Disentangling the attention network test: behavioral, event related potentials, and neural source analyses

Alejandro Galvao-Carmona, Javier J González-Rosa, Antonio R Hidalgo-Muñoz, Dolores Páramo, María L Benítez, Guillermo Izquierdo, Manuel Vázquez-Marrufo, Alejandro Galvao-Carmona, Javier J González-Rosa, Antonio R Hidalgo-Muñoz, Dolores Páramo, María L Benítez, Guillermo Izquierdo, Manuel Vázquez-Marrufo

Abstract

Background: The study of the attentional system remains a challenge for current neuroscience. The "Attention Network Test" (ANT) was designed to study simultaneously three different attentional networks (alerting, orienting, and executive) based in subtraction of different experimental conditions. However, some studies recommend caution with these calculations due to the interactions between the attentional networks. In particular, it is highly relevant that several interpretations about attentional impairment have arisen from these calculations in diverse pathologies. Event related potentials (ERPs) and neural source analysis can be applied to disentangle the relationships between these attentional networks not specifically shown by behavioral measures.

Results: This study shows that there is a basic level of alerting (tonic alerting) in the no cue (NC) condition, represented by a slow negative trend in the ERP trace prior to the onset of the target stimuli. A progressive increase in the CNV amplitude related to the amount of information provided by the cue conditions is also shown. Neural source analysis reveals specific modulations of the CNV related to a task-related expectancy presented in the NC condition; a late modulation triggered by the central cue (CC) condition and probably representing a generic motor preparation; and an early and late modulation for spatial cue (SC) condition suggesting specific motor and sensory preactivation. Finally, the first component in the information processing of the target stimuli modulated by the interaction between orienting network and the executive system can be represented by N1.

Conclusions: The ANT is useful as a paradigm to study specific attentional mechanisms and their interactions. However, calculation of network effects is based in subtractions with non-comparable experimental conditions, as evidenced by the present data, which can induce misinterpretations in the study of the attentional capacity in human subjects.

Keywords: ANT; CNV; P300; alerting; attention; neural networks; orienting; source analysis.

Figures

Figure 1
Figure 1
Experimental procedure. Possible combinations of sets of cues and targets were six: no cue congruent (NC-C), no cue incongruent (NC-I), central cue congruent (CC-C), central cue incongruent (CC-I), spatial cue congruent (SC-C), and spatial cue incongruent (SC-I). Abbreviation: ms, milliseconds.
Figure 2
Figure 2
The 58 scalp electrodes recorded and sets of 42 electrodes analyzed (in red) for ERPs (CNV, P1, N1, and P3) that were used.
Figure 3
Figure 3
Behavioral results. Mean reaction times (in milliseconds) and accuracy (in percentages) with standard deviations according to cues and targets.
Figure 4
Figure 4
Contingent negative variation modulations at Cz electrode and topographical maps. Abbreviations: ms, milliseconds; μV, microvolts.
Figure 5
Figure 5
CNV component modulation in the no cue condition and electrodes that showed statistical differences (in red) between averaged ERP amplitudes and zero value (t-test against zero) in each of the 10 intervals of 100 ms prior to the onset of the target stimulus analyzed. Abbreviations: ms, milliseconds; μV, microvolts.
Figure 6
Figure 6
P1 and N1 modulations in every cue condition at the PO5 and PO6 electrodes and topographical maps. Abbreviations: ms, milliseconds; μV, microvolts.
Figure 7
Figure 7
ERP modulations at the PO6 electrode in every cue × congruence condition. Abbreviations: ms, milliseconds; μV, microvolts.
Figure 8
Figure 8
(A,B) Cortical activation maps presented in Z scores according to the baseline and showing significant activity (FDR-adjusted p < 0.01). Sources of the CNV effect were estimated in 2 CNV intervals of interest, −500 to −400 ms and −100 to 0 ms, before the target stimulus, which had shown previous ERP differences between experimental conditions during the CNV period. Source reconstructions maps were clipped at 50% (FWHM). (C,D) Cue-conditions effects on the mean time-course of activation in superior parietal lobe (SPL), and supplementary motor area (SMA) elicited during the ANT task for no cue (NC), central cue (CC), and spatial cue (SC) conditions in the 100 ms scoring windows at which statistical analyses were carried out. The data represent the grand-average source waveforms for all subjects, collapsing left and right hemispheres for the selected areas.

