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Background: The N200 component of event related potentials (ERPs) is considered an index of monitoring error related responses. The aim of the present work was to study the effect of mismatch conditions on the subjects’ responses in an auditory identification task and their relation to the N200 of stimulus-locked ERPs. Methods: An auditory identification task required to correctly map a horizontal slider onto an active frequency range by selecting a slider position that matched the stimulus tone in each trial. Fourteen healthy volunteers participated in the study and ERPs were recorded by 32 leads. Results: Results showed that the subjects’ erroneous responses were equally distributed within trials, but were dependent on mismatch conditions, generated by large differences between the frequencies of the tones of consecutive trials. Erroneous trials showed a significantly greater negativity within the time window of 164-191 ms after stimulus, located mainly at the Cz and Fz electrodes. The LORETA solution showed that maximum activations, as well as maximum differences, were localized mainly at the frontal lobe. Conclusions: These findings suggest that the fronto-central N200 component, conceived an index of “reorientation of attention”, represents a correlate of an error signal, being produced when representation of the actual response and the required response are compared. Furthermore the magnitude of the amplitude of the N200 rests on the relation between the present and the previous stimulus. Background to negative than positive outcomes in psychophysiologi- To adapt ongoing behavior in a changing world, human cal tasks [4,5]. There is good evidence suggesting that beings have to compare performed actions against their anterior negativities in the N200 latency range are eli- intended outcome; in this process the detection of cited by a variety of manipulations that tax error related errors is of major importance . response and which likely counts no-go N200 [6-8], Interest in behavioral monitoring and evaluative pro- feedback related negativity tasks [5,9], as well as N2 cesses has been heightened by the discovery of an conflict tasks [10-12]. event-related potential (ERP) component referred to as The mismatch negativity (MMN), formerly categorized the error-related negativity (ERN)  or error negativity as the early N2a subcomponent of the N200 [4,13,14], is (Ne) . It is important to note that in the performance a change-specific component of the event-related brain -oriented cognitive literature there are reports indicating potential (ERP), initially observed in the auditory modal- that not only the ERN/Ne waveforms but also the N200 ity and later studied in the other sensory modalities too. component of ERPs might be conceived as an index of The MMN is elicited when there is a change in the monitoring of errors. input, relative to the predictions formed on the basis of The N200 is a frontocentral negative wave peaking a memory trace of previous input. Within this frame- between 100 and 250 ms after stimulus onset that is lar- work the MMN would result from a failure to predict ger to negative than positive feedback, regardless of sen- bottom-up input and consequently to suppress predic- sory modality of the feedback signal, and is also larger tion error [15-17]. Recent work has linked the early component (in the range of about 100-140 ms) to a sen- sorial, or non-comparator account of the MMN, origi- * Correspondence: firstname.lastname@example.org Institute of Communications and Computer Systems, National Technical nated in the temporal cortex, and the later component University of Athens, 9, Iroon Polytechneiou str, 157 73 Zografou Campus, (in the range of about 140-200 ms) to a comparator Athens, Greece © 2010 Karanasiou et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Karanasiou et al. Behavioral and Brain Functions 2010, 6:14 Page 2 of 8 http://www.behavioralandbrainfunctions.com/content/6/1/14 based mechanism of the MMN, involving the prefrontal Secondly, using the LORETA technique, our aim was cortex [18,19]. to investigate candidate brain structures that are Despite the immense number of MMN studies, our responsible for the N200 differences observed under understanding of the processes and mechanisms upon mismatch conditions. which the elicitation of MMN depends is rather incom- plete. For a long time, it was debated whether represen- Methods tations of individual auditory features or an integrated Participants representation of an event’s combined features perform Fourteen healthy individuals (eight men and six the automatic comparison. The MMN can be elicited by women),withmean ageof26.6±2.9years andhigh a variety of stimulus changes, ranging from simple level education (education years 17.7 ± 2.3), all with changes in a single stimulus feature to abstract changes normal hearing as measured by pure-tone audiograms in the relationship between stimuli . The MMN has (thresholds <15dB HL), participated