Behavioral performances.
\r\n\tIn recent years, epidemiological studies, paired with genomic analyses have shed light on specific interactions of Helicobacter pylori and the increased risk of development of digestive and extradigestive outcomes. Genomic tools such as genome sequencing, restriction fragment length polymorphism genome mapping and analytical methods are enhancing the molecular epidemiological methods currently used to study H. pylori pathogenesis. Besides, new drugs and different combinations of them have been suggested to eradicate the microorganism and scientists around the world have discussed the management of the infection, considering the host characteristics.
\r\n\r\n\tThis book is an invitation for having a different look at Helicobacter pylori infection, since its first isolation by Warren and Marshall in the 80´s until nowadays.
",isbn:"978-1-83968-292-6",printIsbn:"978-1-83968-291-9",pdfIsbn:"978-1-83968-293-3",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!1,hash:"f90afe88d326a6554b6e094e93f0f0e7",bookSignature:"Dr. Bruna Maria Roesler",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/10141.jpg",keywords:"Virulence Factors, Genotyping, Pathogenicity, Host-Pathogen Interaction, Gastritis, Peptic Ulcer Disease, Gastric Cancer, Development of Gastrointestinal Disorders, Management of Antimicrobial Resistance, New Drugs, Antibiotics, Helicobacter pylori and Extradigestive diseases",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"September 1st 2020",dateEndSecondStepPublish:"September 29th 2020",dateEndThirdStepPublish:"November 28th 2020",dateEndFourthStepPublish:"February 16th 2021",dateEndFifthStepPublish:"April 17th 2021",remainingDaysToSecondStep:"5 months",secondStepPassed:!0,currentStepOfPublishingProcess:5,editedByType:null,kuFlag:!1,biosketch:"Dr. Roesler is a pharmacist biochemist and holds a Master’s degree in Pharmacology and a Doctoral degree in Basic Sciences - Internal Medicine from the State University of Campinas. Her research includes the etiology, epidemiology, and physiopathology of gastrointestinal diseases.",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"54995",title:"Dr.",name:"Bruna Maria",middleName:null,surname:"Roesler",slug:"bruna-maria-roesler",fullName:"Bruna Maria Roesler",profilePictureURL:"https://mts.intechopen.com/storage/users/54995/images/system/54995.jpg",biography:"Dr. Bruna Maria Roesler is a pharmacist biochemist and holds\r\na Master’s degree in Pharmacology and a Doctoral degree in\r\nBasic Sciences—Internal Medicine from the State University of\r\nCampinas (Campinas, SP, Brazil) where she has identified the\r\nprincipal genotypes of Helicobacter pylori strains in patients with\r\nchronic gastritis, peptic ulcer disease, and gastric cancer (early\r\nand advanced stages) through molecular biology techniques. She\r\nhas published her work in several peer-reviewed journals and given oral and poster\r\npresentations at various congresses. Her research also includes the etiology, epidemiology, and physiopathology of gastrointestinal diseases. She has also participated\r\nin studies that reported the possible relationship between H. pylori and idiopathic\r\nthrombocytopenic purpura, as well as between H. pylori and liver diseases.",institutionString:"State University of Campinas",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"5",totalChapterViews:"0",totalEditedBooks:"4",institution:{name:"State University of Campinas",institutionURL:null,country:{name:"Brazil"}}}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"13",title:"Immunology and Microbiology",slug:"immunology-and-microbiology"}],chapters:null,productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"252211",firstName:"Sara",lastName:"Debeuc",middleName:null,title:"Ms.",imageUrl:"https://mts.intechopen.com/storage/users/252211/images/7239_n.png",email:"sara.d@intechopen.com",biography:"As an Author Service Manager my responsibilities include monitoring and facilitating all publishing activities for authors and editors. From chapter submission and review, to approval and revision, copyediting and design, until final publication, I work closely with authors and editors to ensure a simple and easy publishing process. I maintain constant and effective communication with authors, editors and reviewers, which allows for a level of personal support that enables contributors to fully commit and concentrate on the chapters they are writing, editing, or reviewing. I assist authors in the preparation of their full chapter submissions and track important deadlines and ensure they are met. I help to coordinate internal processes such as linguistic review, and monitor the technical aspects of the process. As an ASM I am also involved in the acquisition of editors. Whether that be identifying an exceptional author and proposing an editorship collaboration, or contacting researchers who would like the opportunity to work with IntechOpen, I establish and help manage author and editor acquisition and contact."}},relatedBooks:[{type:"book",id:"3839",title:"Trends in Helicobacter pylori Infection",subtitle:null,isOpenForSubmission:!1,hash:"3dc63cbee177c36f568ff67aa6ec1413",slug:"trends-in-helicobacter-pylori-infection",bookSignature:"Bruna Maria Roesler",coverURL:"https://cdn.intechopen.com/books/images_new/3839.jpg",editedByType:"Edited by",editors:[{id:"54995",title:"Dr.",name:"Bruna Maria",surname:"Roesler",slug:"bruna-maria-roesler",fullName:"Bruna Maria Roesler"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"5102",title:"Extradigestive Manifestations of Helicobacter Pylori Infection",subtitle:"An 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Optoelectronics",subtitle:null,isOpenForSubmission:!1,hash:"deb44e9c99f82bbce1083abea743146c",slug:"frontiers-in-guided-wave-optics-and-optoelectronics",bookSignature:"Bishnu Pal",coverURL:"https://cdn.intechopen.com/books/images_new/3161.jpg",editedByType:"Edited by",editors:[{id:"4782",title:"Prof.",name:"Bishnu",surname:"Pal",slug:"bishnu-pal",fullName:"Bishnu Pal"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"72",title:"Ionic Liquids",subtitle:"Theory, Properties, New Approaches",isOpenForSubmission:!1,hash:"d94ffa3cfa10505e3b1d676d46fcd3f5",slug:"ionic-liquids-theory-properties-new-approaches",bookSignature:"Alexander Kokorin",coverURL:"https://cdn.intechopen.com/books/images_new/72.jpg",editedByType:"Edited by",editors:[{id:"19816",title:"Prof.",name:"Alexander",surname:"Kokorin",slug:"alexander-kokorin",fullName:"Alexander Kokorin"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"1373",title:"Ionic Liquids",subtitle:"Applications and Perspectives",isOpenForSubmission:!1,hash:"5e9ae5ae9167cde4b344e499a792c41c",slug:"ionic-liquids-applications-and-perspectives",bookSignature:"Alexander Kokorin",coverURL:"https://cdn.intechopen.com/books/images_new/1373.jpg",editedByType:"Edited by",editors:[{id:"19816",title:"Prof.",name:"Alexander",surname:"Kokorin",slug:"alexander-kokorin",fullName:"Alexander Kokorin"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"57",title:"Physics and Applications of Graphene",subtitle:"Experiments",isOpenForSubmission:!1,hash:"0e6622a71cf4f02f45bfdd5691e1189a",slug:"physics-and-applications-of-graphene-experiments",bookSignature:"Sergey Mikhailov",coverURL:"https://cdn.intechopen.com/books/images_new/57.jpg",editedByType:"Edited by",editors:[{id:"16042",title:"Dr.",name:"Sergey",surname:"Mikhailov",slug:"sergey-mikhailov",fullName:"Sergey Mikhailov"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"45291",title:"Exploring the Effect of Verbal Emotional Words Through Event-Related Brain Potentials",doi:"10.5772/56494",slug:"exploring-the-effect-of-verbal-emotional-words-through-event-related-brain-potentials",body:'\nFor centuries, philosophers and neuroscientists have questioned whether the use of language and the ability to solve complex problems are related and, if so, what the nature of the relationship between language and thought is. Most of the attention – and controversy – have been focused on the claim that the structure of language shapes non-linguistic thinking; so-called linguistic relativity.\n
\nHuman intelligence directly derives from brain activity and it is closely linked to the natural languages that humans speak [1]. The Language, this complex system of sound-meaning connections, not only provides a comprehensive description of the world, but its acquisition is one of the most fundamental human traits, and it is obviously the brain that undergoes the developmental changes.
