Biological Psychology 105 (2015) 66–71
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Dual routes to cortical orienting responses: Novelty detection and uncertainty reduction Florian Lange a,∗ , Caroline Seer a , Mareike Finke b,c , Reinhard Dengler a , Bruno Kopp a a b c
Department of Neurology, Hannover Medical School, Hannover, Germany Cluster of Excellence “Hearing4all”, Germany Department of Otolaryngology, Hannover Medical School, Hannover, Germany
a r t i c l e
i n f o
Article history: Received 17 June 2014 Accepted 7 January 2015 Available online 14 January 2015 Keywords: Orienting response Novelty Uncertainty Event-related potentials (ERPs) Novelty P3 Uncertainty P3 Distractibility
a b s t r a c t Sokolov distinguished between reactive and proactive variants of the orienting response (OR). The Novelty P3 is considered as an electrophysiological signature of the reactive OR. Recent work suggests that the proactive OR is reflected in frontally distributed P3 activity elicited by uncertainty-reducing stimuli in task-switching paradigms. Here, we directly compare the electrophysiological signatures of reactive and proactive ORs. Participants completed a novelty oddball task and a task-switching procedure while the electroencephalogram was measured. Novel and uncertainty-reducing stimuli evoked prominent fronto-centrally distributed Novelty P3 and Uncertainty P3 waves, respectively. We found a substantial negative correlation between Novelty P3 and Uncertainty P3 across participants, suggesting that reactive and proactive ORs converge on a common neural pathway, but also that distinguishable routes to orienting exist. Moreover, response accuracy was associated with reduced Novelty-P3 and enhanced Uncertainty-P3 amplitudes. The relation between Novelty P3 and Uncertainty P3 might serve as an index of individual differences in distractibility and cognitive control. © 2015 Elsevier B.V. All rights reserved.
1. Introduction The orienting response (OR) toward novel, salient and informative stimuli may not constitute a unitary process (Barry, 1979). The traditional conception of the OR was that ORs are produced as a consequence of mismatch alone (reactive OR). Sokolov (1966) conceived the OR in the context of uncertainty, and he postulated the existence of conditioned ORs that represent directed enquiries of uncertainty-reducing stimuli (proactive OR). The frontally distributed Novelty P3 (or P3a) has been interpreted as an event-related potential (ERP) sign of the reactive OR because it shares the antecedent conditions of the reactive OR as well as its sensitivity to habituation (Barry, MacDonald, & Rushby, 2011; Friedman, Cycowicz, & Gaeta, 2001; Nieuwenhuis, de Geus, & Aston-Jones, 2011). The Novelty P3 is typically observed in response to novel distractors in oddball (Courchesne, Hillyard, & Galambos, 1975) or distraction paradigms (Escera, Alho, Winkler, & Näätänen, 1998) such that its amplitude has been proposed to reflect automatic shifts of attention toward task-irrelevant stimuli (Debener,
∗ Corresponding author at: Department of Neurology, Hannover Medical School, Carl-Neuberg-Straße 1, 30625 Hannover, Germany. Tel.: +49 511 532 3145. E-mail address: lange.fl[email protected] (F. Lange). http://dx.doi.org/10.1016/j.biopsycho.2015.01.001 0301-0511/© 2015 Elsevier B.V. All rights reserved.
Kranczioch, Herrmann, & Engel, 2002; Escera, Alho, Schröger, & Winkler, 2000). Prominent Novelty P3-like waveforms have also been observed in task-switching paradigms (Barceló, Perianez, & Knight, 2002; Barceló, Escera, Corral, & Perianez, 2006; Kopp, Tabeling, Moschner, & Wessel, 2006; Kopp, Lange, Howe, & Wessel, 2014; Nicholson, Karayanidis, Poboka, Heathcote, & Michie, 2005), suggesting the possibility that the Novelty P3 might also indicate controlled shifts of attention toward task-relevant stimuli (Barceló et al., 2002, 2006; Hölig & Berti, 2010). In a recent example, Kopp and Lange (2013) reported that frontal P3 activity was elicited by task-relevant feedback cues in a task-switching paradigm closely modeled after the Wisconsin Card Sorting Test (WCST; Berg, 1948). Kopp and Lange (2013) suggested that these ERP waveforms (henceforth referred to as Uncertainty P3) constitute an indicator of the proactive OR because these feedback cues were highly informative (i.e., they reduced participants’ uncertainty about the valid task rules, see Fig. 1). Crucially, this analysis implies that the reactive OR and the proactive OR share a common neural pathway, the activation of which is responsible for the generation of the Novelty P3 and the Uncertainty P3, respectively (Barceló et al., 2006). Our study was designed to compare frontal P3 waveforms elicited by task-irrelevant novels on a three-stimulus oddball task and task-relevant feedback cues in a three-rule task-switching
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distractibility. Specifically, we hypothesized behavioral distractibility (as indexed by response accuracy on the two paradigms) to be associated with increased orienting to task-irrelevant stimuli (i.e., increased Novelty-P3 amplitudes) as well as with difficulties in allocating attention to task-relevant stimuli (i.e., decreased amplitudes of the Uncertainty P3). 2. Methods A group of sixteen healthy, right-handed students (14 female) participated for course credit. Participants’ age ranged from 19 to 34 years (M = 25.5, SD = 4.32). All had normal or corrected-to-normal vision. 2.1. Task and procedure Participants completed an auditory novelty oddball task as well as a three-rule task-switching procedure modeled after the WCST (Berg, 1948; Grant & Berg, 1948; Heaton, 1993). Both tasks were designed using the Presentation® software (Neurobehavioral Systems, Albany, CA) and displayed on a 24 in. flat screen (Eizo EV2416W, Eizo, Hakusan, Japan). Auditory stimuli were amplified (Pioneer Stereo Amplifier A-109, Pioneer, Kanagawa, Japan) and presented via Heco Victa 200 loudspeakers (Heco, Pulheim, Germany). Responses were collected by a Cedrus response pad (RB 830, Cedrus, San Pedro, CA). All participants completed the oddball task first to minimize the impact of additional sources of variance (e.g., fatigue effects) when correlating individual performances across paradigms (Carlson & Wang, 2007).
