Exp Brain Res (2009) 197:153–161
DOI 10.1007/s00221-009-1901-7

 R ES EA R C H A R TI CLE



Can illusory deviant stimuli ...
154                                                                                             Exp Brain Res (2009) 197:1...
Exp Brain Res (2009) 197:153–161                                                                                         1...
156                                                                                                Exp Brain Res (2009) 19...
Exp Brain Res (2009) 197:153–161                                                                                          ...
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Exp Brain Res (2009) 197:153–161                                                                                          ...
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Exp Brain Res (2009) 197:153–161                                                                                          ...
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Can Illusory Deviant Stimuli Be Used As Attentional Distractors To Record V Mmn In A Passive Three Stimulus Oddball Paradigm

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Can Illusory Deviant Stimuli Be Used As Attentional Distractors To Record V Mmn In A Passive Three Stimulus Oddball Paradigm

  1. 1. Exp Brain Res (2009) 197:153–161 DOI 10.1007/s00221-009-1901-7 R ES EA R C H A R TI CLE Can illusory deviant stimuli be used as attentional distractors to record vMMN in a passive three stimulus oddball paradigm? Maria Flynn · Alki Liasis · Mark Gardner · Stewart Boyd · Tony Towell Received: 23 September 2008 / Accepted: 9 June 2009 / Published online: 24 June 2009 © Springer-Verlag 2009 Abstract A passive three stimulus oddball paradigm was an embedded active attention task, we conWrmed the exis- used to investigate Visual Mismatch Negativity (vMMN) a tence of an earlier (150–170 ms) and attenuated vMMN. component of the Event Related Potential (ERP) believed Recordings from an intracranial case study conWrmed sepa- to represent a central pre-attentive change mechanism. ration of N1 and discrimination components to posterior Responses to a change in orientation were recorded to and anterior occipital areas, respectively. We conclude that monochrome stimuli presented to subjects on a computer although the illusory Wgure captured spatial attention in its screen. One of the infrequent stimuli formed an illusory own right it did not draw suYcient attentional resources Wgure (Kanizsa Square) aimed to capture spatial attention from the standard–deviant comparison as revealed when in the absence of an active task. Nineteen electrodes (10–20 using a concurrent active task. system) were used to record the electroencephalogram in fourteen subjects (ten females) mean age 34.5 years. ERPs Keywords Event-related potential · Visual mismatch to all stimuli consisted of a positive negative positive com- negativity · Kanizsa Wgure · Orientation plex recorded maximally over lateral occipital areas. The negative component was greater for deviant and illusory deviant compared to standard stimuli in a time window of Introduction 170–190 ms. A P3a component over frontal/central elec- trodes to the illusory deviant but not to the deviant stimulus The Mismatch Negativity (MMN) is deWned as a compo- suggests the illusory Wgure was able to capture attention nent of the Event Related Potential (ERP) that can be and orientate subjects to the recording. Subtraction wave- evoked to stimulus change in the absence of attention. The forms revealed visual discrimination responses at occipital MMN is usually elicited when a deviant stimulus is pre- electrodes, which may represent vMMN. In a control study sented within a sequence of standard stimuli. The auditory with 13 subjects (11 females; mean age 29.23 years), using MMN has been identiWed as a negative deXection usually peaking at 150–200 ms from change onset and is related to automatic discrimination processing and sensory memory M. Flynn · A. Liasis · M. Gardner · T. Towell (&) mechanisms (see Näätänen et al. 2005, 1997; Schröger Department of Psychology, University of Westminster, 309 Regent Street, London W1B 2UW, UK 1997, for reviews). e-mail: towella@wmin.ac.uk A number of studies have identiWed visual Mismatch Negativity (vMMN), as a negative deXection 100–250 ms A. Liasis post-stimulus change onset (see Pazo-Alvarez et al. 2003 Department of Ophthalmology, Great Ormond Street Hospital for Children, for a review). These studies have reported vMMN either to London WC1N 3JH, UK ‘match’ and ‘non-match’ tasks where the stimuli are pre- sented with equiprobability to control the eVects of global S. Boyd stimulus presentation (Fu et al. 2003) for changes in orien- Department of Clinical Neurophysiology, Great Ormond Street Hospital for Children, tation and spatial frequency (Kimura et al. 2006) for London WC1N 3JH, UK changes in spatial frequency), or within an oddball 123