\nBrain development seems to be non-linear, with sensitive periods of time in which the characteristics of experiences determine different possible outcomes [2]. In fact, during development, the brain not only stores linguistic information but also adapts to the grammatical regularities of language.
\nLanguage acquisition might be oversimplified as the way in which the brain learns, perceives, represents and integrates complex sequences of verbal events. The temporal nature of sounds, structural integration, expectations, and cognitive sequencing allows the brain to construct progressively intricate representations of the environment, and with progressive maturity, even aspects of emotion or cognition not readily verbalized may be influenced by linguistically based thought processes.
\nNo matter whether it is verbal or not the new material we have to deal with, once it appears it is processed through a group of co-acting neural specific subsystems which allow us to detect, encode, temporarily hold and compare incoming stimuli with previous material, along with the decision making on what to do next. In this context, it is crucial to understand that certain characteristics of the stimulus might influence its processing and, if so, how these characteristics interact with cognitive processing.
\nPresently, it is generally accepted that incoming information is initially processed in the working memory (WM), which is a theoretical construct used to refer to the system or mechanism underlying the maintenance of task-relevant information during the performance of a cognitive task. WM is crucial for a wide range of complex cognitive activities but has a limited capacity [3-5]. Enough empirical evidence supports that WM plays an important role in recognition, encoding and manipulation of task-related and concurrent distractor stimuli, while WM load influences attention modulation. In fact, the working memory central executive system [6,7], concept based on the “Supervisory Attentional System” proposed by Shallice [8,9], is critical for systematizing a continuous “background monitoring” that searches for new relevant information, even though the information may be irrelevant to the ongoing act [10,11]. These “background-monitoring’’ mechanisms seem to be designed to eventually interrupt the current action and trigger an updating of working memory [12]; thus, WM provides goal-directed control of visual selective attention and allows the minimization of interference caused by goal irrelevant distractors [13].
\nThe interaction between attention and working memory is bidirectional. It has been postulated that the maintenance of information in working memory is accomplished by directing attention to the neural representations of the information itself [14], whereas attentional orienting within working memory can retroactively influence maintenance-related activity in functionally specialized posterior areas by engaging selective retrieval functions [see reference 15 for a review]. Even while flexible switching between goals may require maintaining higher sensitivity to possibly relevant information, distracting stimuli must be continuously evaluated and suppressed. Therefore, behavioral performance could be sensitive to the “on-line” appearance of environmental distractors; especially when they could be “relevant” to the subject.
\nSeveral theories posit that emotionally salient stimuli have privileged access during information processing [16,17] which implies that affective stimuli have the capacity to transcend task boundaries, disrupting ongoing processing regardless of whether they are relevant to the current task-set or not.
\nNumerous studies have addressed the effects of affective stimuli on cognitive processes such as attention, memory and executive functions [18-27]. Actually, it seems that the appearance of an emotional stimulus might interfere with the processing of other stimuli emerging in the temporal vicinity, basically due to the fact that stimuli with emotional content attract attentional resources because of their adaptive relevance [28-31].
\nThe acceptance of the assumption that affective stimuli disrupt subsequent cognitive processing raises the question whether there is an asymmetry between emotional and cognitive processing (i.e., emotional distractors disrupt cognitive processing, but not vice versa). Recently, Reeck and Egner [32] studied this issue using a face-word Stroop protocol adapted to independently manipulate (a) the congruency between target and distractor stimulus features, (b) the affective salience of distractor features, and (c) the task-relevance of emotional compared to non-emotional target features. As a result of this study, the authors concluded that task-irrelevant emotional distractors resulted in equivalent performance costs as task-relevant non-emotional distracters, whereas task-irrelevant non-emotional distractors did not produce performance costs comparable to those generated by task-relevant emotional distractors. In other words, this study documented the abovementioned asymmetry between affective and cognitive processing, supporting the notion that affective stimuli are prioritized in human information processing.
\nOn the other hand, an increased arousal of the stimulus has been associated with a more intense defensive response when compared to appetitive motivational systems [33-35]. Accordingly, the arousal of unpleasant stimuli is comparatively higher, leading to what has been termed as emotional negativity bias [36-38]. In addition, it has been postulated an emotional positivity offset when lower arousal stimuli are processed, as is possible to infer from the enhanced processing of pleasant compared to unpleasant stimuli, when they both are lower arousal ones [33,39,40].
\nEmotional words are consistently acknowledged as low arousal stimuli [41-44], particularly in comparison with emotional scenes or faces [45-47]. This effect has been explained as a result that words depict emotional events less vividly [42]. Interestingly, it has been proposed that verbal material is less capable of disrupting cognitive performance than pictures, particularly when using negative words, what reinforces the notion that emotional verbal stimuli associate with lower brain responsivity. However, it seems that arousing verbal stimuli can lead to amygdala activation similar to that induced by emotional faces, pictures, or conditioned stimuli [48].
\nRecent advances in neuroimaging techniques have demonstrated that the amygdala, ventromedial prefrontal cortex (VMPFC), anterior cingulate, insula, nucleus accumbens and basal ganglia are all involved in emotion processing and executive control in some capacity [49-53]. In fact, it has been found that left and right interior frontal gyrus (IFG) regions differentiate between interference and noninterference trials across neutral and emotional stimuli; a region of the left anterior insula and right orbital frontal cortex (OFC) is capable to differentiate between interference and non-interference trials for emotional stimuli, regardless of valence, whereas the insula, OFC and ventral anterior cingulate cortex (ACC) seem to be sensitive to interference resolution for a select valence and that the left amygdala differentiated emotional and neutral stimuli at encoding and response [54]. Furthermore, the behavioral patterns observed in patients with either left temporal lesion or right OFC lesion suggest that the left amygdala and right OFC are both critical to the emotion facilitation effect [55].
\nIn the last few years, the temporal course of the brain processing of emotional words has been studied through event-related brain potentials (ERPs) techniques, showing that earlier components as P120, N170 and P200 (including a variant closely related to N170 and termed as vertex-positive potential: VPP) could be sensitive to the emotional content of the word and the subsequent attentional allocation process [42,45,56], while later ERP changes as Early Posterior Negativity, N400 and Late Positive Components could reflect semantic stages of processing [40,57,58].
\nEven though there is a general consensus that emotionally arousing faces or scenes capture a substantial amount of visual processing resources even if they appear as distractors for a concurrent cognitive task, scarce data is available on the effect due to task-irrelevant emotional words.
\nA recent study evaluated the effect of written emotional words sharing the scene in which subjects had to perform a simultaneous visual perceptual task [59]. The authors reported emotion effects of task-irrelevant words on the ERPs before 300 ms, but not any interference with the visual foreground task was evidenced by task-related steady-state visual evoked potential amplitudes or behavioral data. The results were interpreted as suggesting a specificity of emotion effects on sensory processing that might depend on the information channel from which emotional significance is derived. However, these effects appeared when distractors and task-relevant stimuli shared the same sensory modality –visual-, along with a similar temporal appearance. Therefore, one could speculate if there is any effect of emotional irrelevant words when equating the nature of both relevant and task-irrelevant stimuli, while delivering distractors through a different sensory modality, but immediately preceding the task onset.
\nFollowing the previous idea, we studied the effect of auditory emotional words on the ERPs and behavioral performance of a subsequent highly demanding visual verbal working memory task, with the general hypothesis that the enhanced capture of lexico-semantic processing resources by emotional distractor words could last long enough as to interfere verbal subsequent processing, particularly in high cognitive demand situations.
\nNext, various methodological considerations and results from the abovementioned study are detailed, as well as how they could be interpreted in the context of the previously discussed related literature.
\n\n Subjects. In order to explore our hypothesis, 18 healthy, right-handed, university female subjects were recruited to voluntarily participate in the experiment (mean age= 26.1 years; SD= 4.1).