in the experiment. been also observed in stimulus paradigms containing no Themale and female subgroupswerehomogeneous frequently repeating sound . with regards to age and educational level. All the partici- Additionally, studies have analysed the mismatch pants were right-handed and had no history of any hear- negativity and error negativity as indices of error com- ing problem. Approval was obtained by the institutes’ mission and monitoring. On error trials during a go/no- ethics committee and informed consent was obtained go auditory oddball task, the mismatch negativity ampli- from all subjects. tude was clearly reduced as compared with mismatch negativity amplitude on correct trials . In two Stimuli and procedures experiments where the perception of vowels belonging In the present research an auditory identification task to two linguistically related languages was investigated, has been used. The person who performed the task sat the results showed that the larger the acoustic differ- in front of a computer screen and at each trial he/she ence, the larger the MMN amplitude. Acoustic differ- heard the stimulus tone (stimulus frequency) with dura- ence between the stimulus pairs was reflected both by tion of 1 sec presented through the headphones (K44 the MMN amplitude and reaction time speed (RTs). headphones, AKG). The MMN amplitude increased and the RTs decreased The stimulus tone was randomly selected for each as the difference between the standard and deviant sti- trial within a fixed frequency range (200-600 Hz) which muli increased . Short reaction times are related to remained thesamethroughoutthe wholeexperiment. increased error rates . An LCD monitor with refresh rate 60 Hz and a custo- Recently, our team studied error related potentials in mized program for stimulus presentation were used. an auditory identification task. The aim for subjects par- The participant’s task was to position a slider pre- ticipating in this task was to correctly map an active sented on the computer screen with a gamepad, such tone-frequency range onto a horizontal bar, by selecting that the slider position would match the frequency of a slider position that matches a stimulus tone that was the stimulus tone. At the beginning of the trial blocks, presented to him/her in the beginning of each trial. Our the starting position of the cursor was in the middle of team examined the patterns of brain activity of actors the slider and the participants did not know the scaling and observers elicited upon receiving feedback informa- of the frequency range within which the slider position tion of the actor’s response and obtained findings sug- should be mapped. After the positioning of the slider, gesting that feedback information has a different effect the frequency corresponding to the participant’s selected on the intensities of the ERP patterns of actors and slider position (response frequency) was presented to observers depending on whether the actor committed the participant. The experiment consisted of 40 trials an error . Part of the data obtained during this for each participant. experiment in the single-participant conditions, that Before the experiment, the subjects were submitted have not been previously reported, were processed in to an acoustic pre-test in order to examine their hear- the framework of the present study focusing on stimulus ing ability in the frequency range that was used in the locked potentials. experiment. During this test two tones were presented More specifically, our purpose was twofold. Firstly, to the participants. Then, the participants had to iden- our aim was to examine the patterns of stimulus- tify which of these tones was higher than the other. locked N200 waveforms during frequency mismatch The frequencies of the two tones selected for the detection in relation to correct versus incorrect acoustic test were determined as the 25% and the 75% responses. The frequency mismatch was studied of the range of 400 Hz bandwidth. The subjects heard between consecutive stimulus tones as well as stimulus the tones with their headphones and responded orally and corresponding response-related feedback tones. to the experimenter. All participants were capable to Karanasiou et al. Behavioral and Brain Functions 2010, 6:14 Page 3 of 8 http://www.behavioralandbrainfunctions.com/content/6/1/14 discriminate between the tones presented in the pre- was 39, since the first trial did not have a previous sti- test. mulus and response frequency. EEG recordings and experimental setup LORETA source localization method The experimental setup included a Faraday room, which The low resolution brain electromagnetic tomography screened any electromagnetic interference that could (LORETA) differentiates between structural and ener- affect the measurements. The EEG was recorded con- getic processes related to information processing as tinuously using a 32-channel electrode cap (Biosemi, revealed by the associated EEG/ERP waveform [27,28]. Active Two system) according to the international 