References

    1. Benjamini Y., Yekutieli D. (2001). The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188 10.1214/aos/1013699998
    1. Benwell C. S., Harvey M., Thut G. (2014). On the neural origin of pseudoneglect: EEG-correlates of shifts in line bisection performance with manipulation of line length. Neuroimage 86, 370–380 10.1016/j.neuroimage.2013.10.014
    1. Brett M., Johnsrude I. S., Owen A. M. (2002). The problem of functional localization in the human brain. Nat. Rev. Neurosci. 3, 243–249 10.1038/nrn756
    1. Brunia C. H. M. (1993). Waiting in readiness: gating in attention and motor preparation. Psychophysiology 30, 327–339 10.1111/j.1469-8986.1993.tb02054.x
    1. Brunia C. H. M., Van Boxtel G. J. M., Böcker K. B. E. (2012). Negative slow waves as indices of anticipation: the Bereitschaftspotential, the contingent negative variation, and the stimulus-preceding negativity, in The Oxford Handbook of Event-Related Potential Components, eds Luck S. J., Kappenman E. S. (Oxford: Oxford University Press; ), 189–207
    1. Bunzeck N., Schütze H., Düzel E. (2006). Category-specific organization of prefrontal response-facilitation during priming. Neuropsychologia 44, 1765–1776 10.1016/j.neuropsychologia.2006.03.019
    1. Burgess P. W., Dumontheil I., Gilbert S. J. (2007). The gateway hypothesis of rostral prefrontal cortex (area 10) function. Trends Cogn. Sci. 11, 290–298 10.1016/j.tics.2007.05.004
    1. Callejas A., Lupiàñez J., Funes M. J., Tudela P. (2005). Modulations among the alerting, orienting and executive control networks. Exp Brain Res. 167, 27–37 10.1007/s00221-005-2365-z
    1. Chica A. B., Thiebaut de Schotten M., Toba M., Malhotra P., Lupiáñez J., Bartolomeo P. (2012). Attention networks and their interactions after right-hemisphere damage. Cortex 48, 654–663 10.1016/j.cortex.2011.01.009
    1. Corbetta M., Shulman G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 10.1038/nrn755
    1. Coull J. T. (2004). fMRI studies of temporal attention: allocating attention within, or towards, time. Brain Res. Cogn. Brain Res. 21, 216–226 10.1016/j.cogbrainres.2004.02.011
    1. Di Russo F., Martínez A., Sereno M. I., Pitzalis S., Hillyard S. A. (2002). Cortical sources of the early components of the visual evoked potential. Hum. Brain Mapp. 15, 95–111 10.1002/hbm.10010
    1. Duncan C. C., Barry R. J., Connolly J. F., Fisher C., Michie P. T., Näätänen R., et al. (2009). Event-related potentials in clinical research: guidelines for eliciting, recording, and quantifying mismatch negativity, P300, and N400. Clin. Neurophysiol. 120, 1883–1908 10.1016/j.clinph.2009.07.045
    1. Eriksen B. A., Eriksen C. W. (1974). Effects of noise letters upon the identification of a target letter in a nonsearch task. Percept. Psychophys. 16, 143–149 10.3758/BF03203267
    1. Fan J., Kolster R., Ghajar J., Suh M., Knight R. T., Sarkar R., et al. (2007). Response anticipation and response conflict: an event-related potential and functional magnetic resonance imaging study. J. Neurosci. 27, 2272–2282 10.1523/JNEUROSCI.3470-06.2007
    1. Fan J., McCandliss B. D., Fossella J., Flombaum J. I., Posner M. I. (2005). The activation of attentional networks. Neuroimage 26, 471–479 10.1016/j.neuroimage.2005.02.004
    1. Fan J., McCandliss B. D., Sommer T., Raz A., Posner M. I. (2002). Testing the efficiency and independence of attentional networks. J. Cogn. Neurosci. 14, 340–347 10.1162/089892902317361886
    1. Fernández-Duque D., Posner M. I. (1997). Relating the mechanisms of orienting and alerting. Neuropsychologia 35, 477–486 10.1016/S0028-3932(96)00103-0
    1. Fuchs M., Wagner M., Kohler T., Wischmann H. A. (1999). Linear and nonlinear current density reconstructions. J. Clin. Neurophysiol. 16, 267–295
    1. Fuentes L. J., Campoy G. (2008). The time course of alerting effect over orienting in the Attention Network Test. Exp. Brain Res. 185, 667–672 10.1007/s00221-007-1193-8