\n\n\n Experimental task. Behavioral data and ERPs were obtained during task performance. Subjects performed a dual working memory task. The first part of the task consisted in the serial presentation of two-syllable, four-letter words during 500 ms. Participants were given explicit instructions to first read the word silently and then, as soon as possible, pronounce aloud an arrangement of letters made up of the second syllable of the word followed by the inverted letters of the first syllable (e.g. BOTE – TEOB). Pronunciation times (RT) and the number of correct responses were measured for all trials. In the second part of the task, subjects were asked to decide, by pressing a key, if a string of four letters (which appear during 500 ms) represented – or not – the inverted order of the first word that was presented [e.g. BOTE – ETOB (inverse; 50% of the stimuli) or OTEB (not inverse: 50% of the stimuli)]. The time interval between the visual appearance of the word and the string of letters was 1000 ms. One hundred and fifty different high frequency words [60] were used as stimuli. Figure 1 shows the experimental flow chart.
\nParticipants were seated comfortably in a quiet, dimly lit room. Visual stimuli were presented on an SVGA monitor (refresh rate: 100 Hz). Words were written in white capital letters (Arial) against a black background displaying a visual angle of 0.80°. Preceding each one of the trials of the task, a context was presented to the subjects. Five blocks of 50 trials each – a total of two hundred and fifty trials – were configured by combining three randomly-distributed main conditions. After each block, subjects had a brief rest period. The presentation order of the blocks was counterbalanced. The two conditions that constituted the trial blocks were:
\n\n A (reference trials): Fifty trials in which the WM trial was free from preceding stimuli.
\n\n B (auditory preceding stimuli) 200 trials in which the WM trials were preceded by words –delivered binaurally- showing different emotional content:
\nBa - positive (50 trials)
\nBb - negative (50 trials)
\nBc - neutral (50 trials)
\n\n C - control (50 trials)
\n\n Auditory stimuli. Auditory stimuli were designed based on the results of a verbal production paradigm performed by 50 female voluntary subjects with similar ages and educational level with the participants in the ensuing electrophysiological experiment. They were instructed to write words freely with three different emotional contents: positive, negative and neutral. Subsequently, the most common 50 words in each category were selected and randomly presented to another group of 50 subjects –similar ages and educational level than participants- with the instruction to classified them in a continuum from very negative (0) to very positive (10) with 5 as the neutral emotional content.
\nLater, twenty-five words with averaged scores below 1.5 were selected and labeled as “negative” (i.e. “TONTA”; “SILLY”). Other twenty-five exemplars with averaged scores above 8.5 were selected and labeled as “positive” (i.e. “BONITA”, “PRETTY”), while further twenty-five words with scores ranging from 4 to 6 points were selected and labeled as “neutral” (i.e. “LADO”, “SIDE”). Both positive and negative words were female adjectives. The 75 resultant words were tape-recorded in a professional facility studio by a professional broadcaster. The length of the audio files was digitally restricted to 500 ms each. Besides, other 75 audio-files were created to be used as controls, by inverting the 75 files containing the spoken words, with the aim to keep similar physical characteristics but avoiding semantic bias.
\nUsing the selected audio-files, three semi-randomized lists with different emotional content -50 words each- were created (each word was presented twice in its corresponding list). In addition, another list of 50 inverted audio-files was created to act as control (C), including 16 inverted positive, 16 inverted negative and 18 inverted neutral spoken words.
\nAll the auditory stimuli were delivered binaurally via COBY (CV-200) headphones (COBY Electronics, Corp., U.S.A) controlled by the software MindTracer (Neuronic S.A., Cuba), at 85 dB SPL. Previous pilot studies were done to guarantee that the sound level used were not only audible but comfortable.
\nExperimental design and flow chart.
ERP Acquisition. ERPs were obtained, in all conditions, time-window starting 500 ms after auditory stimuli onset, which corresponded to 300 ms before dual WM task onset, until 750 ms after it. ERPs were recorded from the Fp1, Fp2, F7, F8, F3, F4, C3, C4, P3, P4, O1, O2, T3, T4, T5, T6, Fz, Cz, and Pz scalp electrode sites, according to the International 10-20 system. The electrooculogram (EOG) was recorded from the outer canthus and infraocular orbital ridge of the right eye.
\nElectrophysiological recordings were made using 10 mm diameter gold disk electrodes (Grass Type E5GH) and Grass electrode cream. All recording sites were referred to linked mastoids. Interelectrode impedances were below 5 kΩ. EEG and EOG signals were amplified at a bandpass of 0.5–30 Hz (3-dB cutoff points of 6 dB/octave rolloff curves) with a sampling period of 4 ms on the MEDICID-04 system. Single trial data were examined off-line for averaging and analysis.
\nERP Scoring. Prior to scoring, EEG data was visually corrected for artifacts due to eye movement. Epochs of data on all channels were excluded from averages when voltage in a given recording epoch exceeded 100 µV on any EEG or EOG channel. In general, 3 to 7 epochs had to be rejected in each condition per subject. Thirty free-artifact correct trials were considered to obtain the individual ERP in each condition, reaching a signal-noise ratio higher than 1.5 in all cases. Amplitude and latency for the ERP components of focal interest were measured according to a 100-ms pre-stimulus baseline. All scoring was conducted baseline-to-peak through visual inspection.
\nData Analysis. Repeated Measure Analyses of Variance (RM-ANOVAs) were used to study behavioral responses and reaction times. Electrophysiological data was analyzed using Randomized-block Analysis of Variance [Conditions x Recording Sites; see reference 61] with average voltage across each time window as the dependent variable. The latency and amplitude of each ERP component were quantified by the highest peak within each respective latency window. Considering the appearance of the task-relevant stimuli as the initial time instant (t0), several time windows were used to examine averaged ERP-waveforms. In addition, post-hoc Tukey’s HSD tests were carried out to explore the trend of the differences found.
\nBehavioral results. The analysis of the correct responses showed significant differences between the experimental conditions (F(4,60)= 4.65, p<0.05). Post-hoc comparisons showed that when the WM task onset was preceded by positive words, the number of correct responses significantly decreased, as compared to negative (Bb) or control (C) auditory stimuli (p<0.05), and when compared to neutral (Bc) or none (A) precedent stimuli (p<0.01) as well. Although the comparison between negative and control stimuli did not reached statistical significance, when negative stimuli preceded the task the amount of correct responses tended to decreased. The Table 1 shows the behavioral performances in the experimental task.
\n\n Experimental Task Performance\n | \nNo Auditory Stimuli | \n \n Auditory words with emotional content\n | \n\n Auditory Control stimuli\n | \n|||||||
\n | \n Mean\n | \n\n SD\n | \n\n Mean\n | \n\n SD\n | \n\n Mean\n | \n\n SD\n | \n\n Mean\n | \n\n SD\n | \n\n Mean\n | \n\n SD\n | \n
\n | \n | \n | \n Neutral\n | \n\n Positive\n | \n\n Negative\n | \n\n | \n | |||
\n Correct Responses\n | \n42.3 | \n6.6 | \n42.3 | \n6.1 | \n38.6 | \n6.4 | \n39.8 | \n4.3 | \n41.4 | \n5.3 | \n
\n Reaction Times\n | \n868.3 | \n88.0 | \n908.4 | \n112.6 | \n986.4 | \n104.2 | \n896.7 | \n76.4 | \n896.7 | \n76.4 | \n
Behavioral performances.
SD: standard deviations. Reaction times are expressed in milliseconds.
The pronunciation times - the time it took the subject to give the verbal response – were also significantly different across conditions (F(4,60)= 6.18, p<0.05). Post hoc analyses showed that the WM task performance preceded by positive words was significantly slower than that associated to control auditory stimuli or the lack of any precedent one (p<0.01). In addition, performances preceded by positive words were also slower than those preceded by neutral or negative words (p<0.05). See Table 1.
