记忆的行为指标

TMS Over the Right Precuneus Reduces the Bilateral FieldAdvantage in Visual Short Term Memory CapacityAntje Kraft a,b,*,Mads Dyrholm c,Stefanie Kehrer a,Christian Kaufmann d,Jovita Bruening a, Norbert Kathmann d,Claus Bundesen c,Kerstin Irlbacher a,1,Stephan A.Brandt a,1a Department of Neurology,CharitéUniversitätsmedizin Berlin,Berlin,Germanyb Berlin Institute of Health,CharitéUniversitätsmedizin Berlin,Berlin,Germanyc Center of Visual Cognition,Department of Psychology,University of Copenhagen,Copenhagen,Denmarkd Clinical Psychology,Department of Psychology,Humboldt-Universität zu Berlin,Berlin,Germanya r t i c l e i n f oArticle history:Received3April2014Received in revised form21October2014Accepted6November2014 Available online4December2014Keywords:Parietal cortexrTMSTVAVisual attentionVisual processing speedVSTM a b s t r a c tBackground:Several studies have demonstrated a bilateralfield advantage(BFA)in early visual attentional processing,that is,enhanced visual processing when stimuli are spread across both visual hemifields.The results are reminiscent of a hemispheric resource model of parallel visual attentional processing, suggesting more attentional resources on an early level of visual processing for bilateral displays[e.g. Sereno AB,Kosslyn SM.Discrimination within and between hemifields:a new constraint on theories of attention.Neuropsychologia1991;29(7):659e75.].Several studies have shown that the BFA extends beyond early stages of visual attentional processing,demonstrating that visual short term memory (VSTM)capacity is higher when stimuli are distributed bilaterally rather than unilaterally.Objective/hypothesis:Here we examine whether hemisphere-specific resources are also evident on later stages of visual attentional processing.Methods:Based on the Theory of Visual Attention(TVA)[Bundesen C.A theory of visual attention. Psychol Rev1990;97(4):523e47.]we used a whole report paradigm that allows investigating visual attention capacity variability in unilateral and bilateral displays during navigated repetitive transcranial magnetic stimulation(rTMS)of the precuneus region.Results:A robust BFA in VSTM storage capacity was apparent after rTMS over the left precuneus and in the control condition without rTMS.In contrast,the BFA diminished with rTMS over the right precuneus. Conclusion:Thisfinding indicates that the right precuneus plays a causal role in VSTM capacity,partic-ularly in bilateral visual displays.Ó2015Elsevier Inc.All rights reserved.IntroductionSeveral studies in visual attention research have examined the consequences of unilateral and bilateral presentation of relevant stimuli.A robust bilateralfield advantage has been demonstrated in distinct attentional tasks,such as target discrimination[1],covert attention on multiple stationary target stimuli[2],as well as attentional tracking tasks[3].Based on these behavioralfindings a hemispheric resource model has been developed that suggests independent attentional resources for the cortical hemispheres [1e7].If targets are presented in the right hemifield only,the contralateral left hemisphere is involved in attentional processing and if targets were presented in the left hemifield only the right hemisphere is involved in attentional processing.In contrast,if targets are presented across both hemifields both hemispheres are involved,thus resulting in higher attentional processing resources for bilateral compared to unilateral displays.It is important to note that this model accounts only for an early level of visual attentional processing.Early visual areas contain retinotopic representations of the contralateral hemifield within each hemisphere[8,9].Using fMRI(functional Magnetic Resonance Imaging)Kraft et al.(2011)[7]examined hemifield effects inFunding:This work was supported by the Deutsche Forschungsgemeinschaft (BR1691/3-3).