Switching Between Internal Attention And External Attention A Spatiotemporal Analysis Of ERP

ObjectiveFunctional neuroimaging studies have found that brain had two sets of information processing system for the external environment and the internal affairs respectively. They can also be referred as the external attention system and the internal attention system by the information source. The former mainly included the dorsal attention network (DNA) and the ventral attention network (VAN), while the latter mainly includes the default mode network (DMN), also referred as the resting-state networks (RSN). Some researches suggested that the activation level of the external attention network and that of the internal attention network was anti-correlative, but there were also evidences shown that both can be activated when mind wanders. A large amount of functional magnetic resonance imaging (fMRI) studies had shown that both the prefrontal and the parietal regions were more active during the preparation stage under condition of the task switching than that of the task repetition condition. Furthermore, some studies found that there may be other function neural networks involved switching between the two networks, involving the core network, the salience network (SN), the attentional gateway system and so on. However, due to the low temporal resolution of fMRI, the neural mechanism of dynamic evolution of the initialization and switching between the external and internal attention networks is still not clear. The mismatch negativity (MMN) obtained using auditory oddball paradigm gets more and more clinical application. The optimal MMN recording conditions were under the passive condition that the participant ignores the auditory stimuli in order to eliminate other cognitive components of event-related potentials (ERP) elicited during the active attention. For construct a passive condition, some visual distraction tasks were used generally, more simple passive auditory oddball paradigm still needs further exploration. Since each subject was instructed to focus on his/her body information during a breath-counting task, it reflects the internal attention function and it may be superior to mind wandering or the visual distraction tasks for clinical applicationIn order to investigate the regulatory mechanism of the internal and external attention networks as well as the differences between the passive and the active auditory processing, we have combined the internal and external attention switching tasks with the statistical parametric mapping (SPM) of spatiotemporal pattern of ERP. We have expected that it would reveal dynamic mechanism between the external and internal attention networks and provide us empirical basis for clinical application of the passive auditory ERP with breath counting as a distraction task.MethodsTwenty college students (10females) aged from24to28years old (mean age25.75, SD1.07years) participated in the experiment. They were all right handed without hearing, neurological and psychiatric system disease. Subjects were informed consent to participate in the experiment and received remuneration.The auditory oddball paradigm was composed of pure sounds of800Hz for the standard stimuli (80%) and1500Hz for the deviant stimuli (20%). Each sound lasted100ms and Inter-stimulus intervals randomly varied between1400ms,1500ms and1600ms. Deviant stimuli presentation was pseudo-random to ensure there were never two deviant stimuli presented successively. Auditory stimuli were played through the loudspeaker that built-in computer located at1.0m distance in front.In a quiet and dark room, participants sat in a comfortable position with a game response pad in hands. We asked them to keep their eyes closed during the recording session. According to different task cues (sound words "exhale" or "sound"), the participants executed breath-counting task (or called internal attention task/passive oddball task) or auditory attention task (or called external attention task/active oddball task), and pressed keypad buttons with their index fingers as soon as possible. In the breath-counting task, participants were required to focus on theirs breathing and were instructed to ignore the pure tone stimulation as far as possible. Based on the breath feeling of each subject, either at100%inspiration or at100%expiratory phase, one needed to press corresponding key respectively. Due to breath continued alternation, left and right buttons were pressed in turn until the next task switching clue. In the auditory attention task, participants were required to focus on the auditory stimuli of external presentation and were instructed to ignore their breath as far as possible. According to presentation was standard or deviant stimuli, they needed to press corresponding key respectively and perform this task until the next task switching cue appear. Two kinds of task cues presentation were pseudo-random to ensure there were never more than three same switching cues presented successively. The left and right buttons of the two types of tasks were counterbalance across subjects. The experiment was divided into three blocks and each block of each cue had twenty-five. Two breaks of30s were arranged between blocks. The whole experiment lasted for55min.The EEG was recorded using an ERP system developed in our lab with the bandwidth of [0.5,100](Hz) and the impedance between scalp and electrode were below10kΩ. The nineteen recording electrode (FP1, FP2, F3, F4, C3, C4, P3, P4,01,02, F7, F8, T3, T4, T5, T6, Fz, Cz, Pz) were installed according to the international10-20system standard lead in which the reference electrode were linked to the bilateral earlobe and grounding electrode was linked to the forehead point FPz. EEG analysis time was from100ms before to1000ms after cues or stimulus onset. Principal component analysis was applied to correct eye movement artifacts and artifact detection threshold was set to70μV. All event-related EEG segments after artifact correction were taken into the average ERP.Behavioral data was carried out to a paired, two-sided t-test on auditory attention task using SPSS13.0, while the switching cost were calculated of first