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  Effects of chewing on cognitive processing speed Yoshiyuki Hirano a,b, ⇑ , Takayuki Obata a,b,c , Hidehiko Takahashi c , Atsumichi Tachibana d , Daigo Kuroiwa a ,Toru Takahashi e , Hiroo Ikehira c , Minoru Onozuka d a Research Program for Carbon Ion Therapy and Diagnostic Imaging Research, Center for Charged Particle Therapy, National Institute of Radiological Sciences, 4-9-1 Anagawa,Inage-ku, Chiba 263-8555, Japan b Research Center for Child Mental Development, Chiba University Graduate School of Medicine, 1-8-1 Inohana, Chuo-ku, Chiba 260-8670, Japan c Department of Molecular Neuroimaging, Molecular Imaging Center, National Institute of Radiological Sciences, 4-9-1 Anagawa, Inage-ku, Chiba 263-8555, Japan d Department of Physiology and Neuroscience, Kanagawa Dental College, 82 Inaoka-cho, Yokosuka 238-8580, Japan e Graduate School of Human Environment Science, Fukuoka Women’s University, 1-1-1 Kasumigaoka, Higashi-ku, Fukuoka 813-8529, Japan a r t i c l e i n f o  Article history: Available online 29 January 2013 Keywords: ChewingAttentionAttentional networksAlertingExecutive functionFunctional MRI a b s t r a c t In recent years, chewing has been discussed as producing effects of maintaining and sustaining cognitiveperformance. We have reported that chewing may improve or recover the process of working memory;however, the mechanisms underlying these phenomena are still to be elucidated. We investigated theeffect of chewing on aspects of attention and cognitive processing speed, testing the hypothesis that thiseffect induces higher cognitive performance. Seventeen healthy adults (20–34years old) were studiedduring attention task with blood oxygenation level-dependent functional (fMRI) at 3.0 T MRI. The atten-tionalnetworktest(ANT)withinasingletaskfMRIcontainingtwocueconditions(nocueandcentercue)andtwotarget conditions (congruent andincongruent) was conductedtoexaminetheefficiencyof alert-ing and executive control. Participants were instructed to press a button with the right or left thumbaccording to the direction of a centrally presented arrow. Each participant underwent two back-to-backANTsessionswithorwithoutchewinggum, odorlessandtastelesstoremoveanyeffectotherthanchew-ing. Behavioral results showed that mean reaction time was significantly decreased during chewing con-dition, regardless of speed-accuracy trade-off, although there were no significant changes in behavioraleffects (both alerting and conflict effects). On the other hand, fMRI analysis revealed higher activationsin the anterior cingulate cortex and left frontal gyrus for the executive network and motor-relatedregions for both attentional networks during chewing condition. These results suggested that chewinginduced an increase in the arousal level and alertness in addition to an effect on motor control and, asa consequence, these effects could lead to improvements in cognitive performance.Published by Elsevier Inc. 1. Introduction Recently, behavioral studies were performed to examine therelationship between chewing and cognitive performance includ-ing memory, attention and executive function. With regard tomemory,ithasbeenreportedthatgumchewingimprovesepisodicand working memory during chewing, suggesting at least in partthat chewing promotes regional cerebral blood flow and glucosedelivery (Stephens & Tunney, 2004; Wilkinson, Scholey, &Wesnes,2002; Zoladz & Raudenbush, 2005). However, the existence of enhancedperformanceofepisodicmemorytaskbycontext-depen-dent effects induced by chewing has remained controversial (Ba-ker, Bezance, Zellaby, & Aggleton, 2004; Johnson & Miles, 2007,2008; Stephens & Tunney, 2004). As for attention, it was reportedthat sustained attention (Smith, 2009a, 2010; Tucha, Mecklinger,Maier, Hammerl, & Lange, 2004) and language-based attention(Stephens & Tunney, 2004) were improved by chewing. On theotherhand,Tuchaetal.