*Corresponding author.Department of Neurology,CharitéUniversitätsmedizin Berlin,Charitéplatz1,10117Berlin,Germany.Tel.:þ49450560323;fax:þ49450 560955.E-mail address:antje.kraft@charite.de(A.Kraft).1These authors contributed equally to thiswork.Contents lists available at ScienceDirectBrain Stimulationjournal h omepage:w/10.1016/j.brs.2014.11.0041935-861X/Ó2015Elsevier Inc.All rights reserved.Brain Stimulation8(2015)216e223parallel attentional processing within the early visual areas V1to V4v.We found that the bilateral field advantage can be assigned,at least partly,to differences in distractor exclusion in parallel atten-tional processing within one hemi field rather than across opposing hemi fields.Distractor exclusion was greater if separated targets were aligned bilaterally,as measured by a lower BOLD (blood oxygenation level dependent)signal modulation at the distracting retinotopic position compared to the unilateral condition.It has been discussed for a long time how visual hemi fields are represented in parietal and frontal cortical areas involved in visual and visual attentional processing.Based on findings from neglect patients,Mesulam (1999)[10]suggested in his prominent model that the left hemisphere represents mainly the right visual field,while the right hemisphere represents both hemi fields.Some fMRI studies support this model also in healthy human test subjects [11,12],while other studies revealed evidence for a contralateral preference in both hemispheres similar to early visual areas [13e 15].Recently,a series of behavioral studies also documented a bilateral field advantage in visual short term memory (VSTM)and visual working memory capacity [16e 18].Kraft et al.(2013)[18]used Bundesen ’s theory of visual attention [19]to analyze whether attention capacity parameters covary with hemi field A can be interpreted as a mathematical formalization of the biased competition model of Desimone and Duncan (1995)[20]where objects compete for categorization.An object is then consciously perceived when encoded to VSTM which is limited by about four objects [21e 23].Analysis of a whole report task with the TVA procedure [24]allowed us to estimate distinct attentional parameters such as the temporal threshold of visual perception,visual processing speed,and VSTM capacity.The study revealed that both VSTM capacity and visual processing speed was higher when the whole report display was aligned across the hemi fields compared to within one-hemi field [18].Thus,it is discussed if hemispheric-speci fic resources are also evident on a later stage of attentional processing.On a neuro-anatomical level,the parietal cortex (posterior parietal cortex (PPC),precuneus and intraparietal sulcus)is suggested to be involved in VSTM [25e 29].Using fMRI,Todd and Marois (2004)[25]could show that activity in the PPC is precisely correlated with the amount of information stored in VSTM during a delayed visual matching to sample task.The neural implementation of the theory of visual attention (NTVA)developed by Bundesen and colleagues in 2005discussed the role of occipito-parietal areas (the precuneus)in higher visual attentional processing (see Bundesen et al.,2005[26]and Fig.2C).In summary the NTVA suggested that visual information is first processed in an unselective processing sweep from the lateral geniculate nucleus of the thalamus to the striate and extrastriate visual cortex.In visual cortex,individual perceptual values for each object are computed and multiplied by pertinence values.The information then enters the pulvinar of the thalamus.There,a saliency map is located where products are summed up as attentional weights.The weighted information is then processed from the pulvinar to higher level visual processing areas in the cortex (i.e.occipito-parietal areas/precuneus).The resulting perceptual values are multiplied by bias values,and the products are then transmitted from the cortex to the thalamic reticular nucleus.Here a VSTM map of locations is represented.Our current findings in healthy subjects using fMRI (see Fig.2C )support the suggestion that the precuneus is part of the NTVA network.Moreover,current results from patients with Alzheimer disease underline the role of the precuneus in TVA-based assessment of visual spatial attention [30].Besides hypo-metabolism in the lateral PPC which causes spatial attentional bias,patients in early Alz-heimer disease had also a reduced metabolism in the precuneus.Repetitive transcranial magnetic stimulation (rTMS)is a noninvasive secure method that allows one to test the functional role of cortical areas in cognitive processes in healthy humantestFigure 1.Experimental procedure.The timing of a single whole report trial (above)and one-hemi field (unilateral)and two-hemi field (bilateral)letter displays (below)are illus-trated.During the left and right rTMS blocks,trains of rTMS pulses at 6Hz for333ms are applied with the onset of the stimulus array.A.Kraft et al./Brain Stimulation 8(2015)216e 223217subjects [31e 33].In recent years this method has been used to investigate several attentional subprocesses,e.g.the role of the frontal eye fields and the PPC in attentional selection during TVA-based assessment in a partial report task [34,35].It has been shown that the right PPC and the right frontal eye field seem to represent both sides of space while the left PPC and the left frontal eye field seem to be representing only the contralateral right visual space (see also Ref.