  2. 2. 154 Exp Brain Res (2009) 197:153–161 paradigm, whereby a variety of dimensions of the visual Marsalek 2003; Polich 2003; Hagen et al. 2006 for stimulus that are known to be important in early visual reviews). The P3 can be further divided into the subcompo- processing are manipulated. These include changes in spa- nents P3a and P3b. P3a originates from frontal attention tial frequency (Maekawa et al. 2005), motion (Kremlacek mechanisms to task novelty and/or distractors whilst the et al. 2006), colour (Czigler et al. 2004; Czigler et al. 2002; P3b is generated in more temporal/parietal regions and is Horimoto et al. 2002), form (Berti and Schroger 2004; associated with context updating and memory storage oper- Besle et al. 2005; Stagg et al. 2004) and orientation ations (Polich 2007). We therefore set out to validate the (Astikainen et al. 2004, 2008; Czigler and Csibra 1992). use of illusory deviant stimuli in orienting attention in a Similar to the auditory MMN the vMMN is thought to passive and active task in the context of a vMMN para- reXect the memory based detection of deviant stimuli rather digm. It was predicted that in the passive paradigm with no than refractoriness (see Czigler et al. 2007 for a detailed task conditions that discrimination components possibly discussion). However, in contrast to the correlation seen reXecting MMN would be evoked by both the deviant and between auditory MMN and behavioural detection of devi- illusory deviant stimuli while a P3a component would only ants (Winkler et al. 1993) there appears to be no such rela- be evident to illusory deviant stimuli that captured attention. tionship in the visual modality. The amplitude of vMMN To test the use of the illusory deviant stimulus in orien- does not increase beyond 40 ms stimulus onset asynchrony tating attention from the standard–deviant discrimination a (SOA) of a masking stimulus whilst detection performance control study was carried out containing an embedded of deviant stimuli and RT improve up to 174 ms SOA active task. Last, the generator sources of the visual ERP (Czigler et al. 2007). These Wndings strongly suggest that components were explored using intracranial recordings in overt detection of visual deviance is not the sole mechanism a subject undergoing presurgical evaluation for epilepsy underlying vMMN. surgery. In comparison to other ERP change components, such as N2 and P3, the MMN can be elicited in the absence of attention (Pazo-Alvarez et al. 2003). Therefore, in order to Methods diVerentiate between MMN and other ERP change compo- nents the subjects’ attention is typically drawn away from Participants the test stimuli, employing a variety of behavioural tasks. For example, Stagg et al. (2004) and Tales et al. (1999) Study 1 and 2 required participants to press a button in response to target stimuli, Astikainen et al. (2004) used an auditory distrac- With ethical approval and informed consent 14 healthy tion task whereby participants were required to focus their adults (mean age 34.5 § 8.6 years (10 females) were attention on counting the number of words in a story whilst recruited for study 1 and 13 healthy adults (mean age being presented with visual stimuli. 29.23 § 8.8 years (11 females) for study 2. Subjects It has generally been understood that a concurrent active reported no history of neurological disease and had normal task is mandatory in eliciting vMMN to control for the or corrected-to-normal visual acuity. eVects of attention so that resources are allocated away from the standard–deviant discrimination towards the Study 3 active task (Heslenfeld 2003; Czigler 2007). However, not all patient populations can meet the demands of an active With hospital ethical approval and patient and parental con- task. Therefore, in the present study a three-stimulus pas- sent, a 15-year-old male with focal epilepsy undergoing sive oddball paradigm was developed. Stimuli diVered with pre-surgical evaluation for resection of a R anterior parietal regard to orientation of local endline type pacman Wgures lesion provided the opportunity to examine whether there and their information/entropy content. So in addition to was a dissociation of detection and discrimination compo- standard and deviant stimuli, an infrequent illusory deviant nents of the visual ERP. stimulus was introduced in order to investigate the eVects of attention. The illusory deviant stimulus was a Kanizsa Stimuli and procedure Wgure (Kanizsa 1976) which formed an illusory square, a salient event thought to demand attention to reconstruct Study 1 contours that are absent from visual images (Kaiser et al. 2004). Three monochrome endline type stimuli based on pacman A consistent Wnding in ERP research is that the P3 wave, Wgures were employed in a behaviourally silent oddball a positive deXection occurring from 280 to 400 ms post- paradigm where the ratio of standards to deviants and illu- stimulus indicates attentional processing (see Hruby and sory deviants was 8:1:1. The stimuli in (Fig. 1a), diVered 123
