Moseley, Peter

Smailes, David

Wilkinson, Sam

English

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GENERAL COMMENTARYpublished: 17 March 2015doi: 10.3389/fnhum.2015.00142Frontiers in Human Neuroscience | www.frontiersin.org 1 March 2015 | Volume 9 | Article 142Edited by:Lorenzo Pia,University of Turin, ItalyReviewed by:Andreas Kalckert,Karolinska Institutet, Sweden*Correspondence:David Smailes,david.smailes@durham.ac.uk†Present Address:Peter Moseley,School of Psychology, University ofCentral Lancashire, Preston, UKReceived: 17 January 2015Paper pending published:26 January 2015Accepted: 01 March 2015Published: 17 March 2015Citation:Smailes D, Moseley P and Wilkinson S(2015) A commentary on: Affectivecoding: the emotional dimension ofagency. Front. Hum. Neurosci. 9:142.doi: 10.3389/fnhum.2015.00142A commentary on: Affective coding:the emotional dimension of agencyDavid Smailes 1*, Peter Moseley 1 † and Sam Wilkinson 21Department of Psychology, Durham University, Durham, UK, 2Department of Philosophy, Durham University, Durham, UKKeywords: affect, emotion, agency, hallucinations, voice hearing, psychosisA commentary onAffective coding: the emotional dimension of agencyby Gentsch, A., and Synofzik, M. (2014). Front. Hum. Neurosci. 8:608. doi: 10.3389/fnhum.2014.00608We welcome Gentsch and Synofzik’s (2014) review of the role of affect in modulating a person’ssense of agency (SoA). The review is timely and synthesizes a great deal of evidence. However, wefeel that their claims concerning the role of affect in modulating a person’s SoA could be usefullyextended to the study of auditory hallucinations (AH), one unusual experience not discussed intheir review. In this commentary, we describe recent findings that suggest that one way in whichnegative affect plays a role in the development of AH is by reducing the SoA associated with self-generated cognitions and suggest that the insula may play an important role in mediating the effectof affect on SoA.Cognitive models of AH (e.g., Bentall, 1990; Waters et al., 2012) suggest that they occur when acognition is misattributed to an external, non-self-source. Consistent with this claim, people whoexperience AH tend to show a bias toward accepting the presence of a verbal stimulus on tasksdesigned to measure reality discrimination (i.e., they tend to confuse internal, self-generated eventsfor external, non-self-generated events, but not vice versa; Brookwell et al., 2013). This is oftendemonstrated using an auditory signal detection task (SDT), in which participants must try todetect speech in an ambiguous auditory stimulus (typically white noise). On trials where the speechis absent, participants have the opportunity to make a false alarm; that is, to report that speechwas present in the white noise, when it was not. Presumably, when participants make a false alarm,they have mistaken their internal representation of the speech for the externally presented, “real”speech.Two recent studies have demonstrated a causal relation between increases in negative affectand weaker reality discrimination. Smailes et al. (2014) reported that participants who per-formed an auditory SDT after completing a negative mood induction (recalling an unpleasantautobiographical memory) made more false alarms, but not more hits, than did participantswho performed the task after completing a neutral mood induction. Similarly, Hoskin et al.(2014), despite employing a different mood induction and a modified SDT, reported that par-ticipants were more likely to make false alarms during a condition in which they were exposedto a stressor than during a control condition. Thus, both studies showed that when partici-pants experienced negative affect, they were more likely to misattribute internal, self-generatedcognitions to an external source. These findings are consistent with data from studies thathave shown that negative affect tends to precede the onset of AH in the daily lives of psy-chosis patients (Nayani and David, 1996; Delespaul et al., 2002), and suggest that negative affectis associated with the onset of AH, at least in part, because it modulates SoA for cognition.Smailes et al. Affect, agency, and auditory hallucinationsGentsch and Synofzik propose that three stages of agencyprocessing—prospective, immediate, and retrospective—exist.First person accounts (e.g., Romme et al., 2009; Scholtus andBlanke, 2012) suggest that people who experience AH do not gothrough a deliberative process to determine whether an unusualauditory percept was self-generated, or was a result of an external,non-self agent. Instead, an AH is experienced “in the moment” assomething that was not self-generated. Thus, in terms of Gentschand Synofzik’s proposed stages, it seems likely that the effect ofnegative emotions on a person’s reality discrimination abilitieswould correspond to either prospective or immediate affectivecoding, rather than retrospective affective coding. That is, neg-ative affect may reduce a person’s SoA over cognition by inter-fering with action planning or with the generation of an accuratesensory outcome representation of a cognition. The most promi-nent cognitivemodels of AH suggest that a forwardmodel systemacts to predict the sensory outcomes of motor commands, andthat dysfunction at one of a number of comparators can lead toa lack of agency over self-generated actions (Jones and Ferny-hough, 2007). Interference with either action planning or accu-rate prediction could therefore lead to external misattributions ofself-generated processes. A potential avenue for research wouldbe to investigate whether negative affect can modulate, for exam-ple, the sensory attenuation which is associated with successfulprediction via forward modeling.Gentsch and Synofzik’s review only briefly discusses thebrain regions that may be