Fig. 1. Task flow of the task-switching paradigm modeled after the Wisconsin Card Sorting Test. Participants were instructed to match a target card to one of four key cards according to the correct sorting rule. Target cards varied on three dimensions (color, shape, number) which defined the three viable task rules. Task rules switched in an unpredictable manner. Feedback cues following each sorting response indicated whether the applied rule had to be changed (“SWITCH”) or maintained (“REPEAT”). Switch cues rendered the participants uncertain about which of the two remaining rules was correct. Informative feedback cues following the subsequent sorting response enabled participants to induce the correct rule. Redundant repeat cues on subsequent trials did not reduce participants’ uncertainty about the valid task rules further.
paradigm. Notice that while both Novelty P3 and Uncertainty P3 might index a similar process of attentional orienting, the two waveforms can be readily dissociated based on quality and direction of these attentional shifts. In the three-stimulus oddball task, the Novelty P3 has been suggested to reflect automatic shifts of attention to task-irrelevant stimuli, whereas in task switching, frontal P3 activity has been linked to controlled shifts of attention to task-relevant events. In line with this functional dissociation, groups of distractible patients have been observed to generate enhanced frontal P3 amplitudes in response to taskirrelevant stimuli (Grillon, Courchesne, Ameli, Geyer, & Braff, 1990; Kaipio et al., 1999; Polo et al., 2003), but to exhibit attenuated amplitudes following task-relevant stimuli (Anderson, Baldridge, & Stanford, 2011). Crucially, neuroanatomical data indicate a competition between the neural activations underlying task-relevant and task-irrelevant attention: increased attention to task-relevant events is associated with decreases in task-irrelevant attention and vice versa (Fox et al., 2005). To date, evidence for such an antagonistic relationship between reactive and proactive OR on the level of electrophysiological responses is still lacking. Here, we aim to compensate for this lack by exploring the relationship between frontal P3 waveforms elicited by task-relevant and task-irrelevant stimuli. We expected amplitudes of the Novelty P3 (elicited by irrelevant distractors) to be negatively correlated with amplitudes of the Uncertainty P3 (elicited by relevant feedback cues). Further, drawing on the clinical literature reviewed above (Anderson et al., 2011; Grillon et al., 1990; Kaipio et al., 1999; Polo et al., 2003), we attempted to dissociate Novelty P3 and Uncertainty P3 based on their respective relations to behavioral
2.1.1. Three-stimulus oddball task Auditory stimuli for the three-stimulus oddball task consisted of standard and target sinusoidal tones as well as 45 distinct novel environmental sounds (Escera et al., 1998) presented with probabilities of .70, .15 and .15, respectively (65 dB, 200 ms duration, 10 ms rise/fall). Target and standard stimuli differed in pitch (600 Hz vs. 700 Hz), with target assignment being counterbalanced across participants. Participants were instructed to respond as fast as possible whenever they detected a target tone, but to withhold responding to the remaining stimuli. Stimuli were randomly distributed across 300 trials with the constraint that two novel stimuli did not follow each other in direct sequence. Inter-stimulus intervals varied according to a uniform distribution, ranging from 950 ms to 1450 ms in steps of 50 ms. 2.1.2. Three-rule task-switching paradigm The task switching paradigm required participants to match a target card to one of four key cards according to a particular sorting rule that changed from time to time (Barceló et al., 2002; Kopp & Lange, 2013). Cards were configured around the center of the screen with the target card appearing below the key cards (see Fig. 1). Participants indicated their sorting choice by pressing one of four keys on the response pad which mapped to the spatial position of the key cards on the screen. Target cards varied on three dimensions (color, shape, number), and these dimensions equaled the three viable task rules. As the target card never shared more than one attribute with any of the keycards, the applied sorting rule could unambiguously be identified (Barceló, 2003; Nelson, 1976). Target displays remained on screen until a response was registered. After a fixed response-cue interval (RCI) of 1000 ms, a feedback cue was presented for 200 ms indicating whether the applied sorting rule should be maintained (“BLEIBEN” [“REPEAT”]) or changed (“WECHSELN” [“SWITCH”]) on the upcoming trial. Subsequent target stimuli appeared after a fixed cue-target interval (CTI) of 1000 ms. Note that switch cues provided implicit information about the currently valid task rule: their occurrence signaled that the previously adopted task rule had changed, thus rendering participants uncertain about which of the two remaining rules was the correct one (West, Langley, & Bailey, 2011). Ideally performing participants would choose one of the two remaining rules on the subsequent trial. Informative feedback cues that followed their initial guess enabled participants to induce the correct rule (see Fig. 1). In contrast, redundant repeat cues on subsequent trials did not reduce participants’ uncertainty about the valid task rules further. Rules changed in an unpredictable manner (Altmann, 2004) after runs of two or more repeat trials (average run length: 3.5 trials). Participants completed 40 task runs involving 39 switch trials. Prior to the experimental sequence, five practice runs were administered. Participants were informed about the three possible sorting criteria and about the fact that the valid task rule would change from time to time in an unpredictable manner. They were told to attend to the feedback cues in order to infer the correct task rule. 2.2. Electrophysiological recordings Continuous electroencephalogram was recorded from 30 active Ag-AgCl electrodes (BrainProducts, Gilching, Germany) placed according to the international 10–20 system. BrainVision Recorder software (Brain Products, Gilching, Germany) was used. Electrode impedance was kept below 10 k. Electrodes were referenced to FCz electrode. Vertical (vEOG) and horizontal (hEOG) electrooculogram were
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recorded with two additional electrodes positioned at the suborbital ridge and the external ocular canthus of the right eye. EEG and EOG channels were digitized at 250 Hz and amplified using a BrainAmp amplifier (Brain Products, Gilching, Germany). 2.3. Data analysis 2.3.1. Behavioral data As indicator for participants’ distractibility, response accuracy was determined separately for the three-stimulus oddball task and the task-switching paradigm. In the oddball task, error rates were composed of the number of false alarms (responses to standard and novel stimuli) and the number of misses (failures to respond to target stimuli). In the task-switching paradigm, we analyzed the proportion of errors on the second trial after the switch cue (i.e., after informative feedback cues allowed for rule induction). We refer to these measures of behavioral distractibility as oddball errors and task-switching errors, respectively. 