(2004)claimednotonlythatmemoryfunc-tions were not improved but also that tonic and phasic alertnesswere adversely affected by chewing. With respect to executivefunction, a study claimed that chewing gum does not appear tobe of benefit to word association executive function (Stephens &Tunney,2004), butanotherstudyreportedabeneficialeffect(Ony-per, Carr, Farrar, & Floyd, 2011).To elucidate these inconsistent results and their mechanisms,several functional neuroimaging studies have been conducted.These studies suggested that chewing facilitated the process of working memory and also that it was related to attention 0278-2626/$ - see front matter Published by Elsevier Inc. ⇑ Corresponding author at: Research Program for Carbon Ion Therapy andDiagnostic Imaging Research, Center for Charged Particle Therapy, NationalInstitute of Radiological Sciences, 4-9-1 Anagawa, Inage-ku, Chiba 263-8555, Japan.Fax: +81 43 206 3487. E-mail addresses: (Y. Hirano), (T. Obata), (H. Takahashi), (A. Tachibana), (D. Kuroiwa), (T. Takahashi), ikehira@nirs. (H. Ikehira), (M. Onozuka). Brain and Cognition 81 (2013) 376–381 Contents lists available at SciVerse ScienceDirect Brain and Cognition journal homepage:  (Hiranoetal.,2008;Wang,Gitelman,&Parrish,2009).Aswell,sev-eral studies mentioned that chewing affects arousal (Onyper et al.,2011; Sakamoto, Nakata, & Kakigi, 2009; Smith, 2010; Stephens &Tunney,2004).Sakamotoetal.(2009)studiedtheeffectofchewing onthecentralnervoussystembymeasuringreactiontime(RT)andevent-relatedpotentials(ERPs).Theysuggestedthatchewinginflu-encesthestateofarousalviatheascendingreticularactivatingsys-tem, and that it accelerates cognitive processing.Based on these studies, we assumed that chewing also affectsaspects of attention and accelerates cognitive processing. Indeed,recent studies, pointing out that reaction times were shortenedby chewing in the categoric search task (Allen & Smith, 2012a;Smith, 2010), vigilance task (Allen & Smith, 2012a), language- based attention task (Stephens & Tunney, 2004), and the encodingof new information in the focused attention task (Smith, 2010).Smith (2010) speculated that positive cognitive performance maycomefromthefact thatsubjectsfeel morealertasdescribed, beingenergetic, quick-witted and attentive, all based on mood improve-ment. However, some studies reported not only that the perfor-mance of sustained attention was not accelerated (Kohler, Pavy,& Van den Heuvel, 2006; Smith, 2010; Tucha et al., 2010) but alsothatvigilancetaskwasdecelerated(Tuchaetal.,2010).Tuchaetal. (2010) indicated that the psychodynamics of gum chewing mightbe an important factor, and these conflicts of cognitive perfor-mance may originate from the duration of the study (Tuchaet al., 2010) and time of the task (Allen&Smith, 2012a, 2012b; Tu-cha & Simpson, 2011). Indeed, Tänzer, Von Fintel, and Eikermann(2009) reported that chewing benefit in concentration perfor-mance showed up after 14min from the initiation of the test. Toelucidate the mechanism of this issue, we considered that a func-tional magnetic resonance imaging (fMRI) assessment might behelpful. The attentional networktest (ANT) providedaway of test-ing for the efficiency of the alerting, orienting and executive (con-flict resolution) functions of attention (Fan, McCandliss, Sommer,Raz, & Posner, 2002), and it was adapted within a single sessionof event-relatedfMRI(Fan, McCandliss,Fossella, Flombaum,&Pos-ner, 2005). In the current study, we examined the effects of chew-ing on alerting and executive attention and their processing speedby comparing the behavioral and fMRI results of ANT. 2. Experimental procedures  2.1. Subjects Nineteen healthy volunteers (aged 20–34) were enrolled forassessment by random-effect analysis (Seghier, Lazeyras, Pegna,Annoni, & Khateb, 2008) in this study. Two participants were ex-cluded from the analysis due to motion (>0.56mm, correspondingto 15% of voxel size in-plane) during the fMRI scan. Therefore, datafrom 17 healthy volunteers (mean age±SD, 25.2±4.79years;range, 20–34years; 8 females) were evaluated in this study. Writ-ten informed consent was obtained from all subjects. The subjectsbrieflypracticedANToutside, andtheninside the MRI scanner justbefore the fMRI scan. Experiments were performed according totheethicalguidelinesapprovedbytheEthicsCommitteeoftheNa-tional Institute of Radiological Sciences.  