate that some people are able to lateralize above chance (Frasnelli et al., 2010) and that an increased numbers of molecules enhances localization ability even for relatively selective olfactory stimuli, like phenyl ethyl alcohol (Frasnelli et al., 2011). Olfactory lateralization ability depends on trigeminal input (Kobal et al., 1989; Lundstrom et al., 2012) and mixed chemicals, activating both receptor types typically can be localized without problems (Frasnelli et al., 2010, 2011; Hummel et al., 2003; Kleemann et al., 2009; Schneider and Schmidt, 1967; von Békésy, 1964; Wysocki et al., 2003).
Rats are able to lateralize odors. This ability involves specialized neurons in the orbitofrontal cortex which are able to process the left, right and bilateral presentation of stimuli. However, it is not clear whether this function is preserved in humans. Humans are in general not able to differentiate whether a selective olfactory stimulant has been applied to the left or right nostril; however exceptions have been reported.
Following a screening of 152 individuals with an olfactory lateralization test, we identified 19 who could lateralize odors above chance level. 15 of these “lateralizers” underwent olfactory fMRI scanning in a block design and were compared to 15 controls matched for age and sex distribution. As a result, both groups showed comparable activation of olfactory eloquent brain areas. However, subjects with lateralization ability had a significantly enhanced activation of cerebral trigeminal processing areas (somatosensory cortex, intraparietal sulcus). In contrast to controls, lateralizers furthermore exhibited no suppression in the area of the trigeminal principal sensory nucleus. An exploratory study with an olfactory change detection paradigm furthermore showed that lateralizers oriented faster towards changes in the olfactory environment.
Taken together, our study suggests that the trigeminal system is activated to a higher degree by the odorous stimuli in the group of “lateralizers”. We conclude that humans are not able to lateralize odors based on the olfactory input alone, but vary in the degree to which the trigeminal system is recruited.
Response times and response accuracy for odor localization and identification
2013, Neuroscience
Citation Excerpt :
Participants were paid a small amount to participate. Odorous stimuli were delivered by an automated, computer-controlled pneumatic stimulator (Institute for Biomagnetism and Biosignalanalysis, University of Münster, Germany) which provides air pulses of well-defined duration and has been adapted for olfactory research, as previously described (Frasnelli et al., 2010). In short, the machine’s outlets were connected to odor chambers via a polyurethane tubing with 3.2 mm outer diameter and an inner diameter of 1.7 mm (Fre-thane 85, Freelin-wade, McMinnville, OR, USA).
Although significant progress has been made over the last decades, the chemical senses remain less well explored than vision or audition. One method to assess participants’ ability to identify or localize odors consists in the application of dichotomous stimuli (e.g., left- and right-sided stimulation). In this study we aimed to explore localization and identification mechanisms by investigating whether response times and response accuracy were correlated, with the aim of establishing the pertinence of response times as an additional measure for assessment of the olfactory function (1). We further examined an advantage of the right nostril which has been reported in several publications (2). We delivered two mixed olfactory/trigeminal odors (benzaldehyde and eucalyptol) to one nostril at a time in a pseudorandomized order to 23 normosmic participants; the other nostril received an odor-free air puff. In half of the trials we asked the participants to detect the stimulated nostril; in the other half, they indicated which odor they had received. We recorded response accuracy and response times.
Participants reached higher accuracy in odor identification than in localization, driven by benzaldehyde. For the stimulus eucalyptol exclusively, we observed that participants were faster to respond after stimulation of the right nostril than to the left nostril, in the localization task. Finally, response times were correlated with response accuracy in the identification task, but not in localization.
Our findings suggest that odor identification is easier than odor localization. In addition, we find further support for an advantage of the right nostril over the left nostril. Moreover, the measurement of reaction times may supplement other techniques of the assessment of odor identification.
Olfactory priming leads to faster sound localization
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Still, previous studies using similar paradigms to ours successfully demonstrated effects of side congruency of the cues [29,39]. It may, however, seem surprising that we did not observe any effect of side congruency even for the somatosensory cues, even if the subjects were able to localize these somatosensory stimuli as shown previously [19]. This is in contrast to previous findings of enhanced performances in detection of visual or auditory targets after the presentation of tactile cues [9,20].
Cross-modal interactions between vision, audition and touch have been extensively studied in the last decade. However, our understanding of how the chemical senses interact with other sensory modalities remains relatively scarce. We performed a cued auditory localization paradigm in healthy young adults by measuring reaction times to monaural auditory stimuli after subjects had been cued by unilateral olfactory stimuli, mixed olfactory/trigeminal stimuli or somatosensory stimuli. As expected, all cuing conditions led to enhanced performances in auditory localization. Further, both odors led to significantly shorter reaction times when compared to the somatosensory stimuli. We did not observe any effect of side-congruency between the cues and the targets. These results suggest facilitative effects of odorous cues independent of a possible trigeminal component in the interaction between olfaction and audition.
Hyposmia in COVID-19: Temporal Recovery of Smell: A Preliminary Study
2023, Medicina (Lithuania)

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Localisation of unilateral nasal stimuli across sensory systems

Abstract

Brain Res. Rev.

Neuropsychologia

Neuropsychologia

Neuropsychologia

Physiol. Behav.

Neuropsychologia

Neurosci. Lett.

Neuroscience

Toxicol. Lett.

Pain

Brain Res.

Brain Cogn.

Physiol. Behav.

Brain Res. Cogn. Brain Res.

Physiol. Behav.

Electroencephalogr. Clin. Neurophysiol.

Physiol. Behav.

Physiol. Behav.

Neurobiol. Aging

Characterization of the mouse cold-menthol receptor TRPM8 and vanilloid receptor type-1 VR1 using a fluorometric imaging plate reader (FLIPR) assay

Br. J. Pharmacol.

Cerebral activation to intranasal chemosensory trigeminal stimulation

Chem. Senses

On the trigeminal percept of androstenone and its implications on the rate of specific anosmia

J. Neurobiol.

Olfactory sensitivity: reliability, generality, and association with aging

J. Exp. Psychol.

Interaction between chemoreceptive modalities of odour and irritation

Nature