  3. 3. Exp Brain Res (2009) 197:153–161 155 Fig. 1 a Stimuli presented in a) b) -8µV c) oddball paradigm with pseudo- N1 random sequence of 8:1:1, respectively. (i) standard, (ii) i) O1 O2 deviant and (iii) illusory deviant 100ms forming a Kanizsa square. b, c Grand average waveforms referenced to Fz at O1 and O2, respectively for (i) Standard P2 P1 (dashed line), deviant (solid ii) line) and illusory deviant stimuli (dotted line) (ii) Deviant minus standard (iii) Illusory deviant minus standard. Note the dis- crimination responses in ii) and iii) with an additional negative component in (iii) corresponding iii) to an inverted P3 from each other only in terms of the orientation of elements In study 3, the two blocks of the stimuli were presented (which were oriented unsystematically around their axes with no embedded active attention task. for the standard and deviant stimuli and formed an illusory Kanizsa Wgure for the illusory deviant stimulus. The stimuli Electroencephalogram recording and data analysis were generated employing STIM software (Neuroscan- STIM version 4; Compumedics USA, Ltd., El Paso, TX, Study 1 and 2 USA) and presented on a computer screen subtending 4°. The stimuli appeared on the screen for 400 ms with an Nineteen silver–silver chloride electrodes were used to inter-stimulus interval of 600 ms. Subjects were seated record the electroencephalogram (EEG) activity and were comfortably in a darkened room 1 m away from the screen positioned at sites in accordance with the International 10– and requested to Wxate on a small red dot in the centre of 20 system (Fz, F3, F4, Cz, C3, C4, T3, T4, Pz, P3, P4, Oz, the screen that was present throughout recording. Within O1, O2, T5, T6, VEOG, M1, M2). The reference electrode the oddball paradigm stimuli were presented in a pseudo- and the ground electrode were placed at the right and left random sequence ensuring that deviant and illusory deviant mastoid, respectively. An electrode was placed above the stimuli were interspersed with standard stimuli. In study 1, left eye to enable online artefact rejection of eye blinks. the stimuli were presented in Wve blocks of 225 stimuli with Continuous EEG was collected using Neuroscan-SCAN up to a minute break between blocks. At the end of the odd- version 4.3; Compumedics USA, Ltd., El Paso, TX, USA at ball recording blocks of 64 deviants and illusory deviants a sampling rate of 1,000 Hz, with a low pass of 100 Hz and ‘alone’ were presented. a high pass of 1 Hz and stored on a computer for oZine analysis. Study 2 Continuous EEG data were epoched oZine ¡100 ms pre-stimulus to +500 ms post-stimulus. The epochs were The same stimuli and procedure as in Study 1 were utilized digitally Wltered with a band pass 1–30 Hz and baseline cor- with the exception that an active attention task was embed- rected. Epochs containing transients greater than §150 V ded in the three stimulus oddball paradigm. Within the were excluded from further analysis. For each subject, ERPs blocks of 225 stimuli, during the interstimulus interval were averaged separately for standard, deviant and illusory (ISI), a small red square replaced the small red Wxation dot deviant stimuli employing Fz as a reference and grand aver- on 22 trials chosen at random. The red square appeared at age waveforms were constructed. Additional ERPs were the start of the 600 ms ISI and stayed on the screen for constructed in study 2 for the red Wxation dot and for the red 200 ms. Subjects were instructed to focus their attention on square that replaced the Wxation dot on a number of trials. the red Wxation dot and press the right button of a mouse as ERPs to standard stimuli were constructed from epochs that quickly as possible whenever the red square appeared. preceded deviant stimuli. As in previous studies (Stagg et al. Inclusion criteria were based on participants achieving 90% 2004; Tales et al. 1999), averaged mastoids were employed or more correct responses, excluding false positives. as a reference to investigate P3 activity. 123