2.3.2. Electrophysiological data Electrophysiological data were evaluated using BrainVision Analyzer 2.0 (Brain Products, Gilching, Germany). After filtering (high-pass: 0.5 Hz, low-pass: 70 Hz, notch: 50 Hz), data were screened for non-stereotyped artifacts and subjected to an ocular-correction independent component analysis (Groppe, Makeig, & Kutas, 2008) for further removal of ocular, muscular, and cardiac artifacts. Data were rereferenced to a common average reference offline, and segmented into epochs from −200 to 1000 ms relative to the onset of auditory stimuli (oddball task) and feedback stimuli (task-switching paradigm). After baseline-correction (−200 to 0 ms), residual artifacts were rejected semi-automatically before data were averaged. ERPs were locked to novel and standard stimuli in the oddball task, as well as to informative and redundant feedback cues in the task-switching procedure. Mean Novelty-P3 and Uncertainty-P3 amplitudes were measured at electrode FCz in a 120 ms interval around individual P3 peak latencies. Peak latencies corresponded to the largest positive deflection in individual ERP waveforms within the latency range between 240 and 380 ms (Novelty P3) or between 320 and 460 ms (Uncertainty P3). The difference between P3 amplitudes elicited by novel vs. standard stimuli served as measure of the Novelty P3. The difference between P3 amplitudes elicited by informative vs. redundant feedback cues served as measure of the Uncertainty P3. 2.3.3. Statistical analysis Statistical analyses were performed using SPSS 21.0 (IBM, Armonk, NY). The level of significance was set at ˛ = .05. Novelty effects in the oddball procedure were examined by means of a paired ttest comparing P3 amplitudes elicited by novel and standard stimuli at electrode FCz. Uncertainty effects in the oddball procedure were examined by means of a paired ttest comparing P3 amplitudes elicited by informative and redundant feedback cues at electrode FCz. Note that we deliberately chose to restrict our analyses to the informative repeat feedback cues (i.e., repeat cues following the initial guess) since these stimuli were physically identical to the redundant repeat cues (i.e., both events were characterized by the presentation of the German word for repeat, “BLEIBEN”). To examine commonalities between the electrophysiological and behavioral measures obtained from the two paradigms, Pearson correlation coefficients were calculated for the pairwise relationships between Novelty P3, Uncertainty P3, oddball errors and task-switching errors. To further illustrate the relationship between behavioral distractibility and P3 amplitudes, we divided our sample into two subgroups of high and low performers based on the number of task-switching errors. Data were then subjected to a subgroup (high performer vs. low performer) × waveform (Novelty P3 vs. Uncertainty P3) analysis of variance (ANOVA). For this subgroup analysis, we chose to focus on task-switching errors as this measure was more sensitive to individual differences than the number of oddball errors. Results did not differ qualitatively when the number of oddball errors or an aggregate error measure were used instead.
3. Results Both novel stimuli and informative feedback cues elicited prominent P3 amplitudes with comparable fronto-central topography (Fig. 2A, Table 1). Mean amplitudes at electrode FCz were higher for novel vs. standard stimuli (t = 4.89, p < .001) and for informative vs. redundant feedback cues (t = 4.55, p < .001). Note that amplitude differences were also statistically reliable at Fz and Cz, but not at Pz, both for the Novelty-P3 and the Uncertainty-P3 contrast (Table 1). We found a substantial negative correlation between individual P3 effects in the two paradigms (r = −.79, p < .001; Fig. 2B), implying that individuals who showed a large Novelty P3 produced only small Uncertainty-P3 amplitudes and vice versa. This relationship remained significant when the individuals showing minimum and maximum Novelty-P3 and Uncertainty-P3 amplitude were
Table 1 Waveform characteristics of Novelty P3 and Uncertainty P3.
Mean latency in ms (SD) Mean amplitude at Fz in V (SD) Mean amplitude at FCz in V (SD) Mean amplitude at Cz in V (SD) Mean amplitude at Pz in V (SD)
Novelty P3
Uncertainty P3
303.38 (32.39) 3.36 (2.48)* 3.49 (2.86)* 2.47 (1.65)* 0.49 (2.26)
413.25 (29.53) 2.53 (2.75)* 2.88 (2.53)* 2.04 (1.67)* 0.41 (2.36)
Note. Novelty P3 and Uncertainty P3 amplitude differences were calculated as the amplitude differences between novel and standard stimuli and between informative and redundant feedback cues, respectively. * Significantly different from zero at the 5% level.
Table 2 Associations between electrophysiological and behavioral measures.
Novelty P3 Uncertainty P3 Oddball errors Task switching errors * ** ***
Novelty P3
Uncertainty P3
Oddball errors
−.79*** .66*** .66***
−.54** −.49*
.38
p < .10. p < .05. p < .01.
removed from the sample (n = 13; r = −.68, p = .010) indicating that our finding is not driven by outliers. At the behavioral level, participants committed an average of 4.06 (SD = 4.84) errors in the oddball task and chose an incorrect sorting criterion on 21% (SD = 17%) of the analyzed trials in the task-switching procedure. Both error measures were positively related to the magnitude of the Novelty P3 while being negatively associated with UncertaintyP3 amplitude (Table 2). Based on error rates in the task-switching paradigm, we divided our sample into two subgroups of high (M = .09) and low (M = .32) performers. These subgroups differed with regard to how effectively participants induced the correct rule following informative feedback cues (t = 3.79, p = .002), while yielding similar age (t = 1.30, p = .21) and gender (one male each) distributions. Crucially, frontal P3 responses allowed for a double dissociation of these groups as indicated by a significant subgroup × P3 waveform interaction (F(1,14) = 4.76, p = .047, 2p = .25, Fig. 2C). High-performing individuals tend to show larger Uncertainty-P3 amplitudes (t = 2.02, p = .063) and smaller NoveltyP3 amplitudes (t = −2.03, p = .061) than low performers. 4. Discussion Novelty P3 (elicited by irrelevant distractors) and Uncertainty P3 (elicited by relevant feedback cues) closely resembled each other with regard to amplitude and scalp topography, possibly indicating that reactive and proactive forms of the OR converge on a common neural pathway (Sokolov, 1966; Kopp & Lange, 2013). However, amplitudes of the Novelty P3 and those of the Uncertainty P3 were strongly negatively correlated. These findings seem to contradict the traditional view that the OR constitutes a unitary process. They support the conception that novelty detection and uncertainty reduction represent functionally dissociable routes to the neural underpinnings of the OR, here labeled reactive and proactive OR, respectively. Further, response accuracy was associated with decreased Novelty-P3 amplitudes and with increased amplitudes of the Uncertainty P3. These findings point into the direction that the balance between Novelty P3 and Uncertainty P3 might represent a trait variable related to individuals’ distractibility. Specifically, this electrophysiological indicator may reflect the neural substrates of individual capabilities to focus on task-relevant information and to attenuate distractor interference (Desimone & Duncan, 1995;
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Fig. 2. ERP results from the task-switching paradigm and the auditory novelty oddball task. (A) Grand average waveforms locked to novel and standard stimuli in the oddball task (left) and to informative and redundant feedback (FB) cues in the task-switching procedure (right). Both novel stimuli and informative FB cues elicited prominent anterior P3 waveforms. Scalp maps indicate topographies of the Novelty P3 (novel–standard) and the Uncertainty P3 (informative FB–redundant FB), measured in a 120 ms interval around mean peak latencies (Novelty P3: 303 ms, Uncertainty P3: 413 ms). The color scale for scalp maps ranges from -3 V to 3 V. (B) Amplitudes of the Novelty P3 (novel–standard) and the Uncertainty P3 (informative FB–redundant FB) are negatively related to each other (p < .001). (C) Scalp topographies of the Novelty P3 (novel–standard) and the Uncertainty P3 (informative FB–redundant FB), separated for subgroups of high-performing and low-performing individuals. Subgroups were defined according to the number of errors committed after the first, informative FB cue in the task-switching paradigm (median split). Low-performing individuals (who were less likely to infer the correct task rule after an informative FB cue) generated larger Novelty-P3 amplitudes, but smaller Uncertainty-P3 amplitudes.