[36]).How visual space is represented in the precuneus was not well understood.However,a recent TMS study provided evidence for a neglect-like effect (rightward spatial bias)for near space judgments [37]after rTMS over the right precuneus,thus underpinning the role of the right precuneus in visuospatial functions.To examine the role of the precuneus in VSTM processes for items presented within and across the visual hemi fields we combine rTMS with a whole report task ([18,21])and analysis in terms of TVA [24].As described above NTVA assumes that occipital-parietal areas such as the precuneus are essential in weighting vi-sual information that is then transmitted to the thalamic reticular nucleus where the VSTM map of locations is represented.It has to be tested if both hemi fields are represented within the right pre-cuneus and whether TMS over the right or left precuneus affect the bilateral field advantage in VSTM.One could suggest that the right precuneus is part of the VSTM representation and serves as a general non-lateralized resource.Thus,we test the hypothesis thatrTMS applied over the right precuneus can directly reduce the bilateral field advantage in VSTM capacity.Our results show that rTMS over the right precuneus affected the bilateral field advantage while rTMS over the left precuneus lead to a similar bilateral field advantage as in the control conditions without TMS.Material and methods ParticipantsFifteen healthy subjects (11female,4male,mean age ¼25.9years,SD ¼3.3years)participated in the study.All were recruited at the Department of Psychology at the Humboldt-Universität zu Berlin and were reimbursed for their participation.Written informed consent was obtained from all participants before the examination.The experimental protocol was approved by the local ethical committee and conformed to the declaration of Helsinki and the safety guidelines for rTMS studies [38,39].Subjects ful filled the following criteria:no history of neurological,psychiatric or ophthalmological pathology,no alcoholism or mental deterioration and no acute or chronic medication affecting the central nervous system.All subjects were right-handed according to the Edinburgh Handedness Inventory [40]and had normal or corrected to normal visual acuity (near and far visus better than0.8).Figure 2.The stimulation center of rTMS over the precuneus (here the left precuneus)in the MNI brain.(A)Sagittal view,(B)coronal view,(D)axial view with corresponding MNI coordinates (À12,À65,50).(C)Illustration of the NTVA model of Bundesen and colleagues in 2005(From “A Neural Theory of Visual Attention:Bridging Cognition and Neuro-physiology,”by Bundesen et al.(2005),Psychological Review,112,p.295)overlaid on a sagittal image of our fMRI findings of a TVA Whole Report task (will be published elsewhere).The stimulation center is marked with a red flash.(For interpretation of the references to color in this figure legend,the reader is referred to the web version of this article.)A.Kraft et al./Brain Stimulation 8(2015)216e 223218Stimuli and procedureThe general procedure is similar to our previous study[18]that studied the effect of hemifield alignment on visual attention capacity parameters using the TVA approach[19,41].Distinct attentional parameters such as the visual span/VSTM capacity(parameter K;i.e.maximum number of reported letters), the visual processing speed(parameter C;rmation accu-mulation rate in number of letters per second),and the temporal threshold for visual perception(parameter t0)could be estimated (see also Shibuya&Bundesen,1988[22])using a whole report paradigm[21],in which the task was to report as many of the displayed letters as possible.The experiment was conducted in a dimly lit room.Subjects were seated90cm from the screen.Stimuli were presented on a 17-in PC monitor screen(1280Â1024-pixel