2.2. Task paradigm ANT was adjusted by adding the gum chewing session whilekeeping the total scan time comparable to the srcinal ANT forthe fMRI study of the previous report (Fan et al., 2005) to avoid areduction in the level of attention. For that reason, we used twocue conditions (no cue and center cue) instead of the three cueconditions (no cue, center cue and special cue) used in their study.As in their study, however, we also used the two target conditions(congruent and incongruent). The cue durations and stimulusintervals were also reduced from 300–11800ms (mean, 2800ms)to 300–6800ms (mean, 1800ms) and from 3000–15000ms(mean, 6000ms) to 3000–8000ms (mean, 5000ms), respectively.Fig. 1 shows the gum chewing and the following ANT, which wasusedforourfMRIstudy,consistingofa10-minsessionduringeachchewing and control condition. Cues consisted of a crosshair ineither bold or the same thickness as the fixation crosshair coloredin black against a gray background. Targets consisted of a row of five arrows with arrowheads pointing leftward or rightward eitheraboveorbelowthefixationcrosshair.Conflictresolutionwasintro-ducedbyincongruentorcongruentstimuli,whichshowedthatthecentral arrow was either flanked or not. Subjects chewed gum for10s at their normal speed (  1Hz) according to instructions onthe screen every six cue-target trials during chewing condition.The existence of cue before showing target activates the alertingsystem, and flankers adjacent to a target activate executive controlof attention (Fan et al., 2002). Then, during control condition, sub- jects were instructed not to chewgum. We used moderately hard-type gum (5.6  10 3 Pa  s; Lotte Co., Ltd., Tokyo, Japan) withoutodor or taste components to remove any effects other than masti-cation.ANTs wereconductedandsynchronizedwiththeMRI scan-ner by using E-Prime software (Psychology Software Tools, Inc.,Sharpsburg, PA, USA). Each subject underwent the adapted ANTcontinuously, with or without chewing gum, in two back-to-backsessions, which were interspersed by a 10-min rest period, duringwhich T1 anatomical images were acquired. The order of condi-tions was randomized among individuals (eight subjects startedwith chewing) and a 10-min waiting period, during which T1 ana-tomical images were acquired, was inserted between the two con-ditions.Subjectswereinstructedtopressabuttonwiththerightorleft thumbaccordingto the directionof the centrallypresented ar-row. Each of the button presses and RTs were also recorded. Thefollowing operational definitions of the efficiencies of the atten-tional networks were used to compare the performance betweenconditions. Alerting effect  ¼  RT  ð no cue Þ   RT  ð center cue Þ Conflict effect  ¼  RT  ð incongruent Þ   RT  ð congruent Þ RTandaccuracyforeachconditionweresubjectedtothree-wayrepeated analysis of variance (ANOVA) followed by Tukey’s posthoc test. Behavioral effects (alerting and conflict effect) and meanRTfor eachchewingconditionweresubjectedto two-wayANOVA.Estimates of effect size were reported for all ANOVAs (partial eta-squared, h2). Correlation coefficients were calculated between thebehavioral effects and RT. All statistical analyses were calculatedusing SPSS (IBM, Chicago, IL, USA).  