Research in Developmental Disabilities 33 (2012) 655–662

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Research in Developmental Disabilities

Event related potential analysis of stimulus over-selectivity

Phil Reed a,*, Amy Savile a, Roberto Truzoli b

a Swansea University, UKb Universita degli Studi di Milano, Italy

A R T I C L E I N F O

Article history:

Received 14 November 2011

Received in revised form 18 November 2011

Accepted 18 November 2011

Available online 18 December 2011

Keywords:

Over-selectivity

Attention

Post-processing

ERP

EEG

A B S T R A C T

Stimulus over-selectivity is a phenomenon often displayed by individuals with many

forms of developmental and intellectual disabilities, and also by individuals lacking such

disabilities who are under cognitive strain. It occurs when only one of potentially many

aspects of the environment controls behavior. Adult participants were trained and tested

on a trial-and-error discrimination learning task, with a concurrent memory load task, and

displayed over-selectivity. Participants’ brain responses were also monitored and

analyzed using an electroencephalogram (EEG). The results demonstrated a significant

difference between the event-related potentials generated to the over-selected and under-

selected stimuli. Although there was no difference in the P300a wave between over- and

under-selected stimuli, the P300b wave was associated with over-selected, but not under-

selected stimuli. This finding suggests that, in this context, the under-selected stimulus did

not elicit ERP activity typically associated with novelty, which, in turn, suggests that over-

selectivity may not be entirely an attention-based effect.

� 2011 Elsevier Ltd. All rights reserved.

Stimulus over-selectivity refers to situations where a subset of elements from a complex stimulus controls behavior at theexpense of other equally salient elements of that stimulus situation (Dube, 2009; Reed & Gibson, 2005). This is a widelyacknowledged problem for individuals with developmental and intellectual disorders (Dube et al., 1999; Koegel &Schreibman, 1977; McHugh & Reed, 2007; Reed, Broomfield, McHugh, McCausland, & Leader, 2009; Wayland & Taplin,1985), and it also occurs with individuals without any form of disorder under conditions of high cognitive demand (e.g., Kim,Kim, & Chun, 2005; Reed & Gibson, 2005).

An experimental methodology used for exploring over-selectivity involves the use of a simultaneous discriminationlearning task (AB+ CD�). Participants are required to learn to respond to one stimulus (AB+) and not to another (CD�)stimulus (see Reynolds & Reed, 2011). Once the discrimination is acquired to criterion, an element of the previouslyreinforced stimulus (either A or B) is presented along with an element from the previously non-reinforced stimulus (either Cor D) in an extinction test (e.g., A vs. C; A vs. D; B vs. C; B vs. D), and the degree of responding to each component is measured.An equal level of responding to the separate components of the previously reinforced complex stimulus (A and B) is found inparticipants without any form of learning disability, or without a concurrent load. However, individuals with developmentaldisabilities, or those who are under cognitive strain (e.g., undertaking a second task), respond to one element from thepreviously reinforced compound (e.g., A) to a much greater extent to the other element (e.g., Koegel & Wilhelm, 1973; Reedet al., 2009; Reed & Gibson, 2005).

Given the range of populations with developmental and intellectual disabilities in which the over-selectivity effect isobserved, it is an important phenomenon to understand, both theoretically and for practical purposes. One widespread andimportant theory regarding over-selectivity is that it reflects the result of a failure to attend to all of the elements of the

* Corresponding author at: Department of Psychology, Swansea University, Singleton Park, Swansea SA2 8PP, UK. Tel.: +44 01792 602047.

E-mail address: p.reed@swansea.ac.uk (P. Reed).

0891-4222/$ – see front matter � 2011 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ridd.2011.11.012

P. Reed et al. / Research in Developmental Disabilities 33 (2012) 655–662656

compound stimulus during initial discrimination training. Thus, only those elements attended to during training cansubsequently control behavior (Dube et al., 1999).

A paradigm that is being increasingly used in the study of many behavioral phenomena is that of the event relatedpotential (ERP); a technology that allows description of the neurological correlates of those behavioral phenomena, andwhich can assist in the development of theoretical accounts of those effects. However, there have been few, if any, studies ofthe neurological correlates of over-selectivity, and such studies may help to illuminate the underlying mechanisms of theover-selectivity effect. Given that over-selectivity has been taken to reflect a failure of attention, then it might be expectedthat ERP responses to under-selected elements may involve systems that already have been identified as being related toattention processes.