Forster & Lavie, 2014; McNab & Dolan, 2014). Our findings are consistent with the notion of two distinct neuroanatomical networks underlying task-relevant and task-irrelevant attention (Corbetta & Shulman, 2002). Most important to the current findings, activity of these networks has been found to be negatively correlated, thus indicating a competitive interaction of the brain’s attentional systems (Fox et al., 2005). Our data illustrate a comparable antagonistic relationship on the level of electrophysiological scalp potentials. Small Novelty-P3 and large Uncertainty-P3 amplitudes appear to be indicative of a rather controlled mode of attentional orienting, while large Novelty-P3 and small Uncertainty-P3 reflect a relative dominance of automatic determinants of attentional focus. Our results can also be reconciled with those models of the OR which highlight the role of stimulus significance in determining ORs (Bernstein, 1979; Bradley, 2009; Maltzman, 1979). According to
these models, ORs are not produced as a consequence of mismatch alone. Instead, Bernstein (1979) proposed that the threshold for the elicitation of ORs is exceeded only if stimuli possess sufficient significance in the present context. To illustrate how significance models account for our results, consider two individuals with relatively high and relatively low threshold levels for the elicitation of the OR, respectively. The high-threshold individual will show weak ORs in comparison to the low-threshold individual when encountering task-irrelevant novel stimuli in oddball tasks since their significance does not exceed the threshold which is required for the elicitation of ORs. Novel oddball stimuli thus elicit small amplitudes of the Novelty P3 in these individuals. High-threshold individuals will, however, orient selectively to informative feedback cues in the task-switching paradigm because informative feedback cues provide significant information for successful task performance.
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These informative feedback cues thus elicit ORs, reflected in large amplitudes of the Uncertainty P3. In contrast, task-irrelevant novel stimuli are more likely to elicit ORs in low-threshold individuals. This results in increased amplitudes of the Novelty P3 and reduced amplitudes of the Uncertainty P3 (due to less differential responding to informative and redundant feedback cues). As a consequence, assuming that stimulus significance contributes substantially to ORs and that individuals vary with regard to OR thresholds might account for the negative correlation of Novelty P3 and Uncertainty P3 that we found in our study. While task-relevant and task-irrelevant stimuli elicited P3 waveforms of comparable amplitude and scalp topography, it has to be noticed that Novelty P3 and Uncertainty P3 differ in latency, with Novelty P3 peaking about 100 ms earlier than Uncertainty P3. This latency difference might be interpreted as challenging our view of a common electrophysiological correlate of reactive and proactive OR. Note, however, that Uncertainty P3 was locked to visual stimuli while Novelty P3 was locked to auditory stimuli. Hence, the observed latency difference might simply be due to auditory information being processed more rapidly than visual information (Romero & Polich, 1996; Woodworth & Schlosberg, 1954). Future studies on the relationship between Novelty P3 and Uncertainty P3 should measure both waveforms within the same modality to control for these processing differences. In sum, our study demonstrates that phenomenologically similar frontal P3 waveforms can be associated with both, proactive attentional orienting to task-relevant stimuli and reactive attentional orienting to task-irrelevant stimuli. Individuals differ with regard to the relative dominance of these two attentional responses and this variation relates to individual differences in behavioral distractibility. The present study constitutes a first step toward an electrophysiological characterization of the competitive interaction between task-relevant and task-irrelevant attention. Further research into the balance between Novelty P3 and Uncertainty P3 might help to shed light on this complex interaction and the functional role of proactive and reactive OR. Acknowledgements F.L. received funding from the German National Academic Foundation. In addition, the research reported here was supported by a grant from the Petermax-Müller-Stiftung, Hannover, Germany. The authors thank Moritz Boos and Andreas Niesel for technical support. References Altmann, E. M. (2004). Advance preparation in task switching: What work is being done? Psychological Science, 15(9), 616–622. http://dx.doi.org/10. 1111/j. 0956-7976.2004.00729.x Anderson, N. E., Baldridge, R. M., & Stanford, M. S. (2011). P3a amplitude predicts successful treatment program completion in substance-dependent individuals. Substance Use & Misuse, 46(5), 669–677. http://dx.doi.org/ 10.3109/10826084.2010.528123 Barceló, F. (2003). The Madrid card sorting test (MCST): A task switching paradigm to study executive attention with event-related potentials. Brain Research Protocols, 11(1), 27–37. http://dx.doi.org/10.1016/S1385-299X(03)00013-8 ˜ Barceló, F., Escera, C., Corral, M. J., & Periánez, J. A. (2006). Task switching and novelty processing activate a common neural network for cognitive control. Journal of Cognitive Neuroscience, 18(10), 1734–1748. http://dx.doi.org/ 10.1162/jocn.2006.18.10.1734 ˜ Barceló, F., Periánez, J. A., & Knight, R. T. (2002). Think differently: A brain orienting response to task novelty. NeuroReport, 13(15), 1887–1892. Barry, R. J. (1979). A factor-analytic examination of the unitary OR concept. Biological Psychology, 8(3), 161–178. http://dx.doi.org/10.1016/0301-0511(79)90045-0 Barry, R. J., MacDonald, B., & Rushby, J. A. (2011). Single-trial event-related potentials and the orienting reflex to monaural tones. International Journal of Psychophysiology, 79(2), 127–136. http://dx.doi.org/10.1016/j.ijpsycho.2010.09.010 Berg, E. A. (1948). A simple objective technique for measuring flexibility in thinking. The Journal of General Psychology, 39(1), 15–22. http://dx.doi.org/10. 1080/00221309.1948.9918159
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Contents lists available at ScienceDirect
Biological Psychology journal homepage: www.elsevier.com/locate/biopsycho
Dual routes to cortical orienting responses: Novelty detection and uncertainty reduction Florian Lange a,∗ , Caroline Seer a , Mareike Finke b,c , Reinhard Dengler a , Bruno Kopp a a b c
Department of Neurology, Hannover Medical School, Hannover, Germany Cluster of Excellence “Hearing4all”, Germany Department of Otolaryngology, Hannover Medical School, Hannover, Germany
a r t i c l e
i n f o
Article history: Received 17 June 2014 Accepted 7 January 2015 Available online 14 January 2015 Keywords: Orienting response Novelty Uncertainty Event-related potentials (ERPs) Novelty P3 Uncertainty P3 Distractibility
a b s t r a c t Sokolov distinguished between reactive and proactive variants of the orienting response (OR). The Novelty P3 is considered as an electrophysiological signature of the reactive OR. Recent work suggests that the proactive OR is reflected in frontally distributed P3 activity elicited by uncertainty-reducing stimuli in task-switching paradigms. Here, we directly compare the electrophysiological signatures of reactive and proactive ORs. Participants completed a novelty oddball task and a task-switching procedure while the electroencephalogram was measured. Novel and uncertainty-reducing stimuli evoked prominent fronto-centrally distributed Novelty P3 and Uncertainty P3 waves, respectively. We found a substantial negative correlation between Novelty P3 and Uncertainty P3 across participants, suggesting that reactive and proactive ORs converge on a common neural pathway, but also that distinguishable routes to orienting exist. Moreover, response accuracy was associated with reduced Novelty-P3 and enhanced Uncertainty-P3 amplitudes. The relation between Novelty P3 and Uncertainty P3 might serve as an index of individual differences in distractibility and cognitive control. © 2015 Elsevier B.V. All rights reserved.