    1. Fuentes L. J., Fernández P. J., Campoy G., Antequera M. M., García-Sevilla J., Antúnez C. (2010). Attention network functioning in patients with dementia with Lewy bodies and Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 29, 139–145 10.1159/000275672
    1. Gómez C. M., Flores A., Ledesma A. (2007). Fronto-parietal networks activation during the contingent negative variation period. Brain Res. Bull. 73, 40–47 10.1016/j.brainresbull.2007.01.015
    1. Gómez C. M., Marco J., Grau C. (2003). Preparatory visuo-motor cortical network of the contingent negative variation estimated by current density. Neuroimage 20, 216–224 10.1016/S1053-8119(03)00295-7
    1. Gonzalez-Rosa J. J., Vazquez-Marrufo M., Vaquero E., Duque P., Borges M., Gamero M. A., et al. (2006). Differential cognitive impairment for diverse forms of multiple sclerosis. BMC Neurosci. 7:39 10.1186/1471-2202-7-39
    1. Gonzalez-Rosa J. J., Vazquez-Marrufo M., Vaquero E., Duque P., Borges M., Gómez C. M., et al. (2011). Cluster analysis of behavioural and event-related potentials during a contingent negative variation paradigm in remitting-relapsing and benign forms of multiple sclerosis. BMC Neurol. 11:64 10.1186/1471-2377-11-64
    1. Hagen G. F., Gatherwright J. R., Lopez B. A., Polich J. (2006). P3a from visual stimuli: task difficulty effects. Int. J. Psychophysiol. 59, 8–14 10.1016/j.ijpsycho.2005.08.003
    1. Harter M. R., Anllo-Vento L. (1991). Visual-spatial attention: preparation and selection in children and adults, in Event-Related Brain Research (EBG Suppl. 42), eds Brunia C. H. M., Mulder G., Verbaten M. N. (Amsterdam: Elsevier Science Publishers, B.V; ), 183–194
    1. Hillyard S. A., Anllo-Vento L. (1998). Event-related brain potentials in the study of visual selective attention. Proc. Natl. Acad. Sci. U.S.A. 95, 781–787
    1. Hillyard S. A., Mangun G. R. (1987). Sensory gating as a physiological mechanism for visual selective attention. Electroencephalogr. Clin. Neurophysiol. Suppl. 40, 61–67
    1. Hillyard S. A., Vogel E. K., Luck S. J. (1998). Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1257–1270 10.1098/rstb.1998.0281
    1. Ikeda A., Shibasaki H., Kaji R., Terada K., Nagamine T., Honda M., et al. (1997). Dissociation between contingent negative variation (CNV) and Bereitschaftspotential (BP) in patients with parkinsonism. Electroencephalogr. Clin. Neurophysiol. 102, 142–151 10.1016/S0921-884X(96)95067-5
    1. Ikemi A. (1988). Psychophysiological effects of self-regulation method: EEG frequency analysis and contingent negative variations. Psychother. Psychosom. 49, 230–239 10.1159/000288088
    1. Ishigami Y., Klein R. M. (2010). Repeated measurement of the components of attention using two versions of the Attention Network Test (ANT): stability, isolability, robustness, and reliability. J. Neurosci. Methods 190, 117–1128 10.1016/j.jneumeth.2010.04.019
    1. Knight M., Mather M. (2013). Look out-it's your off-peak time of day! time of day matters more for alerting than for orienting or executive attention. Exp. Aging Res. 39, 305–321 10.1080/0361073X.2013.779197
    1. Kratz O., Studer P., Malcherek S., Erbe K., Moll G. H., Heinrich H. (2011). Attentional processes in children with ADHD: an event-related potential study using the Attention Network Test. Int. J. Psychophysiol. 81, 82–90 10.1016/j.ijpsycho.2011.05.008
    1. Linssen A. M., Vuurman E. F., Sambeth A., Nave S., Spooren W., Vargas G., et al. (2011). Contingent negative variation as a dopaminergic biomarker: evidence from dose-related effects of methylphenidate. Psychopharmacology 218, 533–542 10.1007/s00213-011-2345-x
    1. Luck S. J., Heinze H. J., Mangun G. R., Hillyard S. A. (1990). Visual event-related potentials index focused attention within bilateral stimulus arrays. II. Functional dissociation of P1 and N1 components. Electroencephalogr. Clin. Neurophysiol. 75, 528–542 10.1016/0013-4694(90)90139-B
    1. Luck S. J., Hillyard S. A., Mouloua M., Woldorff M. G., Clark V. P., Hawkins H. L. (1994). Effects of spatial cuing on luminance detectability: psychophysical and electrophysiological evidence for early selection. J. Exp. Psychol. Hum. Percept. Perform. 20, 887–904 10.1037/0096-1523.20.4.887