involved in mediating the effects ofnegative affect on SoA. At two points, however, they cite evi-dence suggesting that damage to/atypical activity in the insulacan lead to disorders of SoA. We concur that the insula is agood candidate for mediating the effects of negative affect onSoA. This is because, in addition to the evidence cited by Gentschand Synofzik, a number of studies have shown (a) that differentagency experiences are associated with changes in insula activity(e.g., Farrer and Frith, 2002; Farrer et al., 2003), (b) that insulaactivity is atypical in people who report AH (Wylie and Tregel-las, 2010) and (c) that increases in negative affect are associatedwith changes in insula activity (Phan et al., 2002; Harrison et al.,2008). Research that examines whether negative affect bringsabout reductions in a person’s SoA over their cognitions throughmodulation of activity in the insula is required.Demonstrating that affective problems may play an impor-tant role in the development of AH is important for a numberof reasons. First, affect-induced changes in the SoA a personhas over their cognitions can help to explain why AH are typi-cally not experienced constantly (this issue is sometimes raisedas a problem for cognitive models of AH; Gallagher, 2004).Seconds, and perhaps more importantly, it opens up the pos-sibility of novel therapeutic interventions. While the primaryfocus of such interventions may be on ameliorating the affec-tive problems reported by people who hear voices, they mayindirectly reduce the frequency of AH by preventing nega-tive affect-induced modulations of a person’s SoA over theircognitions.ReferencesBentall, R. P. (1990). The illusion of reality: a review and integration of psycho-logical research on hallucinations. Psychol. Bull. 107, 82–95. doi: 10.1037/0033-2909.107.1.82Brookwell, M. L., Bentall, R. P., and Varese, F. (2013). Externalizing biasesand hallucinations in source-monitoring, self-monitoring and signal detec-tion studies: a meta-analytic review. Psychol. Med. 43, 2465–2475. doi:10.1017/S0033291712002760Delespaul, P., de Vries, M., and van Os, J. (2002). Determinants of occurrence andrecovery from hallucinations in daily life. Soc. Psychiatry Psychiatr. Epidemiol.37, 97–104. doi: 10.1007/s001270200000Farrer, C., Franck, N., Georgieff, N., Frith, C. D., Decety, J., and Jeannerod, M.(2003). Modulating the experiences of agency: a positron emission tomographystudy. Neuroimage 18, 324–333. doi: 10.1016/S1053-8119(02)00041-1Farrer, C., and Frith, C. D. (2002). Experiencing oneself vs another person asbeing the cause of an action: the neural correlates of the experience of agency.Neuroimage 15, 596–603. doi: 10.1006/nimg.2001.1009Gallagher, S. (2004). Neurocognitivemodels of schizophrenia: a neurophenomeno-logical critique. Psychopathology 37, 8–19. doi: 10.1159/000077014Gentsch, A., and Synofzik, M. (2014). Affective coding: the emotional dimensionof agency. Front. Hum. Neurosci. 8:608. doi: 10.3389/fnhum.2014.00608Harrison, B. J., Pujol, J., Ortiz, H., Fornito, A., Pantelis, C., and Yücel, M. (2008).Modulation of brain resting-state networks by sad mood induction. PLOS ONE3:e1794. doi: 10.1371/journal.pone.0001794Hoskin, R., Hunter, M. D., andWoodruff, P. W. R. (2014). The effect of psycholog-ical stress and expectation on auditory perception: a signal detection analysis.Br. J. Psychol. 105, 524–546. doi: 10.1111/bjop.12048Jones, S. R., and Fernyhough, C. (2007). Neural correlates of inner speech and audi-tory verbal hallucinations: a critical review and theoretical integration. Clin.Psychol. Rev. 27, 140–154. doi: 10.1016/j.cpr.2006.10.001Nayani, T. H., and David, A. S. (1996). The auditory hallucination: a phe-nomenological survey. Psychol. Med. 26, 177–189. doi: 10.1017/S003329170003381XPhan, K. L., Wager, T., Taylor, S. F., and Liberzon, I. (2002). Functional neu-roanatomy of emotion: a meta-anlysis of emotion activation studies in PET andfMRI. Neuroimage 16, 331–348. doi: 10.1006/nimg.2002.1087Romme, M., Escher, S., Dillon, J., Corstens, D., and Morris, M. (2009). Living withVoices: Fifty Stories of Recovery. Ross-on-Wye: PCCS.Scholtus, S., and Blanke, C. (2012). “Auditory verbal hallucinations, first-personaccounts,” in Hallucinations: Theory and Practice, eds J. D. Blom and I. E. C.Sommer (New York, NY: Springer), 105–108.Smailes, D., Meins, E., and Fernyhough, C. (2014). The impact of negativeaffect on reality discrimination. J. Behav. Ther. Exp. Psy. 45, 389–395. doi:10.1016/j.jbtep.2014.04.001Waters, F., Allen, P., Aleman, A., Fernyhough, C., Woodward, T. S., Badcock, J.C., et al. (2012). Auditory hallucinations in schizophrenia and nonschizophre-nia populations: a review and integrated model of cognitive mechanisms.Schizophr. Bull. 38, 683–692. doi: 10.1093/schbul/sbs045Wylie, K. P., and Tregellas, J. R. (2010). The role of the insula in schizophrenia.Schizophr. Res. 123, 93–104. doi: 10.1016/j.schres.2010.08.027Conflict of Interest Statement: The authors declare that the research was con-ducted in the absence of any commercial or financial relationships that could beconstrued as a potential conflict of interest.Copyright © 2015 Smailes, Moseley and Wilkinson. This is an open-access articledistributed under the terms of the Creative Commons Attribution License (CC BY).The use, distribution or reproduction in other forums is permitted, provided theoriginal author(s) or licensor are credited and that the original publication in thisjournal is cited, in accordance with accepted academic practice. No use, distributionor reproduction is permitted which does not comply with these terms.Frontiers in Human Neuroscience | www.frontiersin.org 2 March 2015 | Volume 9 | Article 142

A commentary on: Affective coding: the emotional dimension of agency

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