  4. 4. 156 Exp Brain Res (2009) 197:153–161 From the grand average waveforms MMN-like diVer- Table 1 Mean ERP amplitude ( V) and standard deviation (SD) for ences were identiWed on the basis of known negative polar- each stimulus type at electrode sites for the 170–190 ms time window ity, known emergence over posterior electrode positions for the passive task (n = 14) and typical latency range (100–250 ms post-stimulus: Pazo- Electrode Mean amplitude ( V) and standard Alvarez et al. 2003). In each study, the maximal diVerence site deviation (§SD) between ERPs to standards and deviants was identiWed at Stimulus occipital sites and a 20 ms time window was centred at this Standard Deviant Illusory deviant latency for electrodes P3, P4, O1, O2, T5, T6 (Astikainen et al. 2008). Mean amplitudes for the time windows were O1 2.98 § 2.32 5.67 § 3.36 7.10 § 4.10 calculated relative to the mean voltage of a 100 ms pre- O2 3.11 § 2.73 5.66 § 3.38 7.33 § 4.38 stimulus baseline for each participant for the standard, devi- P3 1.99 § 1.68 3.75 § 2.85 5.03 § 3.49 ant and illusory deviant stimuli. The mean amplitudes were P4 1.90 § 1.91 3.43 § 2.27 5.08 § 3.12 analysed using ANOVA. In addition, subtraction wave- T5 2.36 § 2.03 4.59 § 2.75 5.42 § 3.07 forms were constructed of deviant minus standard and illu- T6 2.62 § 1.83 4.70 § 2.24 5.13 § 2.75 sory deviant minus standard. Study 3 P < 0.001], indicating that the amplitude of the deviant stimulus was greater than the standard stimulus at occipital The patient was implanted with a 32-contact sub-dural plat- (t = 4.004; df = 13; P = 0.002) and temporal electrodes inum grid straddling the parietal and pre-motor gyri and a (t = 4.552; df = 13; P = 0.001) and that the amplitude of the 6-contact strip extending posteriorly over the inferior parie- illusory deviant was greater than the standard at occipital tal cortex such that the most distal contact (S1) overlay the (t = 4.507; df = 13; P = 0.001), temporal (t = 4.552; R occipital cortex (Fig. 3a). df = 13; P = 0.001) and parietal electrodes (t = 4.276; df = 13; P = 0.001). DiVerence waveforms of deviant minus standard and Results illusory deviant minus standard both revealed vMMN com- ponents (Fig. 1b, c). When comparing the deviant to the Study 1 standard ERP, using the point-by-point t test algorithm (P < 0.05; one-tailed) against baseline there were signiW- A visual response was recorded in all subjects in all trials cant diVerences at O1 between 173 and 217 ms (181– consisting of a P1–N1–P2 waveform. Grand average wave- 203 ms; P < 0.01) and at O2 between 178 and 208 ms forms were constructed for the standard, deviant and illu- (185–196 ms); P < 0.01). Comparing the illusory deviant to sory deviant stimuli (see Fig. 1 for waveforms at O1 and the standard ERP against baseline, there were signiWcant O2). The maximal diVerence between ERPs to standards diVerences (P < 0.05; one-tailed) at O1 between 164 and and deviants was at approximately 180 ms post-stimulus at 212 ms (175–203 ms; P < 0.01) and at O2 between 169 and occipital electrodes. A 20 ms time window was centred at 212 ms (181–199 ms; P < 0.01). this latency for electrodes O1, O2, P3, P4, T5, T6 and, for Illusory deviant stimuli evoked an additional late nega- each participant, mean amplitudes for this time window cal- tive component at 234 ms at Oz. To examine whether this culated relative to the mean voltage of a 100 ms pre-stimu- component corresponded to an inverted P3 component the lus baseline for standards, deviants and illusory deviants. waveforms were re-referenced to averaged mastoids. We Mean amplitudes and standard deviations for the standard, were able to reveal a positive component over the fronto- deviant and illusory deviant are shown in Table 1. central electrode sites corresponding to P3a. At Fz this A three-way within subjects ANOVA was used to ana- component had an onset latency of 244 ms, SD = 13 ms lyse the mean amplitude data in the 170–190 ms time win- and a peak latency of 290 ms, SD = 27 ms with a peak dow. Pairwise comparison of means was carried out using amplitude of 4.19 V, SD = 2.06 V. bonferroni corrected t tests. Factors were location (occipi- To examine whether the diVerences observed in the sub- tal, parietal, temporal), hemisphere (left, right) and stimulus traction waveforms were confounded by pure stimulus (standard, deviant and illusory deviant). The amplitude diVerences we compared the discrimination waveform to diVered signiWcantly with location [F(2,26) = 11.880; the deviant stimulus to the discrimination waveform when P < 0.001] and stimulus type [F(2,26) = 15.886; P < 0.001] that same stimulus was presented alone, i.e. out of context but not with hemisphere [F(1,13) = 0.233; P = 0.794]. and not in an oddball paradigm. Point-by-point t tests There was a statistically signiWcant interaction between revealed no signiWcant diVerences between the deviant– location and stimulus [F(4.52) = 6.503; P = 0.001, standard and deviant alone-deviant waveforms suggesting 123