    1. Macar F., Vidal F., Casini L. (1999). The supplementary motor area in motor and sensory timing: evidence from slow brain potential changes. Exp. Brain Res. 125, 271–280 10.1007/s002210050683
    1. Macleod J. W., Lawrence M. A., McConnell M. M., Eskes G. A., Klein R. M., Shore D. I. (2010). Appraising the ANT: psychometric and theoretical considerations of the Attention Network Test. Neuropsychology 24, 637–651 10.1037/a0019803
    1. Martella D., Manzanares S., Campoy G., Roca J., Antúnez C., Fuentes L. J. (2014). Phasic and tonic alerting in mild cognitive impairment: a preliminary study. Exp. Gerontol. 49, 35–39 10.1016/j.exger.2013.11.001
    1. McConnell M. M., Shore D. I. (2011). Mixing measures: testing an assumption of the Attention Network Test. Atten. Percept. Psychophys. 73, 1096–1107 10.3758/s13414-010-0085-3
    1. Mento G., Tarantino V., Sarlo M., Bisiacchi P. S. (2013). Automatic temporal expectancy: a high-density event-related potential study. PLoS ONE 1:e62896 10.1371/journal.pone.0062896
    1. Missonnier P., Herrmann F. R., Richiardi J., Rodríguez C., Deiber M. P., Gold G., et al. (2013). Attention-related potentials allow for a highly accurate discrimination of mild cognitive impairment subtypes. Neurodegener. Dis. 12, 59–70 10.1159/000338815
    1. Nagai Y., Critchley H. D., Featherstone E., Fenwick P. B., Trimble M. R., Dolan R. J. (2004). Brain activity relating to the contingent negative variation: an fMRI investigation. Neuroimage 21, 1232–1241 10.1016/j.neuroimage.2003.10.036
    1. Neuhaus A. H., Koehler S., Opgen-Rhein C., Urbanek C., Hahn E., Dettling M. (2007). Selective anterior cingulate cortex deficit during conflict solution in schizophrenia: an event-related potential study. J. Psychiatr. Res. 41, 635–644 10.1016/j.jpsychires.2006.06.012
    1. Neuhaus A. H., Trempler N. R., Hahn E., Luborzewski A., Karl C., Hahn C., et al. (2010a). Evidence of specificity of a visual P3 amplitude modulation deficit in schizophrenia. Schizophr. Res. 124, 119–126 10.1016/j.schres.2010.08.014
    1. Neuhaus A. H., Urbanek C., Opgen-Rhein C., Hahn E., Ta T. M., Koehler S., et al. (2010b). Event-related potentials associated with Attention Network Test. Int. J. Psychophysiol. 76, 72–79 10.1016/j.ijpsycho.2010.02.005
    1. Nobre A. C., Sebestyen G. N., Miniussi C. (2000). The dynamics of shifting visuospatial attention revealed by event-related potentials. Neuropsychologia 38, 964–974 10.1016/S0028-3932(00)00015-4
    1. Pascual-Marqui R. D. (2002). Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find. Exp. Clin. Pharmacol. 24 Suppl. D, 5–12
    1. Pascual-Marqui R. D., Esslen M., Kochi K., Lehmann D. (2002). Functional imaging with low resolution brain electromagnetic tomography (LORETA): a review. Methods Find. Exp. Clin. Pharmacol. 24 Suppl. C, 91–95
    1. Peelen M. V., Heslenfeld D. J., Theeuwes J. (2004). Endogenous and exogenous attention shifts are mediated by the same large-scale neural network. Neuroimage 22, 822–830 10.1016/j.neuroimage.2004.01.044
    1. Petersen S. E., Posner M. I. (2012). The attention system of the human brain: 20 years after. Annu. Rev. Neurosci. 35, 73–89 10.1146/annurev-neuro-062111-150525
    1. Polich J. (1986). P300 development from auditory stimuli. Psychophisiology 23, 590–597 10.1111/j.1469-8986.1986.tb00677.x
    1. Polich J. (1987). Task difficulty, probability, and inter-stimulus interval as determinants of P300 from auditory stimuli. Electroencephalogr. Clin. Neurophysiol. 68, 311–320 10.1016/0168-5597(87)90052-9
    1. Posner M. I. (1978). Chronometric Explorations of Mind. Hillsdale, NJ: Lawrence Erlbaum Associates
    1. Posner M. I., Dehaene S. (1994). Attentional networks. Trends Neurosci. 17, 75–79
    1. Posner M. I., Petersen S. E. (1990). The attention system of the human brain. Annu. Rev. Neurosci. 13, 25–42 10.1146/annurev.ne.13.030190.000325
