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Fig.19.1a,bThedualolfactorysystem.(ReproducedwithkindpermissionofNaturePublishingGroupfromShepherdG.Smellimagesand
theflavoursysteminthehumanbrain.Nature2006;444:316–321.)
aBrainsystemsinvolvedinsmellperceptionduringorthonasalolfaction(sniffingin).
bBrain systemsinvolvedinsmellperceptionduringretronasalolfaction(breathingout),withfoodin the oral cavity. Airflows indicatedby
dashedanddottedlines;dottedlinesindicateaircarryingodormolecules.
ACC,accumbens;AM,amygdala;AVI,anterior ventral insular cortex;DI, dorsalinsular cortex;LH, lateralhypothalamus;LOFC,lateral
orbitofrontal cortex;MOFC,medialorbitofrontal cortex; NST, nucleus of the solitarytract; OB,olfactorybulb;OC, olfactory cortex;OE,
olfactory epithelium;PPC,posterior parietal cortex;SOM,somatosensory cortex;V,VII,IX,X,cranial nerves; VC,primaryvisualcortex;
VPM,ventralposteromedialthalamicnucleus.
InteractionBetweenOlfactory–GustatoryandGustatory–OlfactorySystems
Almosttwodecadesagoinmonkeys,single-cellrecordingtechniquesidentifiedsinglecellsresponding
tobothtasteandsmellinthe orbitofrontalcortex,
14
as wellas intheinsula/operculum.
15
Interestingly,
thesebimodalcellsintheorbitofrontalcortexofthemacaquewereselectiveforcongruentstimuli:For
example,acellrespondingoptimallytoasweettastesuchasglucosealsorespondedoptimallytosweet-
likeodorsratherthantoodorsrelatedtosaltyfood.Alsoinprimates,bimodalcellshavebeenidentified
thatreacttobothgustatoryandvisualstimuli.Assuchtechniquesarenotapplicableinhumans,ittookthe
implementation of functional imaging techniques to gain further insight into multimodal processing in
humans.Initialfunctionalimagingworkfocusedontheidentificationofprimaryandsecondaryolfactory
and gustatory cortices. The piriform cortex and medial orbitofrontal cortex,
16
caudal orbitofrontal
cortex,
17
andtheanteriorinsula/frontaloperculum
18
havebeen identified.In allthesestudies,however,
the brain’s reaction to isolated olfactory or gustatory stimuli was recorded. Using positron emission
tomography, Small etal
19
were the firsttoexaminethe brain’s reaction to simultaneous olfactory and
gustatorystimuli.Theywereabletoshowthattheevokedcerebralbloodflowinprimarygustatoryand
secondary gustatoryandolfactory corticesdecreased during simultaneouspresentationofolfactoryand
gustatory stimuli compared with independent presentation of these stimuli alone. This decrease in
responsewaslaterinterpretedtoreflectcompetitionbetweenthetasteandsmellsystems,arisingfromthe
fact thatthe odors were delivered orthonasally byasking subjects to sniff, ratherthan retronasally, as
wouldnaturallyoccurduringbimodaltasteandodorstimulationduringeatingordrinking.
8
Inthisstudy,
olfactoryorgustatorystimuliwerenotonlyapplied“alone”butalso ina“matched”and“mismatched”
flavorcondition(forexample,sourtasteandgrapefruitsmellasamatchedcondition;sweettasteandsoy
sauceodorantas a “mismatched”condition).In the“mismatched” condition,an increaseinbloodflow
wasobservedintheleftamygdaloidregionandintheleftandrightbasalforebrain.Theseresultshave
beeninterpretedasconfirmationofthefunctionoftheamygdalaandbasalforebraininprocessingnovel
orunpleasantstimuli.
19
Fig.19.2Magneticresonance imagelabeled toshoworthonasal andretronasalodorantstimulationvia tubeslocatedin thevestibulum nasi
(yellowodorantstimulation)andatthechoana(blueodorantstimulation).