1. Introduction The orienting response (OR) toward novel, salient and informative stimuli may not constitute a unitary process (Barry, 1979). The traditional conception of the OR was that ORs are produced as a consequence of mismatch alone (reactive OR). Sokolov (1966) conceived the OR in the context of uncertainty, and he postulated the existence of conditioned ORs that represent directed enquiries of uncertainty-reducing stimuli (proactive OR). The frontally distributed Novelty P3 (or P3a) has been interpreted as an event-related potential (ERP) sign of the reactive OR because it shares the antecedent conditions of the reactive OR as well as its sensitivity to habituation (Barry, MacDonald, & Rushby, 2011; Friedman, Cycowicz, & Gaeta, 2001; Nieuwenhuis, de Geus, & Aston-Jones, 2011). The Novelty P3 is typically observed in response to novel distractors in oddball (Courchesne, Hillyard, & Galambos, 1975) or distraction paradigms (Escera, Alho, Winkler, & Näätänen, 1998) such that its amplitude has been proposed to reflect automatic shifts of attention toward task-irrelevant stimuli (Debener,
∗ Corresponding author at: Department of Neurology, Hannover Medical School, Carl-Neuberg-Straße 1, 30625 Hannover, Germany. Tel.: +49 511 532 3145. E-mail address: lange.fl[email protected] (F. Lange). http://dx.doi.org/10.1016/j.biopsycho.2015.01.001 0301-0511/© 2015 Elsevier B.V. All rights reserved.
Kranczioch, Herrmann, & Engel, 2002; Escera, Alho, Schröger, & Winkler, 2000). Prominent Novelty P3-like waveforms have also been observed in task-switching paradigms (Barceló, Perianez, & Knight, 2002; Barceló, Escera, Corral, & Perianez, 2006; Kopp, Tabeling, Moschner, & Wessel, 2006; Kopp, Lange, Howe, & Wessel, 2014; Nicholson, Karayanidis, Poboka, Heathcote, & Michie, 2005), suggesting the possibility that the Novelty P3 might also indicate controlled shifts of attention toward task-relevant stimuli (Barceló et al., 2002, 2006; Hölig & Berti, 2010). In a recent example, Kopp and Lange (2013) reported that frontal P3 activity was elicited by task-relevant feedback cues in a task-switching paradigm closely modeled after the Wisconsin Card Sorting Test (WCST; Berg, 1948). Kopp and Lange (2013) suggested that these ERP waveforms (henceforth referred to as Uncertainty P3) constitute an indicator of the proactive OR because these feedback cues were highly informative (i.e., they reduced participants’ uncertainty about the valid task rules, see Fig. 1). Crucially, this analysis implies that the reactive OR and the proactive OR share a common neural pathway, the activation of which is responsible for the generation of the Novelty P3 and the Uncertainty P3, respectively (Barceló et al., 2006). Our study was designed to compare frontal P3 waveforms elicited by task-irrelevant novels on a three-stimulus oddball task and task-relevant feedback cues in a three-rule task-switching
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distractibility. Specifically, we hypothesized behavioral distractibility (as indexed by response accuracy on the two paradigms) to be associated with increased orienting to task-irrelevant stimuli (i.e., increased Novelty-P3 amplitudes) as well as with difficulties in allocating attention to task-relevant stimuli (i.e., decreased amplitudes of the Uncertainty P3). 2. Methods A group of sixteen healthy, right-handed students (14 female) participated for course credit. Participants’ age ranged from 19 to 34 years (M = 25.5, SD = 4.32). All had normal or corrected-to-normal vision. 2.1. Task and procedure Participants completed an auditory novelty oddball task as well as a three-rule task-switching procedure modeled after the WCST (Berg, 1948; Grant & Berg, 1948; Heaton, 1993). Both tasks were designed using the Presentation® software (Neurobehavioral Systems, Albany, CA) and displayed on a 24 in. flat screen (Eizo EV2416W, Eizo, Hakusan, Japan). Auditory stimuli were amplified (Pioneer Stereo Amplifier A-109, Pioneer, Kanagawa, Japan) and presented via Heco Victa 200 loudspeakers (Heco, Pulheim, Germany). Responses were collected by a Cedrus response pad (RB 830, Cedrus, San Pedro, CA). All participants completed the oddball task first to minimize the impact of additional sources of variance (e.g., fatigue effects) when correlating individual performances across paradigms (Carlson & Wang, 2007).