A widespread paradigm that has been utilized to study attention using ERP technology is the ‘oddball’ procedure (seeCourchesne, Hillyard, & Galambos, 1975; Debener, Makeig, Delorme, & Engel, 2005; Katayama & Polich, 1996), which hasbeen used with participants with autism spectrum disorders (see Sokhadze et al., 2009). In the oddball procedure, a train ofsimilar stimuli are presented to the participant, with occasional deviants being interspersed at irregular intervals. When theERP correlates of this manipulation are studied, it has been found that the occasionally presented ‘deviant’ stimuli are mostoften associated with the elicitation of components of the P300 wave system (Courchesne et al., 1975; Daffner et al., 2011;Debener et al., 2005; Duncan-Johnson & Donchin, 1977). The P300 wave is a complex system, but can be broadlycharacterized as consisting of two components: an anterior component (P300a), in which there is a positive deflection, withmaximum amplitude around 250–400 ms after the stimulus presentation, and that is noted in central-frontal brain regions;and a posterior component (P300b), which has a slightly later maximum positive amplitude (300–600 ms post stimulus),and has a central-posterior location (see Barcelo, Perianez, & Knight, 2002; Belmonte, 2000; Daffner et al., 2011; Debeneret al., 2005; Friedman, Cycowicz, & Gatea, 2001, for descriptions). It is generally thought that the P300a component (the‘novelty P300’) reflects processes related to the orienting response (Barcelo et al., 2002), and is elicited by relatively novelevents (Friedman et al., 2001); while the P300b wave is closely associated with events of greater probability and relevance tothe task (Barcelo et al., 2002; Donchin, Spencer, & Dien, 1997).

Given this, if the under-selected element is not attended to during training, and is, therefore, relatively novel at test, thenthe P300 complex should include much P300a, and little P300b activity. However, although the attention-view of over-selectivity is a widely accepted and supported view (see Dube, 2009; Dube et al., 1999), there are alternative conceptions ofover-selectivity that do not involve the notion of attention. One of these views suggests that over-selectivity is a post-processing phenomenon, involving the suppression/inhibition of less important elements of a stimulus complex by the moreimportant aspects (see Reed, 2011, for a review). If this were the case, then it may be expected that there would be no noveltyP300 wave (P300a), but that the P300 wave evoked would include much P300b activity, and little P300a, at least, for the over-selected stimuli.

The current experiment, therefore, aimed to monitor the brain wave activity during an over-selectivity task (Reed &Gibson, 2005; Reynolds & Reed, 2011), in order to explore potential links between over-selectivity and brain wave activitydifferences in the brain responses to over-selected and under-selected stimulus items, and to further explore the theoreticalunderpinnings of this phenomenon.

1. Methods

1.1. Participants

Nineteen participants (17 males and 2 females) participated in this study. The participants were aged between 18 and 54(mean = 21.84) years. None of the participants had any documented type of learning difficulties, and were students fromSwansea University, who received no form of payment or credit.

1.2. Apparatus and materials

1.2.1. Over-selectivity task

Participants were presented with black-and-white stimuli (each 2 cm by 2 cm). The stimuli were presented on acomputer screen at a distance of approximately 0.5 m from the participant. The stimuli employed were symbols and shapesobtained from various fonts from Microsoft Word 2003 (Windings 1, Windings 2, Windings 3, and Bookshelf Symbol 7).

There were 60 stimuli used in total, with two stimuli used in each stimulus compound. The combination of stimuluselements that were reinforced were randomized, using the E-prime software, across participants to avoid any of the resultsbeing the product of some stimuli being intrinsically more salient than others.

1.2.2. Concurrent load

A concurrent load task was presented as previous reports have demonstrated that over-selectivity emerges in thispopulation with such a task (see Reynolds & Reed, 2011). Participants were required to subtract seven continuouslythroughout the whole study, starting from a random five digit number (e.g., 76,654). The participants were required to dothis verbally ‘out-loud’. If they failed to say a number, or slowed down, they were prompted to continue by the experimenter(‘‘go on, keep subtracting’’).

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1.3. Procedure

Each participant was tested individually in a small, quiet experimental room, with overhead lighting, a computermonitor, and the ERP equipment. Participants were seated facing the computer monitor, and the experimenter was presentat the beginning and end of each complete experimental trial. Prior to the training phase of each experimental trial,participants were presented with the concurrent load task, but they were not required to perform this task in the subsequentphases of the experiment.

1.3.1. Training phase

Each participant received an on-screen instruction for the task:

‘‘In the following, you will be presented with a fixation point, ‘+’, which will be followed by symbols to the right andleft. Please choose one by pressing ‘Left’ for the left symbol or ‘Right’ for the right symbol. Press either key to continue.’’

Participants were then presented with two compound stimuli simultaneously; each compound contained two elements.One compound was presented on the left of the screen, one element directly above the other, separated by 3 cm, and theother compound was presented, similarly, on the right of the screen. The same two compound stimuli were always presentedfor an individual participant within each repetition, but the compounds were presented randomly left to right, and theelements within the compound were presented randomly top to bottom across the trials.