ThisstudywasfollowedbyothersusingfMRItechniques.Cerf-Ducasteletal
20
testedtheinteraction
ofgustatoryandlingualsomatosensoryperceptionatacorticallevelinhumans.Stimulatingsubjectswith
eitherpuregustatorystimuliorstimulicontainingbothgustatoryandsomatosensoryqualities,theywere
able to demonstrate that gustatory and somatosensory lingual representation fields overlap hugely, as
similarcorticalareas(namelytheinsula,theRolandicoperculum[baseofthepre-andpost-centralgyri],
thefrontaloperculum,andthetemporaloperculum)wereactivatedbybothkindsofstimuli.Moreover,in
2001, Cerf-Ducastel and Murphy
21
applied aqueous solutions of odorant intraorally, thus mimicking
retronasal odorant perception. The observed activation pattern included all the brain regions usually
activated when odorants were applied orthonasally, such as the piriform and orbitofrontal cortex, the
hippocampalregion,theamygdala,theinsularlobe,thecingulategyrus,andthecerebellum.Inthisstudy,
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however,nocomparisonwith orthonasallyapplied odorantswasmade. Aregioninthelateral anterior
part of the orbitofrontal cortex was identified in2003 by de Araujo et al as the region activated by
combinedolfactoryandtaste stimuli, but notbyunimodal stimuli alone.
22
Odorants inthis studywere
deliveredinaqueousform,againtomimicretronasalstimulationincombinationwithtastestimuli,justas
they were in another study by Small et al in 2004.
23
Using familiar/congruent taste odor pairs and
unfamiliar/incongruent taste odor pairs, as well as unimodal stimuli, the authors were able to show
superadditive responses in the anterior cingulate cortex, the insula, the orbitofrontal cortex, and the
posterior parietal cortex following stimulation with the congruent pair compared with unimodal
stimulationalone.
In summary,theseinitial studiesusingintraorallyapplied aqueousstimuliincombination withtaste
stimuli toexamineflavor perceptionwere able toidentify theorbitofrontal cortex, the insula, and the
cingulatecortexasthemainareaswhereodorantsandtastantsintegrate.Moreover,itbecameobviousthat
theexperimentalset-up(namelytherouteofdeliveryofthestimuli)wasofgreatrelevance.
The form ofstimulation usedinthese studies(namely,theapplicationofodorantsinaqueousform),
however,is notalwayscomparable with foodconsumption and flavorperceptioninoureverydaylife.
Smalletal
9
thereforeconductedastudyexaminingbrainactivationinresponsetoidenticalorthonasaland
retronasal stimuli applied ingaseous form with anolfactometer.As shownin Fig. 19.2, stimuli were
applied twice, orthonasally and then retronasally. Using a food odor (chocolate) and other, nonfood
odors,Smalletalwereabletoshowthatbrainactivationdiffereddependingontherouteofdeliveryof
the food odor but not of the nonfood odors.
9
These findings prove that food odorants perceived
retronasally—which happensduring foodintake normally—areprocessed indifferent centralnetworks
from nonfood odors perceived retronasally. In combinationwithgustatorystimuli, retronasal olfactory
stimulation,butnotorthonasalolfactorystimulation,hasbeenshowntoaccelerateswallowingactivity.
24
ThisisnotsurprisingconsideringthatretronasalolfactorystimulationactivatesaregionoftheRolandic
operculumatthebaseofthecentralsulcus,
9
andthatthisareacorrespondstoaprimaryrepresentationof
the oral cavity.
25
Looking at interactions theother wayaround, Bultet al
26
were able to show that a
simultaneous odor stimulus was able to influence perceived oral texture (in this case, thickness and
creaminess)offood,butonlywhenitwaspresentedretronasally.Theeffectwasmostpronouncedwhen
odorpresentationcoincidedwithswallowing.
Simultaneous odor perception (if theodorants are perceptuallysimilar) can enhance the perceived
intensityoftastants;however,blockingthenoseseverelydiminishesthiseffect.
27
Thisphenomenonwas
shown by Sakai et al, who were able to demonstrate taste enhancement caused by simultaneously
presentedodorsand,moreover,confirmthattheeffectobservedwasreallyduetosimultaneousolfactory
perceptionandnottotastestimulation.
28
Ithasalsobeenshownthatthepurepresenceofanoralstimulus
increasesodorintensity,irrespectiveofwhethertheodorantisperceivedorthonasallyorretronasally.
29
Inapsychologicalexperiment,Daltonetalwereabletodemonstratethatsubthresholdconcentrationsof
olfactoryandgustatorystimuliintegrate.
30
However,thereismorerecentevidencethattastestimulation influences odor intensity perception
31
and is important for localizing retronasally sensed odorants to the oral cavity.