resolution;60Hz refresh rate)using Presentation(Neurobehavioral Systems,Inc., Albany).The TVA hemifield tests with rTMS(left rTMS or right rTMS on separate testing days)took approximately90min(360trials on each testing day)to complete;the TVA hemifield test without rTMS (no rTMS,360trials)took approximately45min.On each testing day(left rTMS,right rTMS and no rTMS order balanced across subjects),each subject completed four blocks(90trials each)of intermixed1-hemifield(unilateral)and2-hemifield trials(bilat-eral),respectively,yielding a total of1080trials per participant.The general design of each trial and the hemifield conditions are outlined in Fig.1.In all trials participants were asked to maintain fixation on a redfixation cross(0.4 highÂ0.4 wide),centered in the middle of the screen on a black background.Thefixation cross was presented for1000ms and was followed by a100ms blank (black)screen before the letters were displayed.Six letters(1.2 highÂ1.1 wide)were randomly chosen without replacement from a set of20letters(ABDEFGHJKLMNOPRSTVXZ)and presented on an imaginary circle(r¼4.8 visual angle,spacing between center of positions2.8 )for variable exposure durations(16,33,66,100,160 or250ms).Each type of display was presented equally often in a random order.During the left and right rTMS blocks,trains of rTMS pulses at6Hz for333ms(3pulses)started with the onset of the letter array.The array was followed by a500ms mask(six masks, 1.5 highÂ1.5 wide,made from red and blue letter fragments,see Ref.[41]).After the presentation,subjects gave a non-speeded verbal report of the identities of the stimulus letters.The letters could be reported in arbitrary order.Subjects were instructed to report as many letters as possible,but refrain from guessing.Verbal response was recorded with a microphone and typed in by the experimenter seated outside the room.rTMSrTMS was generated by an eXimia biphasic TMS-System (Nexstim,Helsinki,Finland)with afigure-of-eight coil(50mm mean wing diameter)held by a mechanical arm.Stimulation was guided by a very accurate navigation software,which utilizes optical tracking to record the physical parameters with a precision below0.5mm.This procedure is based on a spherical model,the subject’s individual structural MR image and an individual X-ray derived coil model to estimate the intra-cortical stimulation location and strength[42,43].The resulting spatial maps were superimposed in color-code on the participants structural MR image(MDEFT(Modified Driven Equilibrium Fourier Tomography sequence),TE¼3.56ms,TR¼12.24ms,flip angle¼23 ,176slices, 1mm3).Using this system,stimulation was centered either to the left or right precuneus(i.e.Brodmann area7or PE;[44]), based on Montreal Neurological Institute(MNI)coordinates(left precuneusÀ12,À65,50;right precuneus12,À65,50)of the normalized brain for each subject and their corresponding indi-vidual anatomical landmarks on the non-normalized brains used for the TMS navigation software.An example of the stimulation center over the left precuneus is illustrated in Fig.2with corre-sponding MNI coordinates.During rTMS blocks,rTMS was delivered from the onset of each letter array in trains of6Hz for333ms(see Fig.1).The Navigated Brain Stimulation system(NBS)used in the current study provided real-time estimation of the electricalfield induced on the cortical surface by the TMS pulse.Therefore it allowed to precisely con-trolling the stimulation parameters for each subject during each session.TMS intensity was set at90e95V/m at the precuneus in each participant(mean¼91.4,SD¼ 2.4);i.e.50e65%of the maximum stimulator output(mean¼56.7,SD¼3.3).The intensity of rTMS was well within the safety guidelines[38,39].Overall each participant received2160TMS pulses(1080pulses on each rTMS testing day).Data analysisWe hypothesize that VSTM capacity is modulated by rTMS over the precuneus.However,beside the measurement of the in-dividual’s capacity limit of VSTM,TVA allows to measure the individual’s visual processing speed,as well as the individual’s temporal threshold of visual perception.In order to validate the specificity of the precuneus for the individual’s VSTM capacity,we also analyze the parameters processing speed and temporal threshold of visual perception.The TVA parameters K(the capacity of VSTM),C(processing speed,i.e.the total visual categorization rate)and t0(the longest ineffective exposure duration of a visual stimulus),were estimated for unilateral and bilateral conditions separately,for no rTMS trials, left rTMS trials and right rTMS trials,respectively,using a maximum likelihoodfitting procedure(for details see Ref.