Stop Saying That It Is Wrong! Psychophysiological, Cognitive, and Metacognitive Markers of Children’s Sensitivity to Punishment

RESEARCH ARTICLE Stop Saying That It Is Wrong! Psychophysiological, Cognitive, and Metacognitive Markers of Children’s Sensitivity to Punishment Maria Luz Gonzalez-Gadea1,2,3, Anouk Scheres4, Carlos Andres Tobon5,6, Juliane Damm7, Sandra Baez1,2,3, David Huepe3,8, Julian Marino9, Sandra Marder10, Facundo Manes1,2,3,11, Sofia Abrevaya1, Agustin Ibanez1,2,3,11,12* OPEN ACCESS Citation: Gonzalez-Gadea ML, Scheres A, Tobon CA, Damm J, Baez S, Huepe D, et al. (2015) Stop Saying That It Is Wrong! Psychophysiological, Cognitive, and Metacognitive Markers of Children’s Sensitivity to Punishment. PLoS ONE 10(7): e0133683. doi:10.1371/journal.pone.0133683 1 Institute of Cognitive Neurology (INECO), Buenos Aires, Argentina, 2 National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina, 3 UDP-INECO Foundation Core on Neuroscience (UIFCoN), Faculty of Psychology, Diego Portales University, Santiago, Chile, 4 Behavioural Science Institute, Developmental Psychology, Radboud University, Nijmegen, The Netherlands, 5 Grupo de Neurociencias de Antioquia, Facultad de Medicina, Universidad de Antioquia, Medellin, Colombia, 6 Grupo de Neuropsicología y Conducta, Facultad de Medicina, Universidad de Antioquia, Medellin, Colombia, 7 University of Leipzig, Leipzig, Germany, 8 Laboratory of Cognitive and Social Neurosciences, Universidad Diego Portales, Santiago, Chile, 9 Laboratorio de Neuroimágenes, Universidad Nacional de Córdoba, Cordoba, Argentina, 10 Comisión de Investigaciones Científicas de la Provincia de Buenos Aires y Facultad de Psicología (UNLP), La Plata, Argentina, 11 Centre of Excellence in Cognition and its Disorders, Australian Research Council (ACR), Randwick, New South Wales, Australia, 12 Universidad Autónoma del Caribe, Barranquilla, Colombia * Editor: Alessio Avenanti, University of Bologna, ITALY Abstract Received: May 8, 2015 Neurodevelopmental evidence suggests that children’s main decision-making strategy is to avoid options likely to induce punishment. However, the cognitive and affective factors contributing to children’s avoidance to high punishment frequency remain unknown. The present study explored psychophysiological, cognitive, and metacognitive processes associated with sensitivity to punishment frequency. We evaluated 54 participants (between 8 and 15 years old) with a modified Iowa Gambling Task for children (IGT-C) which included options with varying long-term profit and punishment frequencies. Skin conductance responses (SCRs) were recorded during this task. Additionally, we assessed IGT-C metacognitive knowledge, fluid intelligence, and executive functions. Participants exhibited behavioral avoidance and high anticipatory SCRs to options with high frequency of punishment. Moreover, age, IGT-C metacognitive knowledge, and inhibitory control were associated with individual differences in sensitivity to punishment frequency. Our results suggest that children’s preference for infrequently punished decisions is partially explained by psychophysiological signals as well as task complexity and development of cognitive control. Accepted: June 30, 2015 Published: July 28, 2015 Copyright: © 2015 Gonzalez-Gadea et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This research was partially supported by grants from National Council of Scientific and Technological Research (CONICET), National Committee of Scientific and Technological Research (CONICYT) and National Fund for Scientific and Technological Development (FONDECYT) - Regular 1130920, CONICYT and FONDECYT - Regular 1140114, Fund for Scientific and Technological Research (FONCyT) for Scientific and Technological Projects (PICT) 2012-0412, FONCyT-PICT 2012- PLOS ONE | DOI:10.1371/journal.pone.0133683 July 28, 2015 1 / 17 Children’s Sensitivity to Punishment Frequency 1309, FONCyT-PICT 2012-0412, and Foundation of the Institute of Cognitive Neurology (INECO). Competing Interests: The authors have declared that no competing interests exist. Introduction Ferb, an eleven-year-old boy, is completing an e-tutorial in preparation for a math exam. He is frustrated by the visual and auditory cues indicating errors in the tutorial. Also, he is eager to finish the exercises quickly and play his favorite videogame. However, Ferb knows that if he obtains a passing mark in the exam, he will have two months of vacations. Decision-making requires making trade-offs such as suppressing the need for immediate reward and tolerating punishments or errors in the short term, in order to achieve long-term goals. Neurodevelopmental studies suggest that children’s main decision-making strategy is to avoid options with a high frequency of punishment [1–6]. However, the psychophysiological and cognitive processes contributing to sensitivity to punishment frequency remain unknown. Decision-making has been evaluated with the Iowa Gambling Task (IGT) [7] and similar tests adapted for children [4,8]. In these tasks, participants have to win game money by selecting cards from four decks, which differ in the magnitude and frequency of gain and loss. There are two decks considered advantageous in the long run and also two disadvantageous decks. Both options also contained one deck with high punishment frequency and other with low probability of punishment. Most studies found that children do not make advantageous decisions in the IGT until late adolescence [8–12]. However, other reports have noted that children did not behave randomly and selected decks with infrequent punishment, despite the options’ long-term profit [2–4,6,13,14]. It is important to note that previous versions of the IGT feature important caveats for children assessment. This complex task involves several processing dimensions (amounts, frequencies, wins, losses). In addition, it demands mental calculations of costs and profits, which proved challenging for young children (e.g., operations with negative numbers). Besides, implicit emotional processing during IGT performance has been extensively reported in adults through psychophysiological markers, such as skin conductance response (SCR) [15,16–18]. These studies have shown that participants exhibit SCR changes in response to the outcome of their choices (win versus loss). Remarkably, healthy adults show an anticipatory SCR before selecting a disadvantageous option. These signals have been interpreted as an index of emotional arousal and implicit processes underlying advantageous decision making. However, evidence of psychophysiological processes associated with IGT performance in children is scarce. Crone and van der Molen [2] reported that anticipatory SCR to disadvantageous option (...truncated)