32
Interestingly, the
localizationeffectoccursonlyforcongruenttaste-odorpairs.Asweetbutnotsaltytastesensationcauses
subjectstoreportavanillaodorappearingtocomefromthemouth,whereasasaltybutnotsweettaste
sensationproducestheappearanceofasoysauceodor.
Insummary,allthesedataconfirmthat(1)odorantsareprocesseddifferentlywhentheyareperceived
orthonasallyversusretronasally;and(2)theyinteractandinfluencetasteperceptiondifferently.
ClinicalImplications
So far,there has been a limitednumber of studies explicitly examining patients with isolatedlesions.
However,aspreviouslymentioned,ithasbeenshownthatinpatientswithmainlyorthonasalmechanical
obstructions, such as polyps or chronic rhinosinusitis, retronasal olfactory perception is better than
orthonasal olfactory perception.
11
However,it has also beenshownthat incases ofolfactoryloss for
otherreasons,retronasalolfactoryperceptioncanremain,atleastpartly.
12
Incasesofreducedorthonasal
airflow(e.g.,post-laryngectomypatients),retronasalolfactionisreducedaswell.
33
Theexactunderlying
patho-physiologythatmightexplainwhyorthonasalandretronasalolfactoryperceptiondifferiscurrently
unknown.
Therearealsostudiesexaminingtheeffectofgustatorystimulationonolfactoryperception.Inastudy
byWelge-Luessenetal,itwasshownthatcongruentpairedstimuli,suchasasweettastantincombination
withasweetodorant,modulateOERPsoftheodorantandenlargethem,whileaconcomitantsourtastant
enlarges the event-related potentials (ERPs) of simultaneously applied gaseous carbon dioxide.
34
Olfactorystimulation,however,wasonly performed inanorthonasal way. Applying odorants notonly
orthonasally but also retronasally, it has been shown that food-like retronasally applied odors are
processed significantly faster, resulting in shorter OERP latencies, in congruent odor–taste situations
(food-likeodorvanillin,plussweettaste)thaninincongruentsmell–tastecombinations(food-likeodor
vanillin, plus sour taste). Incongruent simultaneous gustatory stimulation applied during orthonasal
olfactionseemedtoinduceconflictpriming,alsoresultinginfasterprocessing.
35
To examinetheinfluenceofthe vagalnerveongustatoryandolfactoryprocessing,asmall groupof
patientswithvagalnervestimulators(VNSs)wasexamined.Ithaslongbeensuggestedthatinterruption
ofalaryngeal–vagalfeedbackmechanism
36
mightcontributetoolfactorydysfunctionafterlaryngectomy,
37
whichmightbeconsideredtobeconsistentwithfindingsfromtheearly1980s.
38
Ontheotherhand,ithas
also been shownthatpartofthehyposmiainpost-laryngectomy patientsisduetoreducedairflow.
39,40
Examiningolfactoryfunctioninsubjectswithvagalstimulators,itwasshownthatvagalnervestimulation
prolonged P2 latencies of OERPs. In patients receiving a therapeutic benefit from VNSs in terms of
seizurecontrol,largeramplitudes duringthe“on”periodthanduringthe“off”periodwereobserved.
41
Even thoughthe number of studies examining vagal–olfactoryinteractionis limited,there seems tobe
growingevidencethatvagal–olfactory interaction doesoccur.It hasalsobeenshownthat patientswith
olfactorydisordersexhibithighergustatorythresholds.
42
Visual–OlfactoryandFlavorInteractions
Asdiscussedintheintroduction,visualinputsinfluenceolfactoryand,inparticular,flavorperceptions.In
astudybyDuBoseetalin1980,participantsoftenmisidentifiedflavorsofdrinkbecausetheiranswers
weremisledbyinappropriatecoloringofthetesteddrink,providingevidencethatvisualcuesinfluence
flavorperception.
43
Consistentwiththisresultisthefactthatwhitewine thathasbeencoloredredhas
beendescribed asfeaturingtypical “red winecharacteristics” bystudentsinanexperimental set-upin
2001.
44
Anatomicallypossiblesitesofintegrationaretheorbitofrontalcortex,
14
thehippocampus,
45
orthe
intraparietalsulcusandthesuperiortemporalsulcus.
46
Eventhough the latterare knowntobe regions
processingmultimodalinteractions,directinputsfromolfactoryregionssuchasthepiriformcortexhave
notyetbeenidentified.Indirectolfactoryprojectionsviatheamygdalaororbitofrontalcortexmightserve
asarouteofinformationtransfertotheseregions.UsingfMRIandcombininganolfactorydetectiontask
with visual presentation, Gottfried and Dolan were the first to show olfactory–visual integration in
humans.