    1. Praamstra P., Kourtis D., Kwok H. F., Oostenveld R. (2006). Neurophysiology of implicit timing in serial choice reaction-time performance. J. Neurosci. 26, 5448–5455 10.1523/JNEUROSCI.0440-06.2006
    1. Ramnani N., Owen A. M. (2004). Anterior prefrontal cortex: in-sights into function from anatomy and neuroimaging, Nat. Rev. Neurosci. 5, 184–194 10.1038/nrn1343
    1. Roberts K. L., Summerfield A. Q., Hall D. A. (2006). Presentation modality influences behavioral measures of alerting, orienting, and executive control. J. Int. Neuropsychol. Soc. 12, 485–492
    1. Roca J., Castro C., López-Ramón M. F., Lupiáñez J. (2011). Measuring vigilance while assessing the functioning of the three attentional networks: the ANTI-Vigilance task. J. Neurosci. Methods 198, 312–324 10.1016/j.jneumeth.2011.04.014
    1. Rohrbaugh J. W., Gaillard A. W. K. (1983). Sensory and motor aspects of the contingent negative variation, in Tutorials in ERP Research: Endogenous Components, eds Gaillard A. W. K., Ritter W. (Amsterdam: North-Holland; ), 269–310
    1. Rohrbaugh J. W., Syndulko K., Lindsley D. B. (1976). Brain wave components of the contingent negative variation in humans. Science 191, 1055–1057 10.1126/science.1251217
    1. Ruchkin D. S., Sutton S., Mahaffey D., Glaeser J. (1986). Terminal CNV in the absence of motor response. Electroencephlogr. Clin. Neurophysiol. 63, 445–463 10.1016/0013-4694(86)90127-6
    1. Rusnáková S., Daniel P., Chládek J., Jurák P., Rektor I. (2011). The executive functions in frontal and temporal lobes: a flanker task intracerebral recording study. J. Clin. Neurophysiol. 28, 30–35 10.1097/WNP.0b013e31820512d4
    1. Snyder A. C., Shpaner M., Molholm S., Foxe J. J. (2012). Visual object processing as a function of stimulus energy, retinal eccentricity and Gestalt configuration: a high-density electrical mapping study. Neuroscience 221, 1–11 10.1016/j.neuroscience.2012.03.035
    1. Spronk M., Jonkman L. M., Kemner C. (2008). Response inhibition and attention processing in 5- to 7-year-old children with and without symptoms of ADHD: an ERP study. Clin. Neurophysiol. 119, 2738–2752 10.1016/j.clinph.2008.09.010
    1. Urbanek C., Weinges-Evers N., Bellmann-Strobl J., Bock M., Dörr J., Hahn E., et al. (2010). Attention Network Test reveals alerting network dysfunction in multiple sclerosis. Mult. Scler. 16, 93–99 10.1177/1352458509350308
    1. van Boxtel G., Brunia C. H. M. (1994). Motor and non-motor aspects of slow brain potentials. Biol. Psychol. 38, 35–51 10.1016/0301-0511(94)90048-5
    1. van Dam N. T., Sano M., Mitsis E. M., Grossman H. T., Gu X., Park Y., et al. (2013). Functional neural correlates of attentional deficits in amnestic mild cognitive impairment. PLoS ONE. 8:e54035 10.1371/journal.pone.0054035
    1. van Rijn H., Kononowicz T. W., Meck W. H., Ng K. K., Penney T. B. (2011). CNV and its relation to time estimation. Front. Integr. Neurosci. 5:91 10.3389/fnint.2011.00091
    1. Walter W. G., Cooper R., Aldridge V. J., McCallum W. C., Winter A. L. (1964). Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature 203, 380–384 10.1038/203380a0
    1. Westlye L. T., Grydeland H., Walhovd K. B., Fjell A. M. (2011). Associations between regional cortical thickness and attentional networks as measured by the attention network test. Cereb. Cortex 21, 345–356 10.1093/cercor/bhq101
    1. Wright M. J., Geffen G. M., Geffen L. B. (1995). Event related potentials during covert orientation of visual attention: effects of cue validity and directionality. Biol. Psychol. 41, 183–202 10.1016/0301-0511(95)05128-7
    1. Yin X., Zhao L., Xu J., Evans A. C., Fan L., Ge H., et al. (2012). Anatomical substrates of the alerting, orienting and executive control components of attention: focus on the posterior parietal lobe. PLoS ONE 7:e50590 10.1371/journal.pone.0050590
    1. Zhang R., Hu Z., Debi R., Zhang L., Li H., Liu Q. (2013). Neural processes underlying the“same”-“different” judgment of two simultaneously presented objects- an EEG study. PLoS ONE 8:e81737 10.1371/journal.pone.0081737

Source: PubMed

3
Se inscrever