Participants were instructed to select a compound rather than an individual element, and were informed that they wouldbe provided with feedback on their choices. On each trial, participants were presented with one compound stimulus (‘AB’)that, if selected, resulted in positive feedback in the form of the word ‘correct’ appearing on the computer screen. Ifparticipants selected the other compound stimulus (‘CD’) they received negative feedback in the form the word ‘incorrect’appearing on the screen.

Each trial was presented on screen until the participant made a choice. Participants were judged to have acquired thetraining discrimination once they produced 10 consecutively correct responses. To reduce the possibility of over-selectivitybeing caused by particular stimuli being intrinsically more salient than others, the actual stimuli that were the elements (i.e.,‘A’, ‘B’, ‘C’ and ‘D’) were different for each participant.

1.3.2. Test phase

Each participant received an on-screen instruction for the task:

‘‘Please continue to select the side that you think is correct. Press either the left or right key to continue.’’

During the test phase the participants were presented with two stimuli simultaneously, each comprising one elementfrom the previous compound stimuli. The elements were paired so that participants had a choice between an element fromthe previously reinforced stimuli and a component from the previously non-reinforced stimuli. There were five trials for eachcombination of previously positively reinforced and negatively reinforced elements (i.e., ‘A vs. C’, ‘A vs. D’, ‘B vs. C’ and ‘B vs.D’). No feedback was given during the test trials. Participants were instructed to select a one picture from the two displayed,by means of pressing the left or right button on the computer keypad.

1.3.3. Single symbol phase

Each participant received an on-screen instruction for the task:

‘‘In the following, you will see the fixation ‘+’, single symbols as you’ve seen before, and the smiley face symbol. Yourtask is to press either ‘left’ or ‘right’ when you see a smiley face. Press either key to continue.’’

Participants were presented with each of the four stimulus elements individually on screen in order to monitor brainactivity in response to the over-selected and under-selected stimulus elements (i.e., A and B) in comparison to the non-reinforced elements (i.e., C and D). Periodically, the participants were also presented with a novel stimulus element, such as apicture of a smiley face, which they were required to acknowledge by pressing either the left or the right key on the computerkeypad. This was done in order to keep the attention level of the participant during this part of the trial, as they were notrequired to press anything when they saw the previously presented elements. Each element was presented once.

Following the single stimulus exposure phase, the participants were given the whole procedure again, with a completelydifferent set of stimuli. They experienced 5 repetitions of the cycle (training, test, single stimulus) in order to produce enoughdata to analyze in terms of the EEG data, and to ensure that any ERP data was not stimulus-specific.

1.4. EEG data acquisition

EEG data was recorded continuously, sampled at 512 Hz, with a BioSemi Active-Two amplifier system, and analyzedoffline with BESA 5.1 software. Filter settings of 0–100 Hz were used when recording the EEG data. Electrocortical activitywas recorded from 64 ‘‘active’’ Ag/AgCl electrodes (BioSemi Active electrodes system) embedded in a cap covering the wholescalp, according to the International 10–20 system. All electrodes were referenced to Cz during the recording.

Fig. 1. Mean percentage of trials in which a component of the reinforced stimulus complex was chosen in preference to a component from the non-

reinforced complex.

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In order to reduce muscle artifacts in the EEG signal, the participant was instructed to assume a comfortable positionand avoid movements. The participant was instructed to look at the computer screen in-front of them, and to avoid anyunnecessary eye movements. Throughout the experiment, the behavior of the participant was observed on a TVmonitor, in order to check for any movements which may affect recordings. The participants were also instructed torespond as quickly and as accurately as possible to each set of stimuli by pressing the appropriate button on thekeyboard.

1.5. EEG data analysis

The analysis period was 1500 ms from the onset of the single stimuli (over-selected, under-selected, or thecontrol novel stimuli). The 200 ms period preceding the onset was used as a baseline. Eyeblink, and eye- and head-movements, were manually identified in the EEG recording, and EEG artifacts during these intervals were removed priorto analysis. Any artifacts with �120 mV were excluded from the averaging procedures. Data were only analyzed if there wassufficient data with no eye movement or eye blink artifacts. Before averaging, the EEG data were filtered with a 0.3-Hz high-pass filter, and a 40 Hz low-pass filter. Three types of recording were obtained for each participant in each of the fivereplications: over-selected stimuli (1500 ms preceding each stimulus presentation), under-selected (1500 ms from stimuluspresentation), and control (1500 ms from stimulus presentation). The ERP data were analyzed using the partial least squares(PLS) technique (see Lobaugh, West, & McIntosh, 2001). Statistical assessment was conducted as described by Braun et al.(1998).

2. Results

2.1. Behavioral data

The participants took a mean 7.18 trials (range of 5–71) before they consecutively choose the positively reinforcedstimulus during the training phases (mean of five exposures to the task). For the probe trials in the test phase, the meanpercentage of times that the elements from the previously reinforced stimulus were chosen by the participant wascalculated. The percentages for the element from the previously reinforced compound chosen most often were pooled acrossall five trails, as was the percentage for the element chosen less often.