47
Olfactory detection was accelerated when odorants were presented in the context of
semantically congruent visual cues (congruent odor–picture pairs) compared with incongruent
combinations.Enhancedactivitywasobservedintheanteriorhippocampusandtheorbitofrontalcortex,
Данная книга находится в списке для перевода на русский язык сайта https://meduniver.com/
provingtheirparticipationinthecrossmodalfacilitationofolfactoryandvisualperception.Besidespure
visualperception,subjects’beliefalsointeractswitholfactoryandflavorperception.Ifsubjectsbelieve
thatdifferentcolorsare associatedwith different flavors,subjectsare morelikelytojudgeaflavoras
different even if the offered samples differ only in color and not in flavor.
48
Further evidence that
“believing” modulatesolfactory perceptioncomes from aninterestingexperimentbydeAraujoetal in
2005.
49
Subjectshadtoratethevalenceofeithercleanairor oneodor,which,however,waslabeled
once as “cheddar cheese” and once as “body odor.” Using fMRI, it could be shown that the rostral
anterior cingulate cortex, the medial orbitofrontal cortex, and the amygdala were significantly more
activated when the odor was labeled “cheddar cheese” than when it was labeled “body odor.”Even
labeling the clean air “cheddar cheese” showed more activation in the cingulate cortex and the
orbitofrontalcortexthanlabelingit“bodyodor.”Thesedatashowthatpuresemanticandcognitiveinputs
modulatesensoryperceptionandprocessing.
ClinicalImplications
To date,thereis alimited number ofstudies examining smallnumbers ofpatientswith reducedvisual
function(mainlycompletelyblindpeople).Someofthesebehavioralstudieshaveyieldedcontradictory
results. While some studies did not show any difference between odor detection thresholds in blind
subjectscomparedwith sightedpeople,
50,51
others,usingolfactory identification tasks, didshowbetter
resultsinblindsubjects.
52–54
Rombauxetalwereabletoshowincreasedolfactorybulb(OB)volumein
blind subjects compared with sighted controls as well as increased olfactory function in the blind
subjects.
55
Olfactory–TrigeminalandTrigeminal–OlfactoryInteraction
Insidethenose,olfactoryreceptorneuronsandtrigeminalnervesarenotonlylocatedveryclosetoeach
other,butalsooftenstimulatedsimultaneously.Severalodorantsareknownnotonlytobeso-calledpure
olfactory odorants, but also to contain characteristics enabling them to elicit simultaneous trigeminal
stimulation.Mostodorants,ifappliedinhigherconcentrations,haveolfactoryandtrigeminalproperties.
Itisthereforenotsurprisingthatinteractionshavebeenpostulatedtooccurperipherallyatthelevelofthe
olfactoryepithelium,aswellascentrally.Inmammals,ithasbeenshown thattrigeminalganglioncells
with sensory endingsinthe respiratoryepitheliumalso get input from the OBor the spinaltrigeminal
complex.
56
Experimental approaches toselectivelyinduce temporaryanosmia or trigeminal anesthesia
intranasallyhavebeenperformed,
57
buthavenotbeenreproducedtostudyinteractionsbetweenthetwo
systems, as selective temporary elimination of only one system intranasally is almost impossible to
achieve.
Eliciting chemosensory ERPs (CSERPs) with increasing concentrations of intranasally applied
nicotine,Hummeletal
58
wereabletoshowthat,withincreasingconcentration,theperceivedqualityof
nicotinechangedfromanolfactoryperceptiontoastinging sensation,suggestingtrigeminalstimulation.
At the highest concentration, the trigeminal system seemed to “suppress” the olfactory perception.
Moreover,thepatternoftherecordedCSERPschangedtoa“trigeminalpattern,”meaningthatthelargest
amplitudeusingthehigherconcentrationwasobservedatCzposition,while,atolfactoryconcentrations,
the largest amplitude was observed at Pz.
58
This confirmed former data.
59
Ona psychophysical level
usingabehavioralparadigm,thesuppressionofolfactoryperceptioncausedbyasimultaneoustrigeminal
stimulushadbeenpreviouslyshown.
60
UsingfMRI,centralregionsofinteractionhavebeenidentifiedand
it has been shown that the combination of both trigeminal and olfactory stimuli elicit higher cortical
activationthanthesumofeachpart.