  5. 5. Exp Brain Res (2009) 197:153–161 157 that when the deviant stimulus was presented alone and out Table 2 Mean ERP amplitude ( V) and standard deviation for each of context it behaved in a similar way to the standard stimu- stimulus type at electrode sites at 150–170 ms for the active task lus even though it was physically diVerent. The same proce- (n = 13) dure was used to compare the illusory deviant stimulus in Electrode Mean amplitude ( V) and standard the context of an oddball paradigm with the illusory deviant site deviation (§SD) stimulus presented alone. Similarly, there were no signiW- Stimulus cant diVerences between the illusory deviant–standard and Standard Deviant Illusory deviant illusory deviant alone-illusory deviant waveforms. O1 4.12 § 2.22 5.12 § 2.10 7.24 § 2.79 Study 2 O2 5.20 § 3.40 6.25 § 3.43 9.27 § 5.20 P3 2.32 § 1.76 2.79 § 1.83 3.51 § 2.22 As in study 1, a visual response was recorded for all sub- P4 3.50 § 2.33 4.07 § 2.01 5.56 § 3.28 jects consisting of a P1–N1–P2 waveform. Grand average T5 3.23 § 1.75 4.18 § 1.82 5.20 § 2.00 waveforms were constructed for the standard, deviant and T6 4.90 § 2.35 5.6 4 § 2.36 7.48 § 3.92 illusory deviant stimuli (see Fig. 2 for waveforms at O1 and O2). The maximal diVerence between ERPs to standards and deviants was at approximately 160 ms post-stimulus at mean voltage of a 100 ms pre-stimulus baseline for stan- occipital sites. A 20-ms time window was centred at this dards, deviants and illusory deviants for each participant. latency for electrodes O1, O2, P3, P4, T5, T6 and mean Mean amplitudes and standard deviations for the standard, amplitudes for this time window calculated relative to the deviant and illusory deviant are shown in Table 2. A three-way within subjects ANOVA was used to ana- lyse the mean amplitude data of the 150–170 ms time win- dow. Pairwise comparison of means was carried out using O1 O2 N1 bonferroni corrected t tests. Factors were location (occipi- tal, parietal, temporal), hemisphere (left, right) and stimulus (standard, deviant and illusory deviant). The amplitude diVered signiWcantly with location [F(2,24) = 16.874; a) P < 0.001], hemisphere [F(2,24) = 7.059; P = 0.021] and stimulus type [F(2,24) = 14.254; P < 0.001]. There was a P1 P2 signiWcant interaction between location and stimulus [F(4.48) = 10.636; P < 0.001] indicating that the amplitude of the deviant stimulus was greater than the standard stimu- lus at occipital (t = 3.796; df = 12; P = 0.003) and temporal -8µV (t = 3.147; df = 12; P = 0.008) electrodes. The amplitude of b) the illusory deviant stimulus was greater than the standard stimulus at occipital (t = 4.494; df = 12; P = 0.001), tempo- 100ms ral (t = 4.425; df = 12; P = 0.001) and parietal (t = 4.105; df = 12; P = 0.001) electrodes. There was a signiWcant interaction between hemisphere and stimulus [F(2,24) = c) 3.402; P = 0.050] indicating that in the left hemisphere the mean amplitude was greater for the deviant (t = 4.194; df = 12; P = 0.001) and illusory deviant (t = 5.536; df = 12; P < 0.001) than for the standard. In the right hemisphere the mean amplitude of the illusory deviant (t = 5.944; df = 12; d) P < 0.001) was greater than the standard as was the deviant P3 but to a lesser extent (t = 2.952; df = 12; P = 0.012). DiVerence waveforms of deviant minus standard and Fig. 2 a Grand average waveforms referenced to Fz for standard illusory deviant minus standard both revealed attenuated (dashed line), deviant (solid line) and illusory deviant stimuli (dotted vMMN components (Fig. 2b, c). When comparing the devi- line) at O1 and O2. Note the P3a component seen only to illusory devi- ant to the standard ERP, using the point-by-point t test ant stimuli. b Deviant minus standard. c Illusory deviant minus stan- algorithm (P < 0.05; one-tailed) against baseline, there dard. d Grand average waveforms for the rarely occurring red Wxation square (solid line) and for the central Wxation dot (dotted line). Note: were signiWcant diVerences at O1 between 138 and 176 ms the attenuated vMMN in b and the P3b wave to the task in d but no signiWcant diVerences were apparent at O2. When 123
  6. 6. 158 Exp Brain Res (2009) 197:153–161 comparing the illusory deviant to the standard ERP against mismatch) were recorded more anteriorly at S3 and S4 and baseline, there were signiWcant diVerences (P < 0.05; one- were characterised by enhanced positivities at about 90 ms, tailed) at O1 between 142 and 178 ms and at O2 between 42.32 V and 219 ms, 87.21 V for S3 and enhanced 147 and 177 ms. positivities at 88 ms, 28.55 V and 237 ms, 45.93 for S4, Illusory deviant stimuli evoked an additional late nega- either side of the major negative component (Fig. 3b). tive component at occipital electrodes. When re-referenced Subtraction waveforms (deviant–standard) revealed dis- to averaged mastoids this component was positive over the crimination responses with positive peaks