Fig. 1 shows the group-mean percentage that the stimuli from the reinforced compound were each chosen relative to thestimulus from the previous negative compound. There was a substantial difference between the percentage of times the twoelements of the previously positively reinforced compound were chosen at test. A two-factor within-subject analysis ofvariance (ANOVA) with stimulus (most chosen vs. least chosen), and trial, as factors was conducted on these data. A rejectioncriterion of p < 0.05 was adopted for this analysis. This ANOVA revealed a statistically significant main effect of stimulus,F(1,18) = 5.50, but no statistically significant main effect of trial or interaction, ps > .10.

Further analysis on the mean data from all five trials was undertaken based on binomial theory to determine whetherchoices for the most-selected and least-selected stimuli were statistically different to chance (see Reynolds & Reed, 2011).The expected difference was 10.7%, and a paired t-test (one-tailed) was performed to compare the obtained difference andthe expected differences, which indicated a significant difference between the obtained and expected difference,t(18) = 3.67.

Fig. 2. Electrode salience for LV, with stable peak salience shown at the top of each plot.

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2.2. Event related potential data

The grand averages from the over-selected and under-selected stimuli in the single stimulus phase of the study areshown in Fig. 2. Visual examination of these data indicates a large positive deflection from 300 to 600 ms (i.e., a P300bwave) across the central and posterior electrodes, which was most strongly expressed at Pz in the over-selectivitycondition.

Fig. 3 shows the grand averaged ERPs from the five midline electrodes for the over-selected and under-selectedconditions. Visual examination of these ERPs indicates a peak at the Pz electrode, and this follows the classic distribution of aP300b component.

Fig. 4 shows the plots of the scalp scores by design scores for the LV. The latent variable (LV) was found to be significant bypermutation test (p < 0.007). The values for the design scores (DS) indicate the distinction on the LV was between the under-selected condition (DS = +0.67) and the over-selected condition (DS = �0.67).

3. Discussion

The present experiment aimed to explore the brain wave activity in relation to the over-selectivity effect, which has, thus,far has received scant attention in the literature. Stimulus over-selectivity was generated in adult participants performing aconcurrent task with no form of autism or learning disability. This result supports the previous demonstration of such an

Fig. 3. Grand averaged ERPs for each condition from four midline electrode sites.

P. Reed et al. / Research in Developmental Disabilities 33 (2012) 655–662660

effect under conditions of cognitive strain reported by Reed and Gibson (2005; Reynolds & Reed, 2011), and which is taken tomodel intellectual and developmental challenges.

The current findings revealed a difference between the ERPs of the under-selected and over-selected stimuli. Thisdifference comprised a greater P300b wave for the over-selected stimulus relative to the under-selected stimulus. Thisfinding is at odds with the predictions that could be derived from an attention-based account of over-selectivity (see Dubeet al., 1999), which are made on the basis of the results of oddball tasks (see Daffner et al., 2011; Debener et al., 2005). Thiswould suggest that the occurrence of the under-selected stimulus, having received less attention during training, would betreated as less probable at test, and would, therefore, elicit a P300a wave. Instead, the over-selected stimulus elicited a P300bwave, typically noted for task-relevant stimuli (see Belmonte, 2000). On face value, these results suggest that the attention-based view of over-selectivity cannot accommodate all of the findings.

However, there are a number of limitations on this conclusion that must be acknowledged and further investigated. Itmust be remembered that the prediction of a P300a wave elicited by an under-selected stimulus is based on generalisation ofthe results from oddball tasks to the current over-selectivity procedure, and it is unclear whether such a generalisation is

Fig. 4. Cross-block and scatter-plot of scalp scores by design scores for LV.

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warranted. Moreover, the current study was based on a model population, and not one with a developmental or intellectualdisorder. However, it should be noted that such a model population has shown highly similar results as high-functioningindividuals with autism spectrum conditions (see Reed et al., 2009). For these individuals, there is amble evidence that over-selectivity may be caused be similar mechanisms. However, it is unclear whether those with more severe intellectualimpairments would produce the same results (see Reed et al., 2009). Such results may serve to further explore whether thereare two forms of over-selectivity: one due to an attention-deficit, and one a post-processing disorder, which may be relatedto the severity of the intellectual impairment (see also Reed, 2006).

In sum, the current study demonstrated that there was significant stimulus over-selectivity in typically developingadults with a cognitive strain. It was also found that there was a significant difference between the event related potentialsof the over-selected and under-selected stimuli. The ERP for the over-selected stimuli was found to be a P300b, which mostlikely represents a response to a task relevant stimulus, and these data form the bases from which further study can bedeveloped.

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