\n\n Electrophysiological results.\n\n Regarding the visual inspection of the resultant ERPs waveforms, three main components were discernible over the fronto-central region, when there was not any auditory stimulus preceding the WM task; an early negativity peaking over 80 ms subsequent to the instant in which the first visual stimuli (word) appeared, followed by a prominent P2 component (VPP) reaching its maximum at 170 ms, and a slow negativity with maximum about 400 ms at vertex. Probably due to the fact that the WM task involved mental manipulation of visual words, a left-lateralized N170 was discernible over the posterior regions. Figure 2 shows the grand-averaged ERPs that correspond to three experimental conditions: none auditory stimuli (A), neutral words (Bc) and reversed-words (C: control) preceding the beginning of the WM dual task.
\nGrand-averaged ERPs in three experimental conditions: without auditory stimuli (A), neutral words (Bc), and reversed-words (C: control), preceding the beginning of the WM dual task.
One first ERP analysis was performed with the aim to elucidate the effect of any auditory stimuli preceding the beginning of the WM task on task-related visual ERP waveforms. With this goal, the three time windows which best represented the main ERPs changes were analyzed in the locations where they mainly occurred (-300-0, 0-300, and 300-750 ms, respectively). The presentation of the first task-relevant stimuli was taken as the initial time instant (t0).
\nRandomized-block ANOVAs using two factors [Condition (3: A, Bc and C); Recording Sites (8: Fp1, Fp2, F3, F4, C3, C4, Fz, and Cz)] were performed, showing significant differences for both factors (Condition: F(2,322)=17.94, p<0.0001, and recording sites: F(2,322)=5.10, p<0.0001), in the time window that preceded the beginning of the experimental task. No relevant interaction was found. This finding is compatible with the decrease observed in the slight early negative shift during conditions in which auditory stimulus were delivered.
\nThe analysis of the time window in which N80 and P170 occurred, showed significant differences between conditions [(F(2,322)= 39.65, p<0.0001)], recording sites [(F(7,322)= 41.11, p<0.0001)], and their interaction [(F(14,322)= 2.99, p<0.001)]. Post-hoc analysis demonstrated that at fronto-central locations, ERPs reached significantly minor voltage amplitude when there was no preceding auditory stimuli (A), in comparison with the conditions in which they were presented (Bc and Bd; p<0.01).
\nFinally, the analysis of the N400 component also showed significant differences between conditions [(F(2,322)= 26.74, p<0.0001)], recording sites [(F(7,322)= 2.78, p<0.001)] and their interaction [(F(14,322)= 2.66, p<0.01)]. In this case, post-hoc tests showed that N400 was widely located, while showing significantly greater amplitude when no auditory stimuli were present, in comparison to the conditions in which they were (p<0.01).
\nFollowing an analog procedure, randomized-block ANOVAs were performed to clarify the effect of the emotional content of the preceding auditory stimuli on task performance. Therefore, two factors were analyzed [Condition: positive (Ba), negative (Bb) and neutral words (Bc); and Recording sites (Pz, P3, P4, O1, O2, T5 and T6)] in the time-windows which corresponded to the main ERP changes: -300-0 ms, 0-250 ms, 250-500, and 500-750 ms. Figure 3 shows the grand-averaged ERPs that correspond to three experimental conditions preceded by the following auditory stimuli: positive words (Ba), negative words (Bb) and neutral words (Bc).
\nGrand-averaged ERPs in three experimental conditions: positive words (Ba), negative words (Bb) and neutral words (Bc), preceding the beginning of the WM dual task.
The ERP analysis of the time elapsed from the auditory stimuli to the task onset (-300-0 ms) showed significant differences between conditions [(F(2,238)= 8.64, p<0.001)] and recording sites [(F(6,238)= 6.55, p<0.0001)] without any relevant interaction. In this case, the experimental conditions preceded by positive and negative words showed significantly minor voltages than that preceded by neutral words. This result suggests that visual ERP are capable of depicting a cross-modal effect of the emotional content of the auditory stimuli even earlier than the beginning of the task-related cognitive effort.
\nSimilarly, the analysis of the time-window between the task-onset and the subsequent 250 ms showed significant differences only between conditions [(F(2,238)= 9.03, p<0.001)] and recording sites [(F(6,238)= 43.83, p<0.0001)]. In this time window the conditions preceded by positive and negative words also showed significantly minor voltages than the neutral ones.
\nThe analysis of the time period between 250 and 500 ms subsequent to the task-onset demonstrated significant differences between conditions [(F(2,238)= 14.43, p<0.0001)] and recording sites [(F(6,238)= 13.68, p<0.0001)] without relevant interactions. As it occurred in the previous time-windows, minor voltages corresponded to trials preceded by positive and negative words, what reinforces the notion that neural effects caused by distracting affective stimuli might last longer than expected.
\nFinally, the analysis of the later period of time showed that conditions [(F(2,238)= 15.55, p<0.0001)] and recording sites [(F(6,238)= 3.95, p<0.01)] reached statistical significance, also without any significant interaction. In this case, there were also higher voltages in trials preceded by neutral words.
\nThe analysis of the correct responses achieved while performing the experimental task showed that when the onset of the WM task was preceded by positive words, the number of correct responses significantly decreased, as compared to the alternative conditions, while negative words tended to show the same effect without attaining statistical significance. In addition, the pronunciation times were significantly different across conditions, being particularly longer when positive words preceded the task onset.
\nTherefore, one possible first conclusion might be that auditory emotional words evoked a sustained interfering effect on task performance, even though they were task-irrelevant. This finding coincides with the report from Sakaki and colleagues [62] who recently studied the effect of emotional events on the cognitive processing of subsequent stimuli. Despite the fact that not all types of later cognitive processes are impaired by preceding negative events, they found that the presentation of negative pictures interferes with subsequent semantic processing. In our experiment, the use of female adjectives might have enhanced the arousal elicited by the auditory verbal stimuli with emotional content, particularly considering that the participants in the experiment were female subjects.
\nIt has been reported that when the subjects are instructed to perform a semantic categorization using emotional words as distractors, affective mismatches are detected automatically and modulate a binding of irrelevant information with responses [63]. Furthermore, the notion that the effect of emotional words could be narrowed to certain aspects of cognitive processing is reinforced by recent findings pointing out that negative words interfere with the allocation of dimensional attention to different features of an attended object, but they do not capture spatial or object-based mechanisms of visual attention [64].
\nWhatever the effect of emotional stimuli might be, it should depend on their distinctive characteristics. In this regard, it has been reiteratively demonstrated that the arousal associated to the stimulus definitely influences its subsequent processing. Despite the low arousal attributed to verbal stimuli, emotional words might be more arousing than neutral ones, probably due to their intrinsic relevance to individual social suitability. In fact, these differences in the word-arousal level could explain distinct processing outcomes as it occurred when Guillet and Arndt [65] demonstrated that while examining memory for peripheral information, memory for peripheral words was enhanced when it was encoded in the presence of emotionally arousing taboo words but not when it was encoded in the presence of words that were only negative in valence.
\nThe effects of the emotional valence of the stimuli have been profusely discussed in the literature. However, beyond the different neural subsystems underlying emotional recognition, the exact effect of emotional words on cognitive processing remains far from being elucidated. During the previous paragraphs, some empirical evidence supporting the notion that negative stimuli interfere with subsequent cognitive processing has been documented. This could portray the tendency observed for some behavioral responses in the present study, but do not elucidate the predominant effect of positive distractors preceding the experimental task.
\nIn order to clarify the effect of preceding positive words on later cognitive processing at least two variables must be considered: a) positive emotional valence and b) dissimilarities in sensory activation when distractors are auditory stimuli while task-relevant targets are visually displayed.