at 86 and 219 ms fronto-central electrode sites. At Fz this had an onset for electrode S3 and 93 and 233 ms at electrode S4. In latency of 223 ms, SD = 18 ms and a peak latency of addition, a later positive response to the illusory deviant 282 ms, SD = 22 ms with a peak amplitude of 5.17 V, stimulus was seen at around 386 ms over pre-motor regions SD = 2.72 V. (G9 > G17 and G18), suggesting activation of a frontal sys- All participants completed the active task (pressing the tem to stimulus novelty and/or target detection (Fig. 3c). mouse when the red Wxation dot was replaced with a red Wxation square) within the limits of the inclusion criteria. As expected, the active task evoked a P3b component Discussion showing that the participants’ attention was engaged with the task (See Fig. 2d). The main result from this study is that visual discrimination responses including vMMN components have been Study 3: intracranial recording recorded in a behaviourally silent oddball paradigm to a change in orientation. The stimuli utilised in this study A negative positive negative complex was recorded maxi- evoked a response that was more negative to the deviant mally to all stimuli at the most posterior electrode site (S1) stimuli than to the standard stimuli in the period 150– (Fig. 3b). The latency and amplitude of the Wrst major neg- 200 ms after stimulus onset. Whilst we acknowledge that ative component (N1) was similar for standard, deviant there were physical diVerences between the stimuli, and stimuli and illusory deviant stimuli (153 ms and ¡32.39 V, that these changes were not equal between standard–devi- 153 ms and ¡48.54 V, 162 ms and ¡45.50 V, respec- ant and standard–illusory deviant comparisons, the employ- tively). Responses to stimulus discrimination (visual ment of a ‘deviant alone’ and ‘illusory deviant alone’ conditions served as controls. Subsequent subtraction waveforms using the subtraction method suggested by Kraus et al. (1995) for delineating the MMN reveals that the diVerence in negativity was attributable not to physical G32 diVerences in the stimuli themselves, but by the context in b) s1 a) xx ++ G17 G9 G1 which the stimuli were presented. s2 S1 S6 The presence of a P3a over frontal/central electrodes for the illusory deviant grand average waveform but not for the s3 standard or deviant grand average waveforms, suggests that c) -30uV G9 the Kanizsa square captured attention. Without the control 100ms s4 task this would imply that the enhanced negativity exhib- G17 ited by the deviant compared to the standard may not s5 depend on attention. However, the use of the illusory Wgure G18 is supported by Senkowski et al. (2005) who found that Kanizsa Wgures automatically capture spatial attention s6 Fig. 3 a Co-registered sub-dural electrode locations, dotted eclipse when used as visual cues and Wallach and Slaughter (1988) denotes surface visible lesion, x seizure onset zone, + somatosensory who found that the familiarity of the illusory shape ERP localised. b Standard and deviant waveforms from the six strip increases the likelihood that the shape will be perceived. In contacts—dashed waveform represents the standard ERP, solid wave- addition, a number of clinical studies show that the form the deviant. At S1 and S2 the illusory deviant waveform did not diVer from the deviant or standard and no consistent changes were seen response to Kanizsa Wgures is robust. In an ERP study, at S3 and S4. For reasons of clarity the illusory deviant waveform is not Grice et al. (2003) examined perceptual completion in par- shown. Peak amplitude of the N1 and inverted discrimination compo- ticipants with Williams Syndrome—a genetic disorder in nent shown by the shaded area of the waveform. c Anterior grid elec- which visuo-spatial performance is poor, and found that trodes revealing a later positive response to the illusory deviant stimulus shown by the shaded area of the waveform. Dashed, solid and although the underlying neural mechanisms of the partici- dotted lines represent ERPs to standard, deviant and illusory deviant pants with Williams Syndrome may be diVerent to controls, stimuli, respectively their ability to perceive illusory contours was apparently 123