2.3. Image acquisition and data analysis fMRI experiments were performed using gradient-echo echo-planar imaging (TE=30ms, TR=2s, field of view=24cm, slicethickness=3.8mm, gap=0.2mm, image matrix=64  64, num-ber of slices=30, flip angle=90  ). After two fMRI scans, T1-weighted anatomical MR images (sequence=3D fast SPGR,TE=1.4ms, TI=450ms, TR=6.5ms, field of view 25.6cm  25.6cm, slice thickness=1mm, image matrix=256  256, num-ber of slices=196, flip angle=12  , number of acquisitions=1)were acquired to help spatial image normalization. Data were ac-quiredbyGESignaExcite3.0TMRI equippedwith8-chphasedar-ray coil (GE, Waukesha, WI, USA). fMRI data were analyzed bySPM5 (Wellcome Trust Centre for Neuroimaging, University Col-lege London, London, UK). Data from the first five volumes werediscarded to avoid transient magnetization. Correction for head Y. Hirano et al./Brain and Cognition 81 (2013) 376–381  377  motion was performed. Each of three hundred successive func-tional images obtained from each subject were normalized to theMNI template (Collins, Neelin, Peters, & Evans, 1994) and spatiallysmoothedby 8-mmGaussiankernel. Statistical analysis bygenerallinearmodelapproach(Fristonetal.,1995)wasperformedonlyfordata in parts of ANT to avoid influence of head motion by gumchewing. Global changes in BOLDsignals were removed using pro-portional scaling. After preprocessing, activated areas associatedwith alerting were isolated by subtracting a no cue condition froma cue condition for first-level individual analysis. Next, activatedareasassociatedwithconflictresolutionwereisolatedbysubtract-ing congruent condition from incongruent condition. Finally, ran-dom effects group analysis was performed on each chewingcondition to estimate activated areas that were consistent for thetotal group of subjects. 3. Results  3.1. Behavioral analysis Table 1 shows mean RT and accuracy for each condition. Three-wayrepeatedmeasuresANOVAofRTshowedthatthemaineffectsof chewing condition ( F  (1,16)=20.30,  p  <0.001, effect size=0.56),target condition ( F  (1,16)=97.29,  p  <0.001, effect size=0.86), andcue condition ( F  (1,16)=9.03,  p  <0.01, effect size=0.36) were sig-nificant. The interactions between chewing condition and targetcondition ( F  (1,16)=0.78, effect size=0.05), chewing conditionand cue condition ( F  (1,16)=0.12, effect size=0.01), target condi-tion and cue condition ( F  (1,16)=0.11, effect size=0.01), andamong all three conditions ( F  (1,16)=2.12, effect size=0.12), werenot significant. Three-way repeated measures ANOVA of accuracyshowed that the main effect of target condition ( F  (1,16)=11.39,  p  <0.005, effect size=0.42) was significant. The main effects of chewing condition ( F  (1,16)=0.16, effect size=0.01) and cue con-dition ( F  (1,16)=0.05, effect size=0.00) were not significant. Theinteractions between chewing condition and target condition( F  (1,16)=1.80, effect size=0.10), chewing condition and cue con-dition ( F  (1,16)=0.05, effect size=0.00), target condition and cuecondition ( F  (1,16)=0.14, effect size=0.00), and among all threeconditions ( F  (1,16)=0.11, effect size=0.01), were not significant.Table 2 shows the behavioral effects and mean RT for eachchewingconditionandthecorrelationcoefficientsbetweenbehav-ioral effects and mean RT. Two-way repeated measures ANOVAshowed that the main effect of chewing condition was not signifi-cant ( F  (1,16)=0.04, effect size=0.00), but that the behavioral ef-fect was significant ( F  (1,16)=6.03,  p  <0.05, effect size=0.27).The interaction between chewing condition and behavioral effectswas not significant ( F  (1,16)=0.89, effect size=0.05). Correlationcoefficients between alerting, conflict and mean RT were not sig-nificant ( r  2 >0.20,  n  =17,  p P 0.07).  