10-20 The structural level, revealed by the location of the local EEG system . The electrodes used were Fp1, Fp2, maxima of the current source density distribution, Pz,Fz, O1,O2, P3,P4, P7,P8, C3,C4, T7,T8, F3,F4, describes the time dependent network of activated brain F7, F8, Cz, Oz, CP5, CP6, CP1, CP2, FC1, FC2, FC5, areas. The magnitude of the source strength, a measure FC6, AF3, AF4, PO3 and PO4. of the energetic component, describes the allocation of Galvanic isolation of the participants was ensured by processing resources . The utilized LORETA version using an optical receiver (Biosemi New USB2 Receiver) was registered to the Talairach brain atlas [30,31]. The for trigger inputs, while in parallel, interference pickup solution space consisted of 2394 voxels with a spatial was also eliminated. The electrode cables were also resolution of 7 mm. LORETA images were constructed bundled to eliminate potential magnetic interference. for each subject averaging for his erroneous and correct The vertical electro-oculogram (EOG) was recorded responses, followed by voxel-by-voxel pairwise t-test bipolarly from electrodes placed above and below the comparisons. The structure probability maps atlas  eyes and the horizontal EOG was monitored from elec- was used to identify which brain regions were involved trodes at the outer canthi of the eyes. The data were fil- in theERP waveformsaswellasindifferences between teredoff-line, high-passat0.05Hzand low-pass at 35 the compared conditions (error vs correct responses). Hz with a zero-phase digital filter in both forward and Brain regions corresponding to the observed locations reverse directions. identified by the Talairach coordinates are reported All signals were digitized with a sampling rate of 256 [30,31]. Hz. All scalp signals were referenced online to both mastoids, but were later offline re-referenced to the Statistical analysis average of all scalp electrodes. Trials were averaged to The overall ratio of erroneous/correct responses was ERPs separately for each condition and each subject, 275/271. This ensured for all subjects an adequate signal relative to a 100 ms pre-stimulus baseline. To eliminate to noise optimization. Differences of fd1 and fd2 EOG artifacts, trials with EEG voltages exceeding 80 μV between the correct and erroneous responses were cal- were rejected from the average. culated using the paired t-test. All ERP analyses were performed using the LORETA Categorization of correct and erroneous responses software. Specifically the input data were the average The auditory frequency perception resolution in humans ERP values for each subject separately for the correct can be described in terms of an Equivalent Rectangular and error condition at each time frame from -100 to Bandwidth (ERB) around a stimulus frequency (Sf). 500 ms around the stimulus tone and at each of the According to psychoacoustics theory, the Equivalent 32 electrodes. Thus for each subject and each condition Rectangular Bandwidth (Be) in Hz can be approximated (i.e. correct and erroneous response) the input data -6 2 according to the following formula: B =6.2310 f + comprised 180 time frames × 32 electrodes giving a -2 9.339 10 f + 28.52, where f is the frequency of the total of 5760 averaged ERP values. sound. The discrimination between the participant’s These initial data were subjected to paired samples erroneous and non-erroneous responses was performed topographic analysis of variance (TANOVA), as well as with the use of the above formula. A subject’sresponse paired samples electrode-wise comparison of ERPs. The was considered correct if the response frequency (Rf) t-values were calculated via randomization using a was in the range between Sf-Be/2 and Sf+Be/2. For each Monte-Carlo method and were corrected for multiple trial starting from the second, two new variables were comparisons . The purpose of this analysis was two- calculated. The first one was the absolute frequency dif- fold. Firstly, to establish the time windows where differ- ference between the present and previous Sf (fd1). The ences between the two conditions are maximal and second one was the absolute frequency difference achieve statistical significance. Secondly, to locate the between the present Sf and the previous Rf (fd2). Conse- electrodes that were most instrumental in the formation quently the number of trials taken into consideration of these differences. Karanasiou et al. Behavioral and Brain Functions 2010, 6:14 Page 4 of 8 http://www.behavioralandbrainfunctions.com/content/6/1/14 Subsequently the ERP data were converted to LOR- between the two conditions occur at the areas of maxi- ETA files using the inverse solution of the software . mum activation. This procedure yields the brain activation maps at 2394 voxels. In the same manner these LORETA files were Discussion subjected to paired samples voxel-wise comparisons at In the present research we examined the patterns of sti- each time frame separately. Once again, the purpose mulus-locked N200 waveforms