  7. 7. Exp Brain Res (2009) 197:153–161 159 normal. Milne and Scope, in their 2007 study, suggested of arc also reveals the contribution of the parvocellular sys- that the perception of illusory contours in participants with tem and ventral stream in detecting diVerences in the Autistic Spectrum Disorder was intact. sequence of unattended central stimuli. The parvocellular Observation and statistical analysis of the waveforms system is particularly adapted to colour and high-contrast and the discrimination components reveals that the ampli- black and white detailed information. tude component N1 for the illusory deviant at the lateral Besle et al. (2005) using the deformation of a circle as a occipital electrodes was greater than for the standard or deviant stimulus embedded within an active task presented deviant stimuli. Many previous studies have demonstrated within 2° of arc demonstrated bilateral vMMN responses at an enhanced visual N1 amplitude component to attended- 216 ms being maximal at electrode PO3 and PO4. In an location stimuli (see Vogel and Luck 2000 for a review) active geometric shape discrimination task P1, N1 and P2 and this evidence further suggests that the illusory deviant components were identiWed at 80, 140 and 200 ms, respec- stimulus captured attention whilst the standard and deviant tively, and the N1 and P2 components became less sharp stimuli did not. and more diVuse as stimulus presentation changed between As with several previous studies (e.g. Tales et al. 1999) 4°, 8° and 12° of arc (Shoji and Ozaki 2006). we also engaged an active control task that required partici- Extra deviant stimuli conceptulised as distractor stimuli pants to press a button at the occurrence of a change in have also been used in the auditory modality to manipulate shape of the central Wxation dot. The understanding here is attention. For instance, Schroger et al. (2000) and Schroger that attentional resources are drawn from the standard– and WolV (1998) in an auditory duration discrimination deviant discrimination to the active task. Under these con- task found that task irrelevant distractors in the form of ditions we were able to conWrm the existence of vMMN small changes in frequency prolonged reaction times and responses although they were signiWcantly reduced in elicited MMN and P3a components, reXecting orientation amplitude. The underlying mechanisms of vMMN are still towards the distractor. to be resolved although a number of studies have suggested Recordings from the intracranial case study support the a memory based rather than refractoriness explanation (see separation of detection and discrimination processes within Czigler 2007). Such a visual based memory system would the visual cortex. The N1 component at 153 ms located at rely on the representation of regularity following repeated the more posterior electrodes corresponds to the scalp exposure to identical frequent stimuli. The violation of such recorded N1 at 167 ms. The waveforms were similar for the regularity following the presentation of a deviant stimulus standard, deviant and illusory deviant stimuli. However, at would elicit an enhanced posterior negativity commonly adjacent posterior electrodes (S3 and S4) the deviant stim- seen as vMMN in subtraction waveforms. However, in this uli evoked early and later positivities that probably contrib- model, it appears that longer sequences (10–15) of fre- ute to the scalp recorded MMN. With respect to scalp quent/standard and identical unattended stimuli will inXu- recordings these potentials to stimulus discrimination are ence the generation of vMMN (Czigler and Pato 2009). In inverted in polarity and the Wrst positive component is seen the current study, the median number of continuous stan- relatively early at around 90 ms. These Wnding are consis- dard sequences was 4 and this may account for the rela- tent with an MEG study showing strong activation of the tively low amplitude of the vMMN responses in study 2. lateral occipital cortex at around 155 ms post-stimulus The latency of the responses in the current study are consis- (Halgren et al. 2003). In MEG studies comparison of illu- tent within the general window for vMMN responses of sory Kanizsa stimuli with control stimuli reveals activation between 100 and 250 ms (Pazo-Alvarez et al. 2003) between 100 and 350 ms post-stimulus (Kaiser et al. 2004) although it is known that latency and duration of vMMN and at around 280 ms (Halgren et al. 2003). It is believed will diVer according to stimulus characteristics and task that illusory contour sensitivity may Wrst occur in middle to complexity with less salient changes and more complex higher order visual processing areas and that feedback rules resulting in longer latency and less phasic vMMN modulation from lateral occipital areas will activate V1 and responses (Czigler et al. 2006). V2 areas (Kaiser et al. 2004). Previous studies on vMMN have tended to engage active Early cortical processing in the visual cortex has also tasks embedded in more peripheral areas of the visual Weld been reported from MEG studies using Xash stimuli that and one study speciWcally set out to assess the contribution reach medial occipital areas around 47 ms (Inui and Kakigi of the magnocellular system (Kremlacek et al. 2006). This 2006). Recent studies using intracranial recordings demon- pathway forms the dorsal stream and is not sensitive to col- strate activation in the superior parietal lobule at 75 ms to our or detail but is thought to be responsible for pre-atten- coloured disc stimuli presented in the macular Weld tive detection of motion stimuli. Whilst in the present study (Molholm et al. 2006) and recordings from the striate we cannot exclude the contribution of the magnocellular cortex to alternating stimuli have been reported as a P55 system, our Wndings of a vMMN in the macular Weld at 4° followed by a more consistent N75 (Farrell et al. 2007). 123