\nAbundant empirical evidence supports the idea that stimuli with positive valence influence subsequent processing. Visual scenes such as smiling and attractive faces, appetizing foods and beautiful pictures can evoke strong emotions. People routinely employ such emotional imagery in the media and even during ordinary social interactions to attempt to bias the decisions of others. However, not all positive stimuli are equally influential. In fact, human smiling facial expressions and images of cute animals bias decisions more than food [66, 67]. Furthermore, there is a recognition bias for information consistent with the physical attractiveness stereotype [68].
\nRecent evidence from brain damaged patients has been interpreted as suggesting that the proper recognition of both negative and positive facial expressions relies on the right hemisphere, and that the left hemisphere produces a default state resulting in a bias towards evaluating expressions as happy [69]. The recent report commenting that the activation of the left dorso-lateral prefrontal cortex favors the memory retrieval of positive emotional information [70] additionally supports this hemispheric disquisition. These findings lead to the conclusion that the positive bias not only includes the recognition process but also the memory and its retrieval, functionally involving several brain neural structures.
\nWith respect to the latter topic to consider -the possible cross-modal effect that time-related auditory and visual stimuli have on cognitive processing- recent studies have found, using different auditory-visual distraction paradigms, that task-irrelevant novel sounds preceding visual targets cause behavioral distraction in adults as reflected by increased reaction times to the visual target preceded by novel sounds when compared to those preceded by standard sounds [71].
\nRegarding this issue, San Miguel and colleagues [72] have proposed that (together with other factors) attention task demands and the temporal position of the novel relative to the encoding or retrieval of the task-related visual information influences whether a novel stimulus causes distraction or facilitation. In fact, they reported a reduced distraction under high memory load [73]. On the other hand, Muller-Gass & Schröger [74] studied whether the distraction effect is modulated by the difficulty of the auditory task. They found that the distraction effect increased while rising memory load task demands, but not while increasing its perceptual difficulty. Interpreting these results together it could be possible to assume that channel separation between task-relevant information and task-irrelevant distracting information has an interactive effect with task demands in determining the magnitude of auditory distraction. Therefore, when channel separation is possible distraction increases, as it occurred in the experiment conducted by San Miguel and colleagues [73], and distraction decreases when processing information in both auditory and visual channels concur. In the present study, we used auditory irrelevant stimuli preceding the performance of a highly cognitive demanding WM visual task, thus it could strengthen the potential impact of the attentional capture elicited by the significant sounds and its consequences on subsequent behavioral task-performance.
\nTwo main effects can be inferred from the ERP data; 1) visual ERP components reach significantly minor voltage amplitude when there are none preceding auditory stimuli in comparison with conditions in which they are present, 2) When the auditory irrelevant stimuli had an emotional content, there is a discernible decrease in the voltage amplitude of the ERP components which appears very early in the processing stream.
\nVoltage increases are usually interpreted as signs of greater neural recruitment, which is commonly seen in more novel tasks or ones that are more difficult [75]. Other possible explanations for the amplifying effect that task-preceding irrelevant distractors impinge on the ERP voltage magnitudes was postulated by Nataanen and colleagues in 1982 [76]. These authors proposed that deviant stimulus elicit two overlapping sequences of brain events: exogenous and endogenous. They described the former as an earlier automatic and inflexible set of brain processes that might provide a central-level stimulus to the latter. In addition, they suggest that there is a subsequent endogenous set of brain waves regarded as a sign of stimulus deviance.
\nIn the same logic, we expected to obtain the overlapped effects of the neural state triggered by the auditory stimuli and that necessary to fulfill task demands. Accordingly, the auditory stimuli processing could either distract neural resources from task performance leading to poorer achievements or deploy additional resources thus improving task performance. The present results favored the latter conjecture.
\nOn the other hand, one important point to elucidate resides on the time in which auditory distracting stimuli influence the visual ERP. The simplest assumption might be that any stimulus preceding the task onset should only influence the ERP corresponding to the beginning of the task due to an earlier processing closure related to the task irrelevance of the former stimulus. However, the present results might suggest that the processing closure of the auditory relevant stimuli could take longer than expected, probably due to the different sensory modality in which task-irrelevant and task-relevant stimuli are delivered.
\nIn general, the N170 component has been interpreted as a hallmark of visual orthographic specialization [77, 78] that may reflect increased visual processing expertise [79], most likely in pre-lexical orthographic processing [80]. The present results seem to correspond well to previously reported findings on the N170 component, where source localization and imaging studies have shown that this early stage of perception processing occurs in the fusiform gyrus and is lateralized depending upon the nature of the stimuli (left side for words; right side for pictures; 81,82]. Accordingly, the component N170 was lateralized at the left side, suggesting that experimental manipulations with the visual words might be performed in a sub-lexical perceptual processing level.
\nThe vertex-positive potential is an ERP waveform that has been described as a positive counterpart at centro-frontal sites of the N170 component. The entire N170/VPP complex has been accounted for by two dipolar sources located in the lateral inferior occipital cortex/posterior fusiform gyrus [82]. These authors postulated that early processes in object recognition respond to category-specific visual information, and are associated with strong lateralization and orientation bias. In addition, it is very probably that differences between N170 and VPP effects observed in ERP studies could be accounted for by differences in reference methodology [83].
\nIn the present experiment the VPP waveform showed greater amplitude at fronto-central regions in the trials preceded by auditory stimuli, whereas its amplitude decreased when the distractors had an emotional content. Despite this component is usually related with configurational information processing more than with emotional processing, the voltage decrement observed in trials preceded by emotional words might depict the amount of resources engaged in the processing of irrelevant stimuli but needed for the concurrent task performance.
\nA component named N2b, one that exhibits peaks later than 250 ms in adults, has been reported during performance of category comparison tasks [84, 85]. Experimental evidence suggests that while the N400 component is a specific marker of semantic incongruity, N2b represents a general correlate of inconsistencies in the detection process, or “conflicts” [85] between representations of task-relevant stimuli features [84]. Both components could fit the explanation for the slight negativity subsequent to the P2 like component observed in the present experiment. However, due to its latency, N400 waveform seems to be more likely to occur in the present conditions.
\nIn our experiment the visual word had to be read and further manipulated in working memory to fulfill the task requirements. The N400 like component observed might be depicting the link between the steps in which visual descriptive information of words is first encoded in semantic memory and subsequently visualized via the network for object working memory [86]. Alternatively, it could depict the timing of the effect resemble brain responses linked to engagement of working memory resources, as it was interpreted recently by Wlotko and Federmeier [87] while evaluating the influence of contextual information on semantic processing. The differences between conditions preceded by auditory stimuli -emotional versus neutral- seem to additionally address the contextual influence on working memory processing.
\nConjunctively, behavioral and electrophysiological results suggest that when verbal distractors precede the beginning of a high demanding verbal WM task, its performance is influenced by the characteristics of the distractors, irrespective of whether they appear in different sensory modalities.
\nIn the present study, a “positivity offset” was confirmed, where positive irrelevant stimuli interfered with task performance. It occurred despite the temporal shift between the appearance of distractors and task-relevant stimuli, as well as, the different sensory modality in which they were both delivered. This could be probably explained as part of the competing effect between irrelevant and relevant stimuli for processing cross-modal common resources.
\nEven though the topic concerning environmental influences on cognitive processing remains incompletely elucidated, we hope that this work could contribute to the understanding of these important relationships. In fact, increasing experimental evidence on the topic suggest that more attention will be paid in the future to the interaction between contextual environment and cognitive processing demands, due to the general idea that verbal positive material could help to process concurrent information, when it seems that exactly the opposite occurs.
\nIn a more general context, the present results should be interpreted within the extensive framework of emotion-cognitive processing relationships. The multisensory continuous assessment of the environment carried on by the central executive systems is constantly challenged by environmental demands, while its response capacity is limited by the amount of available processing resources. Fortunately, this neurofunctional dynamic seems to run asymmetric, in which the intrinsic relevance of certain stimuli (e.g. faces, words, and emotional stimuli) benefit from a special cognitive treatment.