corresponding to subse- was to find the time window where statistically signifi- quent correct versus incorrect responses in relation to cant differences between the two conditions are maxi- the frequency deviation between consecutive stimulus mal, both in terms of absolute differences, and in terms tones and the frequency deviation between the present of the span of the time window itself. Finally, the appli- stimulus tone and response-related feedback tone that cation of pairwise comparisons of the average activation the subject heard just before. Results showed that mis- maps within the specific window revealed the most con- match conditions between two consecutive trials sequential clusters of voxels that differentiate the two increase the probability of errors, which are reflected in conditions. The level of statistical significance through- larger negative peaks of the N200 component at the out the tests was set at 0.05. fronto-central electrodes. This functional mapping of the human brain provides More specifically, greater values of fd1 that signify lar- a means to identify both the temporal and spatial char- ger stimulus frequency differences between two conse- acteristics of the differences between the two conditions, cutive trials create increased mismatch conditions for providing clues to the underlying mechanisms that qua- the subject to correctly identify the present stimulus fre- lify these differences. quency. The effect of mismatch on the subject’s response is even more obvious with respect to fd2, Results which is the difference between the present frequency Preliminary analysis revealed that the subjects’ erro- stimulus and the previous response frequency. For each neous responses within the 39 trials were identically dis- stimulus the subjects responds by positioning the slider. tributed. Conversely, the paired t-test revealed statistical Subsequently, the subject hears a tone corresponding to significant differences of the mean values of fd1 between this position. The subject expects that, by means of sim- the correct (138 ± 96 Hz) and erroneous (161 ± 89 Hz) ple comparison, this feedback information will aid him responses (mean difference = 23 Hz, t(544) = 2.96, p = in the next trial. However, if the stimulus frequency of 0.003). Even greater are the differences of the mean the next trial largely deviates from this response tone values of fd2 between the correct (125 ± 99 Hz) and the value of this feedback information is essentially inva- erroneous (154 ± 89 Hz) responses (mean difference = lidated, resulting in greater probability of committing an 29 Hz, t(544) = 3.60, p < 0.001). error. Consequently, any stimulus that is not similar to The TANOVA procedure revealed a time window at the previous tone will act as an oddball, creating a mis- 164-191 ms where differences between the two condi- match which results in an increased N200 and leads tions achieved statistical significance (p < 0.05). Subse- also to an error. In other words, the appearance of sti- quent paired samples electrode-wise comparisons of the muluslockedN200 andofsubsequentresponseerrors ERPs showed that electrodes Cz and Fz are the most both seem to originate from a common cause, namely consequential in the significant between conditions dif- the mismatch between the previous response and pre- ferences within this time window. As Figure 1 shows, sent stimulus frequencies. Stimulus frequencies that are both electrodes exhibit within this time window a signif- close together promote the subject’s ability to fine-tune icant negative peak. his/her response. Conversely two consecutive frequen- Figure 2 shows the LORETA solution at this negative cies that are further apart hinder the ears’ and ultimately peak for the two conditions. Maximum activation for the brain’s pattern-matching capabilities, which are both conditions was localized at (X = -3, Y = 45, Z = reflected in the increased negative amplitudes of the sti- -6) having best matches in the Talairach atlas at Brod- mulus-locked N200 component, and to inferior mann areas 10 and 11, medial frontal gyrus, frontal judgments. lobe and at Brodmann area 32, anterior cingulate, lim- The present results appear to be compatible with the biclobe. Themoreintense redcolourfor theerro- concept of the N200 system, according to which N200 neous responses in contrast to correct responses is based on a comparison between the current sound indicates greater activation of the specific regions. and a model-based concrete prediction of a forthcoming Interestingly the voxel-wise comparison of the activa- sound. An N200 auditory component, is commonly tion maps between the two conditions was localized at thought to reflect the outcome of a comparison process the same area (X = -3, Y = 45, Z = -6, t-value = 3.55, between the representation of the current event and a p < 0.05). This means that maximal differences representation (memory trace, neural model) of the Karanasiou et al. Behavioral and Brain Functions 2010, 6:14 Page 5 of 8 