3.2. Functional analysis The attention system is anatomically separated into multiplesubsystems from the data processing systems that perform  Table 1 Mean RT ± SD (ms) and accuracies ± SD for each condition. Control After chewingNo cue Center cue Mean No cue Center cue Mean Congruent  RT 545±93 520±91 533±88 510±66 475±60  493±61Accuracy 1.00±0.02 0.99±0.03 0.99±0.02 1.00±0.01 1.00±0.01 0.99±0.01 Incongruent  RT 603±89 569±73 585±75 562±78  543±62 551±66Accuracy 0.97±0.06 0.97±0.04 0.97±0.03 0.96±0.06 0.96±0.04 0.96±0.03MeanRT 573±88 545±81 559±80 535±70 511±59 523±62Accuracy 0.99±0.02 0.98±0.02 0.98±0.01 0.98±0.03 0.98±0.02 0.98±0.02  Significantly different between chewing conditions (  p  <0.05). TargetCueGum chewingCenter cueNo cueCongruentIncongruent 10000 ms300 - 6800 ms(Mean 1800 ms)< 2000 ms3000 - 8000 ms (Mean 5000 ms)200 ms2000 ms Repeat 6 timesRepeat 10 times Fig. 1.  Schematic depiction of adapted ANT in chewing condition. A fixation cross was constantly shown in the center of the screen. A center cue or no cue was shown for200ms randomly. Following a variable duration (300–6800ms), the center arrow as target and flankers of the left and right two arrows were shown until the subjectresponded with a button press, but for less than 2000ms. The target and their flankers disappeared immediately after the subject pressed the button, then the next cue wasshown after variable intervals (3000–8000ms) from the appearance of the target. ANT (Fan et al., 2005) was adapted for this study.378  Y. Hirano et al./Brain and Cognition 81 (2013) 376–381  operations on specific inputs (Posner & Petersen, 1990). In thisANT,alertingisdefinedasachievingandmaintaininganalertstate,and executive control is defined as resolving conflict among re-sponses (Fan et al., 2002). For the alerting network, only the leftpremotor cortex was more activated during chewing condition,while the right postcentral gyrus, anterior lobe of the cerebellumand left superior temporal gyrus were less activated (Fig. 2A andTable 3). On the other hand, for the executive network, while theanterior lobe of the cerebellum was less activated during chewingcondition,leftmiddleandsuperiorfrontalgyri,rightpremotorcor-tex, right precentral gyrus, right anterior and left posterior cingu-late gyri, left parietal operculum, left thalamus and left insulawere more activated (Fig. 2 and Table 4). 4. Discussion Atfirst, themaineffectsof ANTwereidentifiedinbothcuecon-dition(nocue and center cue) andtarget condition(congruent andincongruent) in this study (Table 1). The results indicate that ourversion of ANT was valid with even shorter testing time than thatin a past study, which we refer to as modified ANT for fMRI (Fanet al., 2005). Also, the behavioral effects (Table 2) and RT were roughly equivalent (alerting effect was 4% longer and mean RTwas 13% shorter) except for conflict effect (58% shorter) comparedwiththoseinanotherstudyof theirgroup(Ruedaet al., 2004) con-ducted for similar test length (  30min in total). Our resultsshowedthat (i) the attentionlevel wouldhavebeenkept relativelyhigher during ANT because the total number of test trials was 45%less, and (ii) subjects could relativelyeasily wait until the next tar-get was shown while still maintaining attention because the inter-val was 23% shorter, and especially the longest interval betweentarget andnext cue was 47%(7s) shorter comparedwiththestudyof  Fan et al. (2005).The most significant difference in behavioral results betweenchewing and control conditions was that RT was significantlyshorterduringchewingconditionregardlessofanyspeed-accuracytrade-off. Our results strongly supported previous studies report-ing that gum chewing shortened RT to a numerical working mem-orytask(Wilkinsonetal., 2002),asustainedalertness(Tuchaetal., 2004), an auditory oddball paradigm (Sakamoto et al., 2009), and semantic memory (Smith, 2010). Many reports suggested thatchewing activated the frontal cortex (Momose et al., 1997; Ono-zuka et al., 