\nThe authors are grateful to Psic. Vanessa Ruiz-Stovel for her revision of the text and useful comments.
\nNatural killer (NK) cells represent a highly specialized subpopulation of lymphocytes that are part of the innate immune system, whose functions vary according to the microenvironment. NK cells are involved in the early defense against foreign cells or own cells subjected to some stress (bacterial infection, viral or tumor transformation) through the recruitment of neutrophils, macrophages, dendritic cells, or B/T lymphocytes. They induce an effective adaptive response; regulate, directly or indirectly, the activity of antigen-presenting cells (APCs); and activate T lymphocytes through the natural cytotoxic activity that characterizes them or through the production of cytokines and chemokines that generate an inflammatory environment [1, 2].
\nNK cells play an important role in the surveillance and suppression of tumor cells; despite the significant advances that have been reached in the last decades, it is still unknown if there is a direct relationship among the population dynamics, functionality, and the phenotype of these cells. Its role in the establishment and development of malignant hematological disorders such as acute lymphoblastic leukemia (ALL), a disease characterized by the uncontrolled proliferation of B or T lymphoid precursors, is still unknown.
\nNK cells, although they are larger and present granules in their cytoplasm, morphologically are indistinguishable from the other lymphocytes. According to different authors, they comprise from 5 to 15% [3], 20% [2, 4], or even 25% [5] of total peripheral blood mononuclear cells and are derived from a CD34+ hematopoietic progenitor, as are dendritic cells (DC) and B and T lymphocytes [6].
\nNK cells are phenotypically defined by the expression of CD56 (neural cell adhesion molecule (NCAM) and CD16a (also known as Fcγ-RIIIA), but not CD3 and CD19, which are molecules of T and B lymphocytes, respectively [7, 8]. For a long time, they were considered as the only population of non-B or T lymphocytes. It is currently accepted that NK cells are within a subgroup of the so-called innate lymphoid cells (ILCs), whose subpopulations are differentiated according to the immunophenotype, the profile of cytokines they produce, and the transcription factors they possess [9, 10].
\nThe NK cells were classified in group 1 of the ILCs (ILC1) due to their ability to produce INF-γ, but not cytokines such as IL-4, IL-5, IL-9, IL-13, IL-17, or IL-22, characteristic of the ILC2 and ILC3 groups, respectively [9, 11, 12]. Even within the same subgroup, they differ by having cytotoxic capacity and selectively expressing the eomesodermin (EOMES) transcription factor of other ILC non-NK that also produce INF-γ [13].
\nNK cells maintain a pro-inflammatory environment through the release of cytokines and recruit cells of the immune system to combat infectious agents through the release of chemokines [14] and regulate the activity of dendritic cells or activated lymphocytes [1]; they are in charge of antitumor surveillance and tolerance to healthy own cells, which conditions the rejection of transplants [15] among other functions.
\nIn recent years, it has been reported that in addition to NK cytotoxic or regulatory NK cells, there are memory NK cells [16, 17] and NK cooperators, which secrete Th1-type cytokines (NK1) and Th2 (NK2) [18]. Even, NK cells are similar to antigen-presenting cells [19, 20], although this is in controversy.
\nAccording to what was compiled by Huntington et al., NK cell precursors (NKPs) originate mainly in the bone marrow from hematopoietic precursor cells (HSCs), although they can also do so in organs such as the thymus from early lymphoid progenitor (ELP). These NKPs can mature into competent NK cells in the bone marrow or other organs, such as the liver, spleen, thymus, and lymphoid nodules, to finally enter to the circulation [21]. They migrate to other sites such as the lung, liver, mucous membranes and skin, uterus, pancreas, joints, and central nervous system (CNS), where they can exhibit unique characteristics ranging from the increase or decrease of the expression of activation receptors or effector cytotoxic molecules to the modulation of resident immune cells (Figure 1) [22].
\nOrigin and distribution of NK cells in humans. The precursors of NK cell precursor (NKP) can originate from hematopoietic progenitor cells (HSC) in the bone marrow or from early lymphoid progenitor (ELP). NK cells mature mainly in the bone marrow, although the immature NKP and NK (iNK) can recirculate among the liver, spleen, and lymphoid nodes as alternative maturation sites. Mature NK cells (mNK) that leave the bone marrow reach different organs through blood circulation where they reside and modify their phenotypic and functional characteristics.
According to the expression of CD56 (NCAM), NK cells can be divided into two subpopulations: NKDim and NKBright. However, according to the relative expression of the CD56 and CD16 (FcγRIIIa) markers, their functionality, and their distribution in peripheral blood or lymphoid organs, it is possible to differentiate five subpopulations of mature NK cells (Figure 2).
\nSubpopulations of NK cells in peripheral blood based on the relative expression of CD56 and CD16. (1) CD56Bright CD16Neg, recognized for its immunoregulatory activity, represents between 50 and 70% of the CD56Bright population; (2) CD56Bright CD16Dim represent between 30 and 50% of the CD56Bright population; (3) CD56Dim CD16Neg; (4) CD56Dim CD16Bright is recognized for its cytotoxic activity; and (5) CD56Neg CD16Bright whose function is still unknown. Modified from [23].
The NKBright populations, also known as NK regulators, comprise about 10% of total peripheral blood NK cells. From these, about 50–70% have a [CD56High CD16Neg] phenotype and 30–50% a [CD56High/CD16Low] phenotype [23]; they are mainly characterized by their poor cytotoxic capacity and their high capacity to secrete several types of post-activation cytokines, mainly INF-γ but also TNF-β, IL-5, IL-10, and IL-13 [7, 8] and constitutively some chemokines such as MIP-1α, MIP-1β, and RANTES [24]. They also have the ability to proliferate in culture when exposed to low doses of IL-2 (picomoles) compared to the cytotoxic NK cells, which does not show an evident proliferation under the same conditions [25]. The NKBright cells [CD56High CD16Neg] are assigned an exclusively regulatory function, since their cytotoxic activity is poor and their genetic profile is directed mainly to the production of cytokines and not to the cytotoxic activity, in comparison with the NKDim, whereas the NKBright subpopulation [CD56High CD16Low] is considered more as a transition phenotype [26]; because despite having the same characteristics of the previous phenotype, it has a lower rate of cell division when stimulated with IL-2 and does not change its activity even with ligands for c-KIT [27]. It exhibits cytotoxic activity [28], and it has also been seen that it represents the highest percentage of NK cells in circulation in bone marrow transplants, until its normalization around the fourth month [29, 30]. NKBright cells are usually not found in peripheral blood, bone marrow, and spleen as they are mainly distributed in secondary lymphoid nodules (parafollicular zone of T cells) [31] and tonsils [32].
\nOn the other hand, the NKDim population represents around 90% of peripheral blood NK cells; they have a phenotype [CD56Low CD16Neg] whose main function has not been well established [23] and a main phenotype [CD56Low CD16High] that exhibits potent cytotoxic activity. Although they are generally poor producers of cytokines [7, 8, 33], they tend to predominate in the spleen, peripheral blood, and bone marrow [32, 34].
\nIt is important to clarify that the behavior of each subpopulation, in terms of post-activation secretion of cytokines and chemokines, will depend largely on the stimuli they receive either by recognizing target cells (tumor or transformed) or responding to exogenous cytokines.
\nCompared with NKDim cells, NKBright cells produce more TNF-α and INF-γ after activation with PMA/ionomycin [35] or exogenous cytokines such as IL-12, IL-15, or IL-18, alone or in combination [8].
\nOn the contrary, when it comes to a response to the recognition of target cells, NKDim cells significantly increase their production of cytokines and chemokines compared to NKBright, such as MCP-1 (CCL2), IL-8 (CXCL8), IP-10 (CXCL10), soluble IL-2Rα (CD25), GM-CSF, and IL-5 and low levels of IL-1β, IL-6, IL-7, IL-10, IL-12p40, IFN-α, and MIG (CXCL9). In addition, it increases the production of chemokines such as MIP-1α (CCL3), MIP-1β (CCL4), and RANTES (CCL5) that produce constitutively [24].