http://www.behavioralandbrainfunctions.com/content/6/1/14 Figure 1 Mean amplitude values at Cz and Fz electrodes around the stimulus tone. Amplitude values of the Cz and Fz electrodes in the time window -100 to 500 ms around the stimulus tone depending on the subjects’ subsequent correct and erroneous responses. Black lines depict the correct responses, red lines depict the errors. Dotted blue lines mark the time window of statistical significant differences between the two conditions regularities in the event history. Once a mismatch cortex and the other to the frontal cortex. As mentioned between the two representations is detected, N200 is eli- in the introduction section, reported findings are consis- cited [34-37]. This scheme appears to be in accordance tent with the observation of two sub-components of the with the model that N2 is related to the modulation of MMN; the early component (in the range of about 100- the early stages of response preparation and selection 140 ms) and the later component (in the range of about [38-40]. 140-200 ms) . The sources in the temporal areas are Moreover, the scalp distribution and the obtained thought to be involved in processing changes of the neural generators of the N200 appear to be in line with sound’s physical properties, whereas the sources on the the N2a source localization studies. The scalp-recorded frontal areas have been considered to reflect reorienta- MMN has its largest amplitude over the fronto-central tion of attention [18,41]. scalp areas. Maximal differences between the two condi- A frontal-lobe involvement in MMN generation was tions also occur at the areas of maximum activation. already proposed on the basis of only four-channel scalp Numerous studies have consistently reported evidence potential recordings [4,42,43]. This suggestion  was for two main locations concerning the generators of the supported by later analyses of the MMN scalp-potential MMN. The one location is referred to the temporal distribution, which indicated an MMN source in the Karanasiou et al. Behavioral and Brain Functions 2010, 6:14 Page 6 of 8 http://www.behavioralandbrainfunctions.com/content/6/1/14 Figure 2 Activation maps for the correct and error responses of the subjects for the time window 164-191 ms. Activation maps for the error (top map) and correct (middle map) responses of the subjects for the time window 164-191 ms. Differences (in t-values) between the activation maps for the two conditions (bottom map). frontal lobes [44,45]. Frontal MMN sources were also errors [58,59]. The implication of the ACC in the pre- suggested by studies using source-current modelling sent findings may be explained by the fact that the ERP  techniques. Furthermore, frontal MMN sources comparisons are based on correct and erroneous were also supported by intracranial ERP [47-49], PET responses. , and fMRI recordings [41,51-55] as well as by devel- opmental data . The role of prefrontal also genera- Conclusions tors is supported by studies of patients with prefrontal Analyses revealed that that there are significant differ- lesions who showed diminished temporal MMN ampli- ences in ERPs elicited at the stimulus tone depending tudes . on whether the subject’s subsequent response was cor- Besides the frontal neural generators also the ACC rect or erroneous. Both the differences in ERP patterns (Anterior Cingulate Cortex) seems to be involved in the at the stimulus tone and the differences in the responses observed ERP results. The ACC is typically linked to may be attributed to a common cause, which is the Karanasiou et al. Behavioral and Brain Functions 2010, 6:14 Page 7 of 8 http://www.behavioralandbrainfunctions.com/content/6/1/14 13. Näätänen R: Selective attention and evoked potentials in humans - a magnitudeofthe differencebetween thepreviousand critical review. 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Journal of Greece. Technological Education Institution of Athens, Greece. Psychophysiology 2007, 21(3-4):147-163. 22. Elton M, Spaan M, Ridderinkhof KR: Why do we produce errors of Authors’ contributions commission? An ERP study of stimulus deviance detection and error ISK and EIT performed the acquisition of the EEG data. MK, ISK and EIT monitoring in a choice go/no-go task. Eur J Neurosci 2004, contributed to the statistical analysis of the data. CP, ISK and EIT participated 20(7):1960-1968. to the interpretation of the results and composed the manuscript. GKM and 23. Savela J, Kujala T, Tuomainen J, Ek M, Aaltonen O, Näätänen R: The EMV participated to the interpretation of the results. NKU conceived the mismatch negativity and reaction time as indices of the perceptual core of the study design. NKU, GKM and EMV also revised the manuscript distance between the corresponding vowels of two related languages. critically. All authors read and approved the final manuscript. 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Behavioral and Brain Functions – Springer Journals
Published: Feb 23, 2010
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