  8. 8. 160 Exp Brain Res (2009) 197:153–161 Polarity inversions between the cortex and the scalp can Czigler I, Csibra G (1992) Event-related potentials and the identiWca- indicate local generator sources in that region of cortex. As tion of deviant visual stimuli. Psychophysiology 29:471–485 Czigler I, Pato L (2009) Unnoticed regularity violation elicts change- these scalp recorded N1 and MMN Welds are interactions of related brain activity. Biol Psychol 80:339–347 the super imposition of several bilateral generators it is Czigler I, Balázs L, Winkler I (2002) Memory-based detection of task- diYcult to understand how focal intracranial potentials con- irrelevant visual changes. Psychophysiology 39:869–873 tribute to the scalp recorded N1 and MMN. The inverted Czigler I, Balázs L, Pató LG (2004) Visual change detection: event- related potentials are dependent on stimulus location in humans. biWd positive discrimination component may well represent Neurosci Lett 364:149–153 the existence of one or more local generator sources to Czigler I, Weisz J, Winkler I (2006) ERPs and deviance detection: change detection. Complex and widespread activation has visual mismatch negativity to repeated visual stimuli. Neurosci also been recorded to alternating and on/oV stimuli from the Lett 401:178–182 Czigler I, Weisz J, Winkler I (2007) Backward masking and visual striate cortex and visual association areas (Farrell et al. mismatch negativity: Electrophysiological evidence for memory- 2007) further supporting the view that it is diYcult to based detection of deviant stimuli. Psychophysiology 44:610–619 entangle the generator sources that contribute to responses Farrell DF, Leeman S, Ojemann A (2007) Study of the human visual measured at the scalp. cortex: direct cortical evoked potentials and stimulation. J Clin Neurophysiol 24:1–10 Intracerebral potentials to rare distractor visual and audi- Fu S, Fan S, Chen L (2003) Event-related potentials reveal involuntary tory stimuli have been recorded from frontal regions as a processing of orientation changes in the visual modality. Psycho- widespread negative–positive–negative waveform at physiology 40:770–775 approximate latencies of 210–280–390 ms, respectively Grice SJ, de Hahn M, Halit H, Johnson MH, Csibra G, Grant J, KarmiloV-Smith A (2003) ERP abnormalities of illusory contour (Baudena et al. 1995). It is believed that this waveform cor- perception in Williams Syndrome. Neuroreport 14:1773–1777 responds with the scalp recorded N2a/P3a/slow wave that is Hagen GF, Gatherwright JR, Lopez BA, Polich J (2006) P3a from associated with orienting. In the present study the later pos- visual stimuli: task diYculty eVects. Int J Psychophysiol 59:8–14 itivity to the illusory deviant stimulus seen at around Halgren E, Dale AM, Mendola J, Chong CDR (2003) Cortical activa- tion to illusory shapes as measured with magnetoencephalogra- 386 ms over pre-motor regions may correspond to this nov- phy. Neuroimage 18:1001–1009 elty orienting process. Heslenfeld DJ (2003) Visual mismatch negativity. In: Polich J (ed) In conclusion, we suggest that visual discrimination Detection of change: event-related potential and fMRI Wndings. potentials containing vMMN components can be elicited Kluwer, Dordrecht, pp 41–60 Horimoto R, Inagaki M, Yano T, Sata Y, Kaga M (2002) Mismatch using a paradigm with no task demands. The inclusion of negativity of the color modality during selective attention task to an illusory square was intended to capture the subject’s auditory stimuli in children with mental retardation. Brain Dev attention and therefore orientate them to the recording. The 24:703–709 existence of attenuated vMMN when subjects engaged in Hruby T, Marsalek P (2003) Event-related potentials—the P3 Wave. Acta Neurobiol Exp 63:55–63 an active distractor task supports the contention that the Inui K, Kakigi R (2006) Temporal analysis of the Xow from V1 to the illusory square was unable to command all resources away extrastriate cortex in humans. J Neurophysiol 96:775–784 from the standard–deviant comparison. Kaiser J, Bühler M, Lutzenberger W (2004) Magnetoencephalographic gamma-band responses to illusory triangles in humans. 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