\nThe cytotoxic activity exhibited by NK cells does not require prior sensitization to kill their target cells, since it is not dependent on the presentation of a specific antigen as in the case of CD8+ T cells [7, 36] and can be mediated through membranolitic and/or apoptotic mechanisms (Figure 3).
\nRecognition and elimination of abnormal cells by NK cells. NK cells possess the ability to discriminate normal cells of tumor or transformed cells by detecting alterations at the HLA-I level; the target cells are eliminated by membranolitic and/or apoptotic mechanisms.
The membranolitic mechanisms include the production of perforins, enzymes that when integrated into the cell membrane form a pore that allows water to enter and cause osmotic lysis [37]. In the past, it was believed that both NKBright and NKDim cells had similar levels of perforins [38]; however, more recent studies by flow cytometry indicate that NKDim cells have at least 10 times more perforins than NKBright ones [35].
\nRegarding apoptotic mechanisms, these can induce the death of the target cell through complex mechanisms that involve both death-inducing proteins and specific ligand-receptor interactions through one of the following routes:
\nGranzymes are proteins capable of activating the apoptosis program [39] following two mechanisms. The first does not depend on the activity of caspase proteins and is mediated mainly by granzyme A, and this fraction is single-stranded DNA (ssDNA) and interferes in the repair of genetic material without producing cell lysis [40, 41], while the second promotes the activity of caspase proteins and is mediated mainly by granzyme B [42].
\nThe NK cell presents granzymes A, B, K, and M; NKDim cells present a high expression of granzymes A and B, whereas NKBright cells mainly express granzyme K [35, 43]. There are reports that NK cells express almost exclusively granzyme M; this enzyme is capable of mediating cell death independent of the activation of caspase proteins and in the presence of perforins, without fractionating DNA or producing changes in mitochondria [44].
\nIn mice, deficient in granzymes A/B and/or perforins, it has been seen that there is uncontrolled growth of solid tumors, which suggests that these enzymes play an important role in the immunosurveillance of tumor cells mediated by NK cells [45].
\nThey include Fas ligands [FasL (CD95L)-Fas (CD95)] and/or the ligand that induces apoptosis related to tumor necrosis factor α (TRAIL) [46, 47].
\nNK cells express FcγRIIC/CD32c [48] and FcγRIIIA/CD16a [34]. These receptors interact with opsonized target cells, through the Fc regions of the antibodies, which combined with cellular antigens that cause the death of the target cell [49]. To through of mechanisms that involve the release of cytotoxic granules (perforin-granzyme), or by stimulation of apoptosis through of TNF-related apoptosis-inducing ligand (TRAIL) and/or by release of pro-inflammatory cytokines that promote the activity of other cells [50].
\nNKDim cells with [CD56Low CD16High] phenotype direct this mechanism in comparison with NKBright cells. Although it has been seen that the subpopulation with [CD56High CD16Low] phenotype exhibits low cytotoxic activity [51], NKDim cells [CD56Low CD16Neg] show a higher antitumor activity against cell lines (natural cytotoxicity) than other subpopulations [52]. This is supported by other studies where it is reported that NKDim cells [CD56Low CD16High] lose the expression of CD16 and increase the expression of CD107a (a degranulation marker), through a disintegrin and a metalloprotease-17 (ADAM-17), to become [CD56Low CD16Neg] with high cytotoxic capacity [53].
\nThe role of the [CD56Neg CD16High] subpopulation is still not clearly defined. It is known that it is found in a low frequency in healthy individuals. It does not express surface molecules of other lymphoid lineages and that in chronic viral diseases, such as the human immunodeficiency virus (HIV). It presents changes in the level of expression of their activity receptors, characterized by the increase in the expression of inhibitory receptors and the decrease of natural cytotoxicity receptors (NCRs), together with other effector molecules that are hardly observed in healthy people [54, 55, 56].
\nIt is considered that the [CD56Neg CD16High] subpopulation is dysfunctional in terms of its lytic and antiviral activity, although it retains the ability to produce pro-inflammatory chemokines [54, 55, 56].
\nZulu et al. demonstrated that the HIV induces the expansion of the negative CD56 population of NK cells through the upregulation of NKG2C receptors and the negative regulation of Siglec-7, NKG2A, and CD57 receptors [57].
\nNK cells have signals through a wide variety of receptors that allow them to respond to different types of stimuli and grant great flexibility when exercising their effector and/or cytotoxic function.
\nThe function of the NK cell is given by a complex collection of receptors that act in a synergistic way to recognize, regulate, or amplify the response according to the microenvironment. Thus highlighting the pattern recognition receptors (PRRs), such as Toll-like receptors or natural cytotoxicity receptors, and inhibitory killing receptors (iNKRs), such as receptors that are activated during early response to pathogens, cells transformed by virus or tumor cells [58].
\nPRRs are a family of innate immune response receptors that recognize evolutionarily conserved microbial products whose activation favors the production of pro-inflammatory cytokines. Within the PRR group, the TLRs are the most studied, although they are not the only ones; there are also the NOD-like receptors (NLRs) and the retinoid acid-inducible gene I (RIG-I)-like receptors (RLRs) [59].
\nNK cells express innate immune response receptors, such as NOD2, NLRP3, TLR3, TLR7, and TLR9, and promote the production of inflammatory cytokines and chemokines that are capable of amplifying the immune response [60]. The modulation of these cells through their innate immune response receptors, mainly via TLR, has gained interest and represents a promising therapeutic alternative against conditions such as cancer. Since there have been studies for a long time that support the possibility of its use, it has been observed that when ODNs (ligands of TLR9) are intraperitoneally administered in lymphoma murine models, an effective elimination of tumor cells occurs in 80% of cases [61].
\nToll-like receptors are among the most important group of pattern recognition receptors, since they orchestrate a wide variety of activities related to the immune response.
\nThese receptors recognize a wide variety of molecules evolutionarily conserved, associated with microorganisms, such as lipopolysaccharides, lipoproteins, mycolic acids, non-methylated DNA, and double-stranded RNA, generically known as pathogen-associated molecular patterns [62, 63, 64]. TLRs also recognize endogenous molecules called damage-associated molecular patterns, which originate from damaged cells [65] or are products of altered metabolism of transformed cells in conditions such as cancer [66, 67] and autoimmune diseases [67, 68, 69, 70] or associated with chronic inflammation [71, 72]. They play an important role in the evolution of these conditions.
\nStructurally, TLRs are type I integral glycoproteins that present an extracellular domain with leucine-rich repeats (LRRs) that are responsible for binding and discriminating ligands (PAMPs or DAMPS) present in the cellular microenvironment. They have a transmembrane domain and an intracellular Toll/interleukin (IL)-1 receptor (TIR) domain that triggers the signaling cascade via MyD88/TRIF and is highly conserved among each subfamily of TLRs [73].
\nThere are 13 TLRs described in mammals, and 10 are found at the protein level in humans and differ according to their cellular localization and to the different PAMPs/DAMPs to which they respond. TLR11 in humans is a pseudogene, so it is not expressed [74].
\nThe TLRs that are found mainly in the cell membrane are TLRs 1, 2, 4, 5, and 6. They sense structural components of bacteria, fungi, helminthes, or protozoa, whereas TLRs that are mainly found in intracellular compartments, such as TLRs 3, 7, 8, and 9, sense nucleic acids of viral and/or bacterial origin [73, 75] (Figure 4).
\nToll-like receptors and their ligands. TLRs are transmembrane proteins of a glycoprotein nature that possess the ability to sense highly conserved microorganism molecules known as pathogen-associated molecular patterns (PAMPs), such as flagellin, LPS, or genetic material (ssDNA, ssRNA, dsDNA, dsRNA). In humans, 10 of the 13 TLRs present in mammals have been detected [84].