Fig. 1. Task flow of the task-switching paradigm modeled after the Wisconsin Card Sorting Test. Participants were instructed to match a target card to one of four key cards according to the correct sorting rule. Target cards varied on three dimensions (color, shape, number) which defined the three viable task rules. Task rules switched in an unpredictable manner. Feedback cues following each sorting response indicated whether the applied rule had to be changed (“SWITCH”) or maintained (“REPEAT”). Switch cues rendered the participants uncertain about which of the two remaining rules was correct. Informative feedback cues following the subsequent sorting response enabled participants to induce the correct rule. Redundant repeat cues on subsequent trials did not reduce participants’ uncertainty about the valid task rules further.
paradigm. Notice that while both Novelty P3 and Uncertainty P3 might index a similar process of attentional orienting, the two waveforms can be readily dissociated based on quality and direction of these attentional shifts. In the three-stimulus oddball task, the Novelty P3 has been suggested to reflect automatic shifts of attention to task-irrelevant stimuli, whereas in task switching, frontal P3 activity has been linked to controlled shifts of attention to task-relevant events. In line with this functional dissociation, groups of distractible patients have been observed to generate enhanced frontal P3 amplitudes in response to taskirrelevant stimuli (Grillon, Courchesne, Ameli, Geyer, & Braff, 1990; Kaipio et al., 1999; Polo et al., 2003), but to exhibit attenuated amplitudes following task-relevant stimuli (Anderson, Baldridge, & Stanford, 2011). Crucially, neuroanatomical data indicate a competition between the neural activations underlying task-relevant and task-irrelevant attention: increased attention to task-relevant events is associated with decreases in task-irrelevant attention and vice versa (Fox et al., 2005). To date, evidence for such an antagonistic relationship between reactive and proactive OR on the level of electrophysiological responses is still lacking. Here, we aim to compensate for this lack by exploring the relationship between frontal P3 waveforms elicited by task-relevant and task-irrelevant stimuli. We expected amplitudes of the Novelty P3 (elicited by irrelevant distractors) to be negatively correlated with amplitudes of the Uncertainty P3 (elicited by relevant feedback cues). Further, drawing on the clinical literature reviewed above (Anderson et al., 2011; Grillon et al., 1990; Kaipio et al., 1999; Polo et al., 2003), we attempted to dissociate Novelty P3 and Uncertainty P3 based on their respective relations to behavioral
2.1.1. Three-stimulus oddball task Auditory stimuli for the three-stimulus oddball task consisted of standard and target sinusoidal tones as well as 45 distinct novel environmental sounds (Escera et al., 1998) presented with probabilities of .70, .15 and .15, respectively (65 dB, 200 ms duration, 10 ms rise/fall). Target and standard stimuli differed in pitch (600 Hz vs. 700 Hz), with target assignment being counterbalanced across participants. Participants were instructed to respond as fast as possible whenever they detected a target tone, but to withhold responding to the remaining stimuli. Stimuli were randomly distributed across 300 trials with the constraint that two novel stimuli did not follow each other in direct sequence. Inter-stimulus intervals varied according to a uniform distribution, ranging from 950 ms to 1450 ms in steps of 50 ms. 2.1.2. Three-rule task-switching paradigm The task switching paradigm required participants to match a target card to one of four key cards according to a particular sorting rule that changed from time to time (Barceló et al., 2002; Kopp & Lange, 2013). Cards were configured around the center of the screen with the target card appearing below the key cards (see Fig. 1). Participants indicated their sorting choice by pressing one of four keys on the response pad which mapped to the spatial position of the key cards on the screen. Target cards varied on three dimensions (color, shape, number), and these dimensions equaled the three viable task rules. As the target card never shared more than one attribute with any of the keycards, the applied sorting rule could unambiguously be identified (Barceló, 2003; Nelson, 1976). Target displays remained on screen until a response was registered. After a fixed response-cue interval (RCI) of 1000 ms, a feedback cue was presented for 200 ms indicating whether the applied sorting rule should be maintained (“BLEIBEN” [“REPEAT”]) or changed (“WECHSELN” [“SWITCH”]) on the upcoming trial. Subsequent target stimuli appeared after a fixed cue-target interval (CTI) of 1000 ms. Note that switch cues provided implicit information about the currently valid task rule: their occurrence signaled that the previously adopted task rule had changed, thus rendering participants uncertain about which of the two remaining rules was the correct one (West, Langley, & Bailey, 2011). Ideally performing participants would choose one of the two remaining rules on the subsequent trial. Informative feedback cues that followed their initial guess enabled participants to induce the correct rule (see Fig. 1). In contrast, redundant repeat cues on subsequent trials did not reduce participants’ uncertainty about the valid task rules further. Rules changed in an unpredictable manner (Altmann, 2004) after runs of two or more repeat trials (average run length: 3.5 trials). Participants completed 40 task runs involving 39 switch trials. Prior to the experimental sequence, five practice runs were administered. Participants were informed about the three possible sorting criteria and about the fact that the valid task rule would change from time to time in an unpredictable manner. They were told to attend to the feedback cues in order to infer the correct task rule. 2.2. Electrophysiological recordings Continuous electroencephalogram was recorded from 30 active Ag-AgCl electrodes (BrainProducts, Gilching, Germany) placed according to the international 10–20 system. BrainVision Recorder software (Brain Products, Gilching, Germany) was used. Electrode impedance was kept below 10 k. Electrodes were referenced to FCz electrode. Vertical (vEOG) and horizontal (hEOG) electrooculogram were
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recorded with two additional electrodes positioned at the suborbital ridge and the external ocular canthus of the right eye. EEG and EOG channels were digitized at 250 Hz and amplified using a BrainAmp amplifier (Brain Products, Gilching, Germany). 2.3. Data analysis 2.3.1. Behavioral data As indicator for participants’ distractibility, response accuracy was determined separately for the three-stimulus oddball task and the task-switching paradigm. In the oddball task, error rates were composed of the number of false alarms (responses to standard and novel stimuli) and the number of misses (failures to respond to target stimuli). In the task-switching paradigm, we analyzed the proportion of errors on the second trial after the switch cue (i.e., after informative feedback cues allowed for rule induction). We refer to these measures of behavioral distractibility as oddball errors and task-switching errors, respectively. 