[24]). The TVA model predicts that the mean number of correctly reported letters(the score)increases as a function of exposure duration such that,for exposure durations shorter than t0ms,the score via nonguessing is zero;for exposure durations longer than t0ms,the score initially increases steeply,at a rate of C items/s, and then levels off,approaching an asymptote at a value equal to the VSTM capacity K or the number of letters in the stimulus, whichever is greatest[19,24].For most subjects,K lies between3 and4letters.Further statistical analysis was carried out using SPSS Software (Version19).Two way repeated measures ANOVA with factor “hemifield”(unilateral,bilateral)and factor“stimulation”(no rTMS, left rTMS,right rTMS)were used to evaluate the effect of rTMS stimulation over the left or right precuneus on the difference between the hemifields for TVA parameters K,C and t0 (Greenhouse e Geisser correction if necessary).Planned paired t-tests were used to test the difference between hemifield condi-tions for each stimulation condition separately.Differences were considered to be statistically significant at the0.05alpha level.ResultsAll subjects performed the task without any adverse effects due to TMS stimulation.TMS stimulation over the left or right pre-cuneus elicited no sensory paresthesias or muscle twitches.TVA capacity parametersFigure3A shows the mean VSTM capacity during no rTMS,left rTMS and right rTMS conditions.Figure3A suggests a bilateralfield advantage for the no rTMS and the left rTMS conditions,while theA.Kraft et al./Brain Stimulation8(2015)216e223219right rTMS condition indicates a reduced bilateral field advantage.The 2-way ANOVA with factor hemi field (unilateral,bilateral)and stimulation (no rTMS,left rTMS,right rTMS)revealed a signi ficant main effect for the factor hemi field [F (1,14)¼28.76,P <0.001],whereas the main effect for the factor stimulation [F (2,28)¼0.85,P >0.05]and the interaction between both factors [F (2,28)¼1.19,P >0.05]showed no signi ficance.Planned paired t -test con firmed a signi ficant bilateral field advantage for the no rTMS condition [t (14)¼À3.21,P <0.01]and the left rTMS condition [t (14)¼À5.06,P <0.001].In contrast,after right rTMS a bilateral field advantage cannot be observed [t (14)¼À1.82,P >0.05].To further analyze differences between left or right-sided rTMS in the left or right visual field we performed a 2-way ANOVA with factor visual field (left,right,bilateral)and factor stimulation (left rTMS,right rTMS).The main effect for the factor visual field reached signi ficance [F (2,28)¼30.38,P <0.001],whereas the factor stim-ulation [F (1,14)¼1.05,P >0.05]and the interaction between both factors [F (2,28)¼2.36,P >0.05]revealed no signi ficance.Figure 3Bshows that VSTM capacity was higher in the right compared to the left visual field,both for the left rTMS [t (14)¼À4.17,P <0.01]and the right rTMS condition [t (14)¼À6.44,P <0.001].The reduction of VSTM capacity during right rTMS is re flected in a similar per-formance for the right and bilateral visual field condition [t (14)¼0.10,P >0.05].VSTM capacity for bilateral displays is signi ficantly higher than for the right visual field condition after left rTMS [t (14)¼À3.21,P <0.01],as well as for the left visual field condition,both for left rTMS [t (14)¼À6.10,P <0.001]and right rTMS [t (14)¼À3.44,P <0.01].To further clarify this aspect,we performed a two-way ANOVA with factors visual field (left visual field,right visual field)and TMS condition (left rTMS,right rTMS)on the number of correctly reported letters in the bilateral visual field condition.If the precuneus is involved in the VSTM representation of each hemi-sphere/hemi field,a lateralized effect of stimulation should occur.If the resource is a supra-spatial one,there should be no difference in what is reported from each hemisphere/hemi field.The ANOVA revealed no signi ficant main effects for the factors visual field [F (1,14)¼0.12,P >0.05]and TMS condition [F (1,14)¼0.99,P >0.05]and no signi ficant interaction between both factors [F (1,14)¼0.36,P >0.05].Figure 4A illustrates mean visual processing speed during no rTMS,left