The stimulation of the TLRs is capable of initiating an immune response to various stimuli on its own, as well as of controlling the adaptive response through the inflammatory process with the production of pro-inflammatory cytokines (IL-1β, IL-6, TNF-α), chemokines (IL-8, MCP-1) [76]; defensins [77]; type I interferons [78]; co-stimulation and MHC molecules [79]. The union between the different types of immune responses through the TLRs takes as a classic example the dendritic cells. They inspect their environment through the TLRs [80]; and once they detect a ligand (bacterial product, viral or stress protein), increase the expression of co-stimulatory molecules capable of stimulating T naive cells [81] and polarizes the adaptive immune response toward Th1 or Th2 profiles [82].
\nThe cellular response through direct stimulation with TLR ligands will depend largely on the type of lineage in question. The information that is reported about activity and expression in NK cells is relatively new, and it is more associated with innate antibacterial or antiviral immune response [83], but not in cancer.
\nThe expression profile of TLRs in NK cells was initially limited to the detection of mRNA. However, the results do not always reflect the expression of the protein since it is difficult to identify the receptors in the NK cell.
\nNK cells express most of the human TLRs reported to date, although the detection and level of mRNA expression of each receptor vary depending on the author. There are authors who indicate that NK cells express high levels of TLR1, followed by TLR2, TLR3, TLR5, TLR6, and low levels of TLR4 [85, 86]. Other authors agree that TLR2 and TLR3 have greater expression, followed by TLR5 and TLR6; in those studies, TLR1 mRNA was not quantified [87, 88, 89]. On the other hand, TLR7 [85, 89, 90] and TLR10 [83, 86] present levels so low that they are practically undetectable.
\nThere is a controversy about whether or not NK cells express TLR8 [86, 87, 89] and TLR9 [86, 88], although some authors point out that the cells constitutively express mRNA of all TLRs [85, 91, 92].
\nNK cells have higher levels of TLR3 mRNA than any other peripheral blood mononuclear cell, such as monocytes, B and T lymphocytes, or plasmacytoid dendritic cells [85].
\nThrough techniques such as flow cytometry, Western blot, and immunoprecipitation, it is possible to know that NK cells of healthy people have a defined TLR expression profile (Table 1) and the expression of receptors is independent of their activation state [58].
\nTLR | \nmRNA1 | \nProtein | \nDetection method | \n
---|---|---|---|
Presence | \n|||
1 | \nVery high | \nYes | \nFlow cytometry [97] Western blot [97] | \n
2 | \nHigh/moderate | \nYes3 | \nDirect activation of the TLR2-/MyD88-dependent pathway [96] Flow cytometry [95, 96, 97] Western blot | \n
3 | \nHigh/moderate | \nYes | \nFlow cytometry [93, 94] Western blot [94] | \n
4 | \nLow | \nYes4 | \nFlow cytometry [94, 95, 99] | \n
5 | \nHigh/moderate | \nYes5 | \nS/R | \n
6 | \nHigh/moderate | \nYes | \nFlow cytometry and Western blot [97] \n | \n
7 | \nVery low/undetectable | \nYes | \nFlow cytometry [93, 94] Western blot [94] | \n
8 | \nLow2 | \nYes | \nFlow cytometry [94] Western blot [90, 94] | \n
9 | \nLow2 | \nYes | \nFlow cytometry [93, 95, 100] Western blot [100] | \n
10 | \nVery low/undetectable | \nN/R | \nN/R | \n
Expression of TLRs in human natural killer cells.
The levels of relative expression are given according to what was reported by [85, 91] and refer to the comparison of expression among the 10 TLRs.
There is a controversy whether or not they express mRNA of these TLRs, since some reports indicate that it was not possible to detect it.
In previous studies, TLR2 could not be detected by flow cytometry or by immunoprecipitation.
More recent studies indicate that it is expressed mainly as intracellular [95, 99].
No reports were found indicating the presence of TLR5; however it is inferred that it is present as it responds specifically to flagellin [88, 101, 102], a molecule that it is only recognized through this receptor.
N/R, not reported.
In addition, there are variations in the level of TLR expression within the same subpopulations of NK cells. It is accepted that both NKBright and NKDim exhibit a similar mRNA profile of TLRs, although it is not always reflected at the protein level and there is a great controversy regarding the distribution and presence of some of these receptors in both subpopulations, especially TLR2, TLR4, and TLR3.
\nTLR2 and TLR4 are mainly distributed on the cell surface, whereas TLR3 is generally found in intracellular vesicles [75]; however, it has been seen that in NK cells, TLR3 is expressed both within [93] and on the cell surface [94]. There are publications reporting that TLR2 and TLR4 exhibit a marked intracellular distribution [95], although other authors indicate otherwise [96, 97].
\nThe relative amount of some TLRs may vary according to the phenotype (Dim or Bright), although expression levels appear to be higher in cells with regulatory phenotype [89], which suggests that the type of response could be conditioned to promote a cytotoxic or immunomodulatory response when using one ligand or another in TLR activation assays (Table 2).
\nTLR | \nCellular localization | \nPopulation distribution | \n
---|---|---|
1 | \nExtracellular [97] | \nNKBright > NKDim [97] | \n
2 | \nExtracellular [96, 97] and intracellular [95] | \nNKBright > NKDim [97] | \n
3 | \nIntracellular [93] and extracellular1 [94] | \nN/R | \n
4 | \nExtracellular [94] and intracellular2 [95, 99] | \nNKBright < NKDim [99] NKBright = NKDim [95] | \n
5 | \nN/R | \nN/R | \n
6 | \nExtracellular [97] | \nNKBright > NKDim [97] | \n
7 | \nIntracellular [93, 94] | \nN/R | \n
8 | \nIntracellular [94] | \nN/R4 | \n
9 | \nMainly intracellular3 [93, 95, 100] | \nNKBright = NKDim5 [95] | \n
10 | \nN/R | \nN/R | \n
Localization and differential distribution of TLRs in human natural killer cells.
It was found that both, in cell lines (NKL, NK92, and YT) and in NK of peripheral blood, TLR3 is expressed on the surface [94].
Studies that are more recent indicate that it is mainly expressed as intracellular [95, 99].
TLR9 expression exists in plasma membrane, but it is quite low compared to intracellular expression.
There are no studies that determine whether there is differential expression, although it has been seen that NKBright cells are better activated with ssRNA40 than NKDim cells, suggesting that the latter have a lower expression of TLR8.
In other studies, it seems that NKDim cells express more TLR9 than NKBright cells and its expression conditions the response to ligands of this TLR [100].
N/R, not reported.
It has been seen that NKBright cells express more TLR1, TLR2, and TLR6 than NKDim [97], although other studies report that less than 1% of total NK cells express these three receptors [98].
\nNKDim cells can express, under normal conditions, more TLR4 than NKBright cells [99] although other authors seem to find no differences in the expression in TLR2, TLR4 [95], and TLR9 [95, 100].
\nThere is no information about whether there is differential expression of TLRs 3, 5, 7, or 8, and the distribution pattern of TLR5 is not known. However, it is inferred that NK cells express it, since they respond to flagellin and there are several studies that demonstrate it [88, 101, 102]. To date there are no reports about the presence, distribution, or role of TLR10 in NK cells.
\nThe therapeutic use of TLR ligands in the modulation of NK cells against cancer, especially in malignant hematological disorders such as leukemia, is an interesting alternative for the treatment of this type of diseases, since there are reports that reveal their therapeutic use as potential antitumor agents and as adjuvants in vaccines and other therapeutic modalities [103]. It is currently the subject of an extensive review by several research groups [104, 105].
\nIn this chapter, we included the overview of NK cells, their population diversification and role in the immune response, and their expression and role of TLRs.
\nThe authors declare that there is no conflict of interest.
We thank doctors Jacques Zimmer, MD, PhD, and Sankar Ghosh, PhD, for allowing us to use some of their figures, Figures 2 and 4, in this chapter of the book.
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