2.3.2. Electrophysiological data Electrophysiological data were evaluated using BrainVision Analyzer 2.0 (Brain Products, Gilching, Germany). After filtering (high-pass: 0.5 Hz, low-pass: 70 Hz, notch: 50 Hz), data were screened for non-stereotyped artifacts and subjected to an ocular-correction independent component analysis (Groppe, Makeig, & Kutas, 2008) for further removal of ocular, muscular, and cardiac artifacts. Data were rereferenced to a common average reference offline, and segmented into epochs from −200 to 1000 ms relative to the onset of auditory stimuli (oddball task) and feedback stimuli (task-switching paradigm). After baseline-correction (−200 to 0 ms), residual artifacts were rejected semi-automatically before data were averaged. ERPs were locked to novel and standard stimuli in the oddball task, as well as to informative and redundant feedback cues in the task-switching procedure. Mean Novelty-P3 and Uncertainty-P3 amplitudes were measured at electrode FCz in a 120 ms interval around individual P3 peak latencies. Peak latencies corresponded to the largest positive deflection in individual ERP waveforms within the latency range between 240 and 380 ms (Novelty P3) or between 320 and 460 ms (Uncertainty P3). The difference between P3 amplitudes elicited by novel vs. standard stimuli served as measure of the Novelty P3. The difference between P3 amplitudes elicited by informative vs. redundant feedback cues served as measure of the Uncertainty P3. 2.3.3. Statistical analysis Statistical analyses were performed using SPSS 21.0 (IBM, Armonk, NY). The level of significance was set at ˛ = .05. Novelty effects in the oddball procedure were examined by means of a paired ttest comparing P3 amplitudes elicited by novel and standard stimuli at electrode FCz. Uncertainty effects in the oddball procedure were examined by means of a paired ttest comparing P3 amplitudes elicited by informative and redundant feedback cues at electrode FCz. Note that we deliberately chose to restrict our analyses to the informative repeat feedback cues (i.e., repeat cues following the initial guess) since these stimuli were physically identical to the redundant repeat cues (i.e., both events were characterized by the presentation of the German word for repeat, “BLEIBEN”). To examine commonalities between the electrophysiological and behavioral measures obtained from the two paradigms, Pearson correlation coefficients were calculated for the pairwise relationships between Novelty P3, Uncertainty P3, oddball errors and task-switching errors. To further illustrate the relationship between behavioral distractibility and P3 amplitudes, we divided our sample into two subgroups of high and low performers based on the number of task-switching errors. Data were then subjected to a subgroup (high performer vs. low performer) × waveform (Novelty P3 vs. Uncertainty P3) analysis of variance (ANOVA). For this subgroup analysis, we chose to focus on task-switching errors as this measure was more sensitive to individual differences than the number of oddball errors. Results did not differ qualitatively when the number of oddball errors or an aggregate error measure were used instead.
3. Results Both novel stimuli and informative feedback cues elicited prominent P3 amplitudes with comparable fronto-central topography (Fig. 2A, Table 1). Mean amplitudes at electrode FCz were higher for novel vs. standard stimuli (t = 4.89, p < .001) and for informative vs. redundant feedback cues (t = 4.55, p < .001). Note that amplitude differences were also statistically reliable at Fz and Cz, but not at Pz, both for the Novelty-P3 and the Uncertainty-P3 contrast (Table 1). We found a substantial negative correlation between individual P3 effects in the two paradigms (r = −.79, p < .001; Fig. 2B), implying that individuals who showed a large Novelty P3 produced only small Uncertainty-P3 amplitudes and vice versa. This relationship remained significant when the individuals showing minimum and maximum Novelty-P3 and Uncertainty-P3 amplitude were
Table 1 Waveform characteristics of Novelty P3 and Uncertainty P3.
Mean latency in ms (SD) Mean amplitude at Fz in V (SD) Mean amplitude at FCz in V (SD) Mean amplitude at Cz in V (SD) Mean amplitude at Pz in V (SD)
Novelty P3
Uncertainty P3
303.38 (32.39) 3.36 (2.48)* 3.49 (2.86)* 2.47 (1.65)* 0.49 (2.26)
413.25 (29.53) 2.53 (2.75)* 2.88 (2.53)* 2.04 (1.67)* 0.41 (2.36)
Note. Novelty P3 and Uncertainty P3 amplitude differences were calculated as the amplitude differences between novel and standard stimuli and between informative and redundant feedback cues, respectively. * Significantly different from zero at the 5% level.
Table 2 Associations between electrophysiological and behavioral measures.
Novelty P3 Uncertainty P3 Oddball errors Task switching errors * ** ***
Novelty P3
Uncertainty P3
Oddball errors
−.79*** .66*** .66***
−.54** −.49*
.38
p < .10. p < .05. p < .01.
removed from the sample (n = 13; r = −.68, p = .010) indicating that our finding is not driven by outliers. At the behavioral level, participants committed an average of 4.06 (SD = 4.84) errors in the oddball task and chose an incorrect sorting criterion on 21% (SD = 17%) of the analyzed trials in the task-switching procedure. Both error measures were positively related to the magnitude of the Novelty P3 while being negatively associated with UncertaintyP3 amplitude (Table 2). Based on error rates in the task-switching paradigm, we divided our sample into two subgroups of high (M = .09) and low (M = .32) performers. These subgroups differed with regard to how effectively participants induced the correct rule following informative feedback cues (t = 3.79, p = .002), while yielding similar age (t = 1.30, p = .21) and gender (one male each) distributions. Crucially, frontal P3 responses allowed for a double dissociation of these groups as indicated by a significant subgroup × P3 waveform interaction (F(1,14) = 4.76, p = .047, 2p = .25, Fig. 2C). High-performing individuals tend to show larger Uncertainty-P3 amplitudes (t = 2.02, p = .063) and smaller NoveltyP3 amplitudes (t = −2.03, p = .061) than low performers. 4. Discussion Novelty P3 (elicited by irrelevant distractors) and Uncertainty P3 (elicited by relevant feedback cues) closely resembled each other with regard to amplitude and scalp topography, possibly indicating that reactive and proactive forms of the OR converge on a common neural pathway (Sokolov, 1966; Kopp & Lange, 2013). However, amplitudes of the Novelty P3 and those of the Uncertainty P3 were strongly negatively correlated. These findings seem to contradict the traditional view that the OR constitutes a unitary process. They support the conception that novelty detection and uncertainty reduction represent functionally dissociable routes to the neural underpinnings of the OR, here labeled reactive and proactive OR, respectively. Further, response accuracy was associated with decreased Novelty-P3 amplitudes and with increased amplitudes of the Uncertainty P3. These findings point into the direction that the balance between Novelty P3 and Uncertainty P3 might represent a trait variable related to individuals’ distractibility. Specifically, this electrophysiological indicator may reflect the neural substrates of individual capabilities to focus on task-relevant information and to attenuate distractor interference (Desimone & Duncan, 1995;
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Fig. 2. ERP results from the task-switching paradigm and the auditory novelty oddball task. (A) Grand average waveforms locked to novel and standard stimuli in the oddball task (left) and to informative and redundant feedback (FB) cues in the task-switching procedure (right). Both novel stimuli and informative FB cues elicited prominent anterior P3 waveforms. Scalp maps indicate topographies of the Novelty P3 (novel–standard) and the Uncertainty P3 (informative FB–redundant FB), measured in a 120 ms interval around mean peak latencies (Novelty P3: 303 ms, Uncertainty P3: 413 ms). The color scale for scalp maps ranges from -3 V to 3 V. (B) Amplitudes of the Novelty P3 (novel–standard) and the Uncertainty P3 (informative FB–redundant FB) are negatively related to each other (p < .001). (C) Scalp topographies of the Novelty P3 (novel–standard) and the Uncertainty P3 (informative FB–redundant FB), separated for subgroups of high-performing and low-performing individuals. Subgroups were defined according to the number of errors committed after the first, informative FB cue in the task-switching paradigm (median split). Low-performing individuals (who were less likely to infer the correct task rule after an informative FB cue) generated larger Novelty-P3 amplitudes, but smaller Uncertainty-P3 amplitudes.