2003; Sesay, Tanaka, Ueno, Lecaroz, & De Beaufort,2000; Takada & Miyamoto, 2004; Takahashi, Miyamoto, Terao, &Yokoyama, 2007; Tamura, Kanayama, Yoshida, & Kawasaki,2003), which may cause improvement in alerting and executivefunctions assumed to be executed in that region (Fan et al.,2002). In addition, Takada and Miyamoto (2004) suggested that the fronto-parietal network during chewing contributed to highercognitive processing. More recently, Sakamoto et al. (2009) sug-gested that shortened RT resulted from shortened cognitive pro-cessing time caused by the central nervous system affected bychewing through its complex behavior such as jaw and tonguemovement,tactilesensationintheoralcavity,andsalivasecretion.Furthermore,Smith(2009b)reportedthatchewingincreasedalert-ness, suggesting improved test performance. Also, several reportshavesupportedthenotionthatchewingimprovedsustainedatten-tion (Smith, 2009a) and persistent cognitive performance (Hirano et al., 2008; Sakamoto et al., 2009). Thus, the effect of chewingon RT is considered to be related to alertness and attention. Fur-thermore, we noted that the chewing effect on cognitive perfor-mance is not sustained after cessation of chewing, based on thefact that our results were calculated from data during both chew-ing conditions, with the order of chewing condition randomizedand carried out with a 10-min interval in our study. This was con-sistent with the proposal of recent studies, that the time-limitednature of performance benefits can be attributed to mastication-induced arousal (Onyper et al., 2011), alertness (Allen & Smith, 2012a, 2012b), and mood (Smith, 2009a). These mechanisms are still being debated (Sakamoto et al., 2009; Smith, 2009b), andfurther investigations will be required to address these issues.Additionally, we consider that chewing might have a stress reduc-tioneffect.Ingeneral,theenvironmentintheMRIscannerissome-what stressful mainly due to the acoustic noise during scanningand the confined space. 3 T MRI scanners generate acoustic noiseof more than 110dB while running gradient-echo echo-planarimaging sequence (Price, De Wilde, Papadaki, Curran, & Kitney,2001). Participants might have experienced feelings of excitementand stress when being positioned in the MRI scanner. Therefore,the positive effects on mood by gum chewing might have reducedstress and affected the performance of the test. aciththpcipcisfgRL z = 40y = -40x = 4x = -8y = -12 mfgpmiaciacicer aciacisfgsfgpo B R z = 64y = -8y = -38 Lstgpmcer pcgpcg A Fig. 2.  Significantly different activated regions between chewing and controlconditions for the alerting network (A) and the executive network (B). Yellowvoxels show more activated regions during chewing condition than controlcondition. Red voxels show less activated regions during chewing condition thancontrol condition. The statistical threshold was set at  p  <0.01, uncorrected formultiplecomparisons.Theextentthresholdwassetatmorethan30voxels.  x ,  y ,and  z   in cross-sectional view indicate Talairach coordinates (Talairach & Tournoux,1988). Abbreviations: aci, anterior cingulate gyrus; cer, cerebellum; ci, cingulategyrus; i, insula; mfg, middle frontal gyrus; pci, posterior cingulate gyrus; pcg,postcentral gyrus; pm, premotor cortex; po, parietal operculum; sfg, superiorfrontal gyrus; stg, superior temporal gyrus; th, thalamus. (For interpretation of thereferences to color in this figure legend, the reader is referred to the web version of this article.)  Table 2 Behavioral effects and correlation coefficients for each chewing condition. Control After chewingEffect±SD (ms) Alerting Conflict Effect±SD (ms) Alerting ConflictAlerting 28±48 24±37Conflict 52±29   0.13 58±25   0.20Mean RT 559±80 0.16   0.45 523±62 0.29 0.22 Y. Hirano et al./Brain and Cognition 81 (2013) 376–381  379
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