three reaction both in the breath-counting task and auditory attention task. The ERP data of each channel was entered into two kinds of two-way ANOVA of repeated-measures: attention state (internal/external) x task type (switch/maintain) and stimuli probability (high/low) xattention task (passive/active) separately. Further, paired t-tests were performed under different conditions. Statistical parametric mapping [SPM(F) or SPM(t)] was obtained from interpolation calculated by each channel’s F-values or t-values. The significant level was0.05.ResultsBehavior resultsIn the internal attention task, the switching costs (SW) of the fist three average response time interval (RIT) were gradually increased [SW1(-316.00+316.00) ms<SW2(-60.88+234.81) for ms<SW3ms (337.01+200.51)]. Making the paired t test (switching-maintain) for each RIT, there were significant differences between only the first RIT (t=5.05, p=5.05) and no between the second and third (t (19)=-1.13, p=0.213; t (19)=1.33, p=0.200). In the external attention task, the switching costs of the fist three average reaction time (RT) were gradually decreased [SW1(94.35±79.27) ms> SW2(33.76±59.62) ms> SW3(14.66±43.06) ms]. Making the pair t test (switching-maintain) for each RT, there were significant differences between the first and second RT (t (19)=5.32,p=000; t (19)=2.53, p=0.020) and no between the third RT(t(19)=1.52,p=0.144). Overall, in auditory attention task, the deviant stimuli showed longer reaction time [(511.3±79.8) ms vs (437.0±99.6) ms, P<0.001] and lower accuracy [(90.8±5.6)%vs (97.0±1.9)%, P<0.001] than the standard stimuli.Spatiotemporal patterns of SPM(F)For the two-way (attention state:internal/external)×(task type: switch/maintain) ANOVA of repeated-measures, the main effect of attention state ordinal activated frontal system (100～200ms), cingulo-opercular network (CON)(225～250ms), frontoparietal network (FPN)(275～400ms), CON and ventral attention network (VAN)(500～650ms), the main effect of task type ordinal activated right prefrontal (150～500ms), CON and VAN (400～500ms), insular and temporoparietal system (550～850ms). The interaction effect ordinal appeared left parietotemporal system and VAN (175～500ms), bilateral frontal, especially in the left (550～850ms). Further, the paired t test for the each condition detailed the attention and task main effects and revealed that the potential polarity was opposite between internal and external attention.For the two-way (stimuli probability: high/low) x (attention task: passive/active) ANOVA of repeated-measures, main brain areas and periods with statistical significance effects of ERP were listed below. The main effect of probability activated frontal region (125～200ms), frontotemporal region (200～300ms), fronto-parietal and temporal areas.(300～450ms), frontal region (450～650ms), parietal area (650～700ms) and frontoparietal region (700～850ms), the main effect of task activated the left FPN and the right frontal pole(100～150ms), parietal area (175～300ms), central executive network(CEN) and VAN(300-500ms), right temporoparietal region (500～850ms), the interaction effect activated left frontal region (125-175ms), left parietal-occipital cortex (300～550ms), posterior central parietal-occipital regions (700～850ms). The spatiotemporal patterns of SPM(t)(deviant-standard) under passive and active condition respectively revealed that the MMN, P300and slow waves effects were shown both in the two condition and all involved the dorsomedial frontal area. The active MMN effect was distributed in the fronto-parietal regions, while the passive involved the fronto-parietal and temporal areas. The passive slow wave effect in the dorsomedial frontal region showed shorter duration than the active one [(450～550) ms vs.(450-600) ms, P<0.05].ConclusionBehavior results of the longer RT and lower accuracy of the deviant stimuli show a higher degree of automation to perform the high probability task in our experiment. In the internal attention task, the fist and second RIT of switching task is shorter than the maintain task. This is contrary to previous studies. This may be related to the big execution time gap between internal and external attention task switching. Negative switching costs may be influenced by the fast keying frequency of external attention before conversion. In external attention task, the RT of switching task is always longer than maintain task and the SW is decreased with the extension of time.Using task switching paradigm, we study the neural mechanisms between external and internal attention network. We find the fronto-central areas (125～200ms) relates to the switching between internal and external attention during the MMN stage of auditory ERP. This is consistent with both the study of Baldeweg et al. and Sato et al., which presented auditory MMN involves attention switching. In addition, the result that the potential polarity is opposite between internal and external attention coincides with the study of Fox et al., which suggested that the external attention network and the DMN has anti-correlations property. Our studies suggest that gateway system still can be further divided into internal attention and external attention systems, which is different from the gateway hypothesis that at least some regions of rostral PFC are specialized, along a medial-lateral dimension, for differences in requirements for stimulus-oriented or stimulus-independent attending, proposed by Burgess et al.By comparing the dynamic mechanism related neural network processing of auditory oddball stimuli in the internal attention (passive) and external attention (active) conditions reveals that the processing lifetime of the passive deviant stimuli resembles that of the active ones in college students. The repeated activation of the dorsomedial frontal area in different processing stages suggests its process generality. The passive MMN involves more brain areas whereas the passive slow wave is more limitedly distributed. By taking the breath-counting as a distractive task, the passive oddball paradigm together with the spatiotemporal patterns analysis of ERP can provide more information for clinical applications of auditory ERP.