61
ClinicalImplications
Ithasbeenshownthatthetrigeminalsensitivityinpatientswithanosmiaisreduced.
62,63
Interestingly,only
intranasaltrigeminalthresholdchanges,whilecutaneoustrigeminalthresholdseemsnottobeinfluenced
by the loss of olfactory function. Moreover, the etiology of the olfactory loss (post-traumatic versus
postinfectious), as well as the degree of the olfactory disturbance, seems to have an influence on
trigeminal threshold: In patients with anosmia there seems to be no difference intrigeminal threshold
betweenpost-traumaticandpostinfectiousolfactorydisorders;inpatientswithhyposmia,however,those
withpost-traumaticdisordershadhighertrigeminalthresholdsthanthosewithpostinfectiousdisorders.
64
Aswellastheetiologyoftheolfactorydisorder,ageandolfactorystatusaffecttrigeminalsensitivity.
65
Recording electrophysiological responses from the intranasal mucosa and ERPs in subjects with
congenital anomia
66
and acquired anosmia,
67
Frasnelli et al were able to reveal different interaction
levels,bothperipherallyandcentrally,comparedwithhealthycontrols. Anegativecorrelationbetween
threshold,discrimination,and identificationscoreand thecomponents oftheCSERPtypicallyoccurred
aftertrigeminalstimulationhasalsobeenshown.
68
Olfactory–trigeminalinteractioncanalsobeobserved
in patients suffering from reduced trigeminal sensitivity, a rare, but sometimes observed, entity. In a
patient with unilateral loss of trigeminal sensitivity due to a meningioma, olfactory threshold was
severelyelevatedonthe affected side,
69
just as it was in patients following ballooncompression for
casesoftrigeminalneuralgia.
70
Fig.19.3Thedifferentsensorymodalities(smell,taste,vision,hearing,somatosensory)that,togetherwiththeinformationprovidedfromthe
gut,contributetoflavorperception.Moreover,differentbrainsystemsparticipatinginfoodintakeregulationandevaluationanditsinteraction
aredepicted.(ModifiedwithkindpermissionofNaturePublishingGroupfromShepherdG.Smellimagesandtheflavoursysteminthehuman
Данная книга находится в списке для перевода на русский язык сайта https://meduniver.com/
brain.Nature2006;444:316–321.)
In summary, in patients with olfactory deficits, trigeminal thresholds are elevated. It is especially
importanttokeepthisinmindinmedicolegalcasesinordernottomisinterpretsuchresultsassignsof
malingering.
Conclusions
Thereisgrowingevidencethattheolfactory,gustatory,andtrigeminalsystemsinteract.Flavorperception
can also be influenced by visual inputs and beliefs and expectations (Fig. 19.3).
71
This is of great
importance for the clinician examining patients withlesions previouslyconsidered “isolated,” as this
knowledgehelpstobetterunderstanddeficitsandimpairmentsreportedbypatients.Untilnow,manyof
these complaints have not been taken seriously or even considered possible, as the underlying
pathophysiologyhasnotyetbeenidentified.
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Index
Pagenumbersinboldrefertomaterialintablesandpagenumbersinitalicsrefertomaterialinfigures.
A
Aachen“rhinotest”63
acupuncture100
adaptation36
adenosinemonophosphate,cyclic22,26,46
adrenergicfibers18
afferentconnectionsgustatorycortex,primates158–159
parvicellularpartofventralposteromedialnucleus157–158
age-relatedloss(older/elderlypersons)
nasaltrigeminalsystemfunction143–144
smell1,3–4,102
taste1,4–5
ageusia180
definition1,68,180
airconditioning,nasal10–11
airpassages,nasal10
airborneparticles,nasal
responseto144
airwaysseerespiratorytract
Alcohol-Sniff-Test59
children121
allergy,nasal(allergicrhinitis)81–83
trigeminalsystemand143–144,145
alliesthesia119
negative119
Alzheimerdementia132,183
ambientodorants,impacton
behaviorandhealth6
AMP,cyclic22,26,46
amygdala33–34
gustationand160,165
olfactionand27,33–34
anatomy(functional)
gustatorysystemseegustatorysystem
olfactorysystemseeolfactorysystem
trigeminalsystem138–139
aneurysm,anteriorcerebralartery201
anosmia141,216–217
casestudy216–217
congenitalseecongenitalolfactorydisorders
definition1
expertopinion209,210,211,216–217
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