Forster & Lavie, 2014; McNab & Dolan, 2014). Our findings are consistent with the notion of two distinct neuroanatomical networks underlying task-relevant and task-irrelevant attention (Corbetta & Shulman, 2002). Most important to the current findings, activity of these networks has been found to be negatively correlated, thus indicating a competitive interaction of the brain’s attentional systems (Fox et al., 2005). Our data illustrate a comparable antagonistic relationship on the level of electrophysiological scalp potentials. Small Novelty-P3 and large Uncertainty-P3 amplitudes appear to be indicative of a rather controlled mode of attentional orienting, while large Novelty-P3 and small Uncertainty-P3 reflect a relative dominance of automatic determinants of attentional focus. Our results can also be reconciled with those models of the OR which highlight the role of stimulus significance in determining ORs (Bernstein, 1979; Bradley, 2009; Maltzman, 1979). According to
these models, ORs are not produced as a consequence of mismatch alone. Instead, Bernstein (1979) proposed that the threshold for the elicitation of ORs is exceeded only if stimuli possess sufficient significance in the present context. To illustrate how significance models account for our results, consider two individuals with relatively high and relatively low threshold levels for the elicitation of the OR, respectively. The high-threshold individual will show weak ORs in comparison to the low-threshold individual when encountering task-irrelevant novel stimuli in oddball tasks since their significance does not exceed the threshold which is required for the elicitation of ORs. Novel oddball stimuli thus elicit small amplitudes of the Novelty P3 in these individuals. High-threshold individuals will, however, orient selectively to informative feedback cues in the task-switching paradigm because informative feedback cues provide significant information for successful task performance.
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These informative feedback cues thus elicit ORs, reflected in large amplitudes of the Uncertainty P3. In contrast, task-irrelevant novel stimuli are more likely to elicit ORs in low-threshold individuals. This results in increased amplitudes of the Novelty P3 and reduced amplitudes of the Uncertainty P3 (due to less differential responding to informative and redundant feedback cues). As a consequence, assuming that stimulus significance contributes substantially to ORs and that individuals vary with regard to OR thresholds might account for the negative correlation of Novelty P3 and Uncertainty P3 that we found in our study. While task-relevant and task-irrelevant stimuli elicited P3 waveforms of comparable amplitude and scalp topography, it has to be noticed that Novelty P3 and Uncertainty P3 differ in latency, with Novelty P3 peaking about 100 ms earlier than Uncertainty P3. This latency difference might be interpreted as challenging our view of a common electrophysiological correlate of reactive and proactive OR. Note, however, that Uncertainty P3 was locked to visual stimuli while Novelty P3 was locked to auditory stimuli. Hence, the observed latency difference might simply be due to auditory information being processed more rapidly than visual information (Romero & Polich, 1996; Woodworth & Schlosberg, 1954). Future studies on the relationship between Novelty P3 and Uncertainty P3 should measure both waveforms within the same modality to control for these processing differences. In sum, our study demonstrates that phenomenologically similar frontal P3 waveforms can be associated with both, proactive attentional orienting to task-relevant stimuli and reactive attentional orienting to task-irrelevant stimuli. Individuals differ with regard to the relative dominance of these two attentional responses and this variation relates to individual differences in behavioral distractibility. The present study constitutes a first step toward an electrophysiological characterization of the competitive interaction between task-relevant and task-irrelevant attention. Further research into the balance between Novelty P3 and Uncertainty P3 might help to shed light on this complex interaction and the functional role of proactive and reactive OR. Acknowledgements F.L. received funding from the German National Academic Foundation. In addition, the research reported here was supported by a grant from the Petermax-Müller-Stiftung, Hannover, Germany. The authors thank Moritz Boos and Andreas Niesel for technical support. References Altmann, E. M. (2004). Advance preparation in task switching: What work is being done? Psychological Science, 15(9), 616–622. http://dx.doi.org/10. 1111/j. 0956-7976.2004.00729.x Anderson, N. E., Baldridge, R. M., & Stanford, M. S. (2011). P3a amplitude predicts successful treatment program completion in substance-dependent individuals. Substance Use & Misuse, 46(5), 669–677. http://dx.doi.org/ 10.3109/10826084.2010.528123 Barceló, F. (2003). The Madrid card sorting test (MCST): A task switching paradigm to study executive attention with event-related potentials. Brain Research Protocols, 11(1), 27–37. http://dx.doi.org/10.1016/S1385-299X(03)00013-8 ˜ Barceló, F., Escera, C., Corral, M. J., & Periánez, J. A. (2006). Task switching and novelty processing activate a common neural network for cognitive control. Journal of Cognitive Neuroscience, 18(10), 1734–1748. http://dx.doi.org/ 10.1162/jocn.2006.18.10.1734 ˜ Barceló, F., Periánez, J. A., & Knight, R. T. (2002). Think differently: A brain orienting response to task novelty. NeuroReport, 13(15), 1887–1892. Barry, R. J. (1979). A factor-analytic examination of the unitary OR concept. Biological Psychology, 8(3), 161–178. http://dx.doi.org/10.1016/0301-0511(79)90045-0 Barry, R. J., MacDonald, B., & Rushby, J. A. (2011). Single-trial event-related potentials and the orienting reflex to monaural tones. International Journal of Psychophysiology, 79(2), 127–136. http://dx.doi.org/10.1016/j.ijpsycho.2010.09.010 Berg, E. A. (1948). A simple objective technique for measuring flexibility in thinking. The Journal of General Psychology, 39(1), 15–22. http://dx.doi.org/10. 1080/00221309.1948.9918159
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