rTMS and right rTMS conditions.Figure 4A suggests that left rTMS and right rTMS lead to increased visual processing speed for bilateral displays.However,the 2-way ANOVA with factor hemi field (unilateral,bilateral)and stimulation (no rTMS,left rTMS,right rTMS)showed no signi ficant effects;main effect hemi field [F (1,14)¼2.39,P >0.05],main effect stimulation [F (2,28)¼0.79,P >0.05],interaction hemi field Âstimulation [F (2,28)¼ 1.19,P >0.05].Figure 4B displays mean perceptual threshold during rTMS,left rTMS and right rTMS conditions.There is no systematic effect of rTMS on the perceptual threshold.The 2-way ANOVA with factor hemi field (unilateral,bilateral)and stimulation (no rTMS,left rTMS,right rTMS)showed no signi ficant main effects for the factors hemi field [F (1,14)¼0.76,P >0.05]and stimulation [F (2,28)¼0.20,P >0.05].Also,the interaction between hemi field and stimulation reached no signi ficance [F (2,28)¼0.98,P >0.05].DiscussionWe examined the role of the right and left precuneus during TVA-based assessment of a whole report task that allows to measure attention capacity parameters in unilateral and bilateral stimulus displays.Note that the interactions in the analyses of variance between the factors hemi field and type of stimulation were not signi ficant.According to our hypothesis we however computed planned post-hoc tests.Planned comparisons can examine speci fic and focused questions that are developed a-priori,based on hypothesis [45].We found that 6Hz TMS over the right precuneus diminished the bilateral field advantage in VSTM capacity,while we found a persisting and robust bilateral field advantage when rTMS was applied over the left precuneus,similar to the control condition without rTMS.Therefore,the stimulation effect of TMS over the right precuneus cannot be attributed to the presence or absence of rTMS per se,as it was speci fic for right but not left precuneus rTMS.Note also that rTMS over the left or right precuneus had no effect on visual processing speed and the temporal threshold of visual perception,under-lining the speci ficity of rTMS over the precuneus on the VSTM capacity parameter.The present findings indicate that the right precuneus has a causal role for the bilateral field advantage in VSTM capacity,thus supporting the notion that hemisphere-speci fic resources arealsoFigure A parameter estimates for the VSTM capacity parameter K.(A)The capacity of VSTM K across trials for the one-hemi field (unilateral)and two-hemi field (bilateral)trials for the no rTMS condition (indicated in white bars),the left rTMS condition (indicted in gray bars)and the right rTMS condition (indicted in black bars).(B)The capacity of VSTM K across trials for the left visual field (left),right visual field (right)and bilateral displays (bil)for the left rTMS condition (left bars)and the right rTMS condition (right bars).A.Kraft et al./Brain Stimulation 8(2015)216e 223220evident on a later stage of visual attentional processing [16e 18].According to the concept of Marsel Mesulam [10]the right hemi-sphere represents both sides of the visual field rather than only the contralateral visual field.The apparent hemispheric asymmetry in our study fits well with this concept and is congruent with a pre-vious TMS study [34],neuroimaging findings [11,12,46]and lesion studies [47,48].In the study of Hung et al.(2005)[34]TVA analysis of a partial report task revealed that TMS applied over the right PPC affected the ef ficiency of top-down control in both visual fields.While it disrupted attentional selection in the contralateral left visual field,it enhanced top-down control in the ipsilateral right visual field.This indicates that rTMS over the PPC has an effect on the contralateral and ipsilateral field while rTMS over the pre-cuneus only has an effect on bilateral displays.Moreover,analyzing the correctly reported letters in the bilat-eral conditions revealed no difference for the left and right visual field after rTMS over the right precuneus.As described in the re-sults section this finding is not congruent with the assumption of a VSTM representation for each hemi field within each hemisphere.Then a lateralized effect of stimulation should occur.Instead,the current findings indicate a supra-spatial resource within the right precuneus.Note also that there was no effect on performance after rTMS over the right precuneus if targets were presented unilat-erally.One could suggest that bilateral presentation induce competition for representation which is augmented after TMS over the right precuneus similar to the phenomenon of extinction [36,37].Recent studies indicated that the bilateral field advantage is stronger if distractors were to be introduced [2,16].Moreover,VSTM capacity varies between individuals [49]and recent studies have shown that the activity level in the PPC predicts differences in VSTM capacity between individuals [50].Future work could test how visual attention capacity parameters and top-down control change with rTMS over the left and right precuneus in unilateral and bilateral stimulus displays for high and low performers if dis-tractor stimuli were introduced [28].Furthermore,previous behavioral studies showed that the bilateral field advantage in VSTM could be restricted to speci fic visual modalities (letter versus color identi fication task)[51].We have shown that rTMS over the precuneus affect speci fically letter identi fication in a whole report task but it remains unclear if this effect can be generalized to other attention tasks.fMRI studies provide evidence that spatial coding in the parietal cortex can be attention-task-speci fic [46],for instance stronger lateralized activ-ity to the right and left hemisphere in subprocesses of attention such as stationary spatial orienting versus visual search.However,a previous TMS study [34]provides evidence that also color-based selection can be in fluenced by rTMS over the PPC.In the present study rTMS over right precuneus reduced VSTM capacity.Interestingly no effect on visual processing speed and the temporal threshold of visual perception was found.In healthy control subjects the parameter processing speed and the param-eter VSTM capacity correlate about 0.40[52],although such dependence is left undeclared in the TVA model [19].Studies investigating stroke patients with large frontal or parietal lesions after stroke [53,27,54,55]also found that both parameters are affected.TMS-induced disruption targets a speci fic region in normal subjects,and our results indicate a speci fic effect on VSTM capacity,while not affecting processing speed signi ficantly.A study investigating alertness effects on TVA parameters in normal subjects found a speci fic effect on the parameter processing speed,while not affecting the VSTM capacity [56].This indicates that the TMS-induced effect on the VSTM capacity cannot be explained as an alertness effect.Moreover,in a recent event related potential (ERP)study Wiegand and colleagues (2013)[57]found distinct ERP correlates for visual processing speed and VSTM storage capacity parameters using the TVA approach.While high processing speed was re flected in a reduced N1component,a high VSTM storage capacity was re flected in an enhanced contralateral delay activity over visual areas.The find-ings of Wiegand et al.(2013)[57]and the current results support the suggestion that processing speed and VSTM storage capacity have distinct underlying brain mechanism.This assumption of distinct neurophysiological correlates for the two parameters is congruent with the neural implementation of the TVA model,called NTVA [26].However,a recent study by Soto et al.(2012)[58]revealed that rTMS over the occipital cortex can enhance the detection of features that should be held in working memory.So far,there has been no rTMS study investigating how the bilateral field advantage in attentional processing is modulated if rTMS is delivered over the occipital cortex and whether processing speed and VSTM capacity are modulated independently,as suggested by Wiegand et al.(2013)[57]and the presentstudy.Figure A parameter estimates for the processing speed parameter C and the perceptual threshold t 0.(A)The visual processing speed C across trials for the one-hemi field (unilateral)and two-hemi field (bilateral)trials for the no rTMS condition (indicated in white bars),the left rTMS condition (indicted in gray bars)and the right rTMS condition (indicted in black bars).(B)The temporal threshold for visual perception t 0for the one-hemi field (unilateral)and two-hemi field (bilateral)trials for the no rTMS condition (indicated in white bars),the left rTMS condition (indicted in gray bars)and the right rTMS condition (indicted in black bars).A.Kraft et al./Brain Stimulation 8(2015)216e 223221。