Emotional Arousal to Novel Sounds Is Reflected in The
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bioRxiv preprint doi: https://doi.org/10.1101/250084; this version posted January 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 2 3 Emotion lies in the eye of the listener: emotional arousal to novel sounds is reflected in the 4 sympathetic contribution to the pupil dilation response and the P3 5 6 Andreas Widmann1, Erich Schröger1, & Nicole Wetzel1,2,3 7 8 1Cognitive and Biological Psychology, Institute of Psychology, University of Leipzig, 9 Germany 10 2CBBS Research Group Neurocognitive Development, Leibniz Institute for Neurobiology, 11 Magdeburg, Germany 12 3Center for Behavioral Brain Sciences Magdeburg, Germany 13 14 15 16 17 Corresponding author: 18 Andreas Widmann 19 Institute of Psychology 20 University of Leipzig 21 Neumarkt 9−19 22 D-04109 Leipzig Germany 23 E-mail: [email protected] 24 25 26 27 28 Keywords: Pupillometry, emotional arousal, novelty, P3a, pupil dilation, autonomic nervous 29 system 1 bioRxiv preprint doi: https://doi.org/10.1101/250084; this version posted January 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 30 Abstract 31 Novel sounds in the auditory oddball paradigm elicit a biphasic dilation of the pupil (PDR) 32 and P3a as well as novelty P3 event-related potentials (ERPs). The biphasic PDR has been 33 hypothesized to reflect the relaxation of the iris sphincter muscle due to parasympathetic 34 inhibition and the constriction of the iris dilator muscle due to sympathetic activation. We 35 measured the PDR and the P3 to neutral and to emotionally arousing negative novels in dark 36 and moderate lighting conditions. By means of principal component analysis (PCA) of the 37 PDR data we extracted two components: the early one was absent in darkness and, thus, 38 presumably reflects parasympathetic inhibition, whereas the late component occurred in 39 darkness and light and presumably reflects sympathetic activation. Importantly, only this 40 sympathetic late component was enhanced for emotionally arousing (as compared to neutral) 41 sounds supporting the hypothesis that emotional arousal specifically activates the sympathetic 42 nervous system. In the ERPs we observed P3a and novelty P3 in response to novel sounds. 43 Both components were enhanced for emotionally arousing (as compared to neutral) novels. 44 Our results demonstrate that sympathetic and parasympathetic contributions to the PDR can 45 be separated and link emotional arousal to sympathetic nervous system activation. 46 47 Highlights 48 • PDR and ERP effects of novel emotional and neutral oddball sounds were studied. 49 • Parasympathetic and sympathetic contributions to the PDR were dissociated by PCA. 50 • The parasympathetic PDR component was absent in darkness. 51 • Emotional arousal enhanced the sympathetic contribution to the PDR and the P3 ERP. 52 • Effects of emotional arousal are mediated by the sympathetic pathway. 53 2 bioRxiv preprint doi: https://doi.org/10.1101/250084; this version posted January 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 54 Introduction 55 The pupil diameter is controlled by both autonomic nervous systems via two muscles. The 56 ring-shaped iris sphincter muscle is innervated by the parasympathetic nervous system while 57 the radial iris dilator muscle is innervated by the sympathetic nervous system (Einhäuser, 58 2017; McDougal & Gamlin, 2008). Both nervous systems closely couple the pupil to the 59 locus coeruleus-norepinephrine (LC-NE) system (via an inhibitory projection to the Edinger- 60 Westphal nucleus in case of the parasympathetic system). The LC-NE system is a 61 neuromodulatory system that is central for various functions, in particular attention, emotion, 62 motivation, decision making, and memory (Aston-Jones & Cohen, 2005; Murphy, O'Connell, 63 O'Sullivan, Robertson, & Balsters, 2014; Murphy, Robertson, Balsters, & O'Connell, 2011; 64 Preuschoff, ’t Hart, & Einhäuser, 2011; for review see, Laeng, Sirois, & Gredebäck, 2012; 65 Einhäuser, 2017). The LC-NE system shows a phasic activation in response to task-relevant, 66 salient, or arousing stimuli (for review see e.g.,Sara & Bouret, 2012). Rare or novel events 67 presented within a sequence of frequently repeated standard events (the oddball paradigm) do 68 elicit a pupil dilation response (PDR; Friedman, Hakerem, Sutton, & Fleiss, 1973; Hochmann 69 & Papeo, 2014; Liao, Kidani, Yoneya, Kashino, & Furukawa, 2016; Liao, Yoneya, Kidani, 70 Kashino, & Furukawa, 2016; Murphy et al., 2014; Murphy et al., 2011; Qiyuan, Richer, 71 Wagoner, & Beatty, 1985; Steinhauer & Hakerem, 1992; Wetzel, Buttelmann, Schieler, & 72 Widmann, 2016). 73 74 Independently from sounds' novelty, the PDR has also been shown to be highly sensitive to 75 emotional arousal. For example, Partala and Surakka (2003) reported enhanced PDRs in 76 response to sounds with positive or negative valence compared to neutral sounds. Also in the 77 visual modality, Bradley, Miccoli, Escrig, and Lang (2008) observed larger pupil dilation 78 responses for pleasant and unpleasant emotionally arousing pictures compared to emotionally 79 neutral pictures. In their study Bradley and colleagues observed a co-variation of the PDR and 80 skin conductance changes but no co-variation of PDR and cardiac deceleration. Based on this 81 indirect evidence Bradley and colleagues (2008) suggested that the emotion-related PDR 82 effects are supposed to be specific for sympathetic nervous system activity. However, this has 83 not yet been directly shown on the basis of the PDR itself. Both nervous systems 84 antagonistically contribute to the observed pupil dilation: relaxation of the iris sphincter 85 muscle by parasympathetic inhibition and constriction of the iris dilator muscle by 86 sympathetic activation. Attempts to non-invasively dissociate their contributions have not yet 87 been successful (Einhäuser, 2017). The possibility to separate the differential contributions of 3 bioRxiv preprint doi: https://doi.org/10.1101/250084; this version posted January 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 88 the parasympathetic and sympathetic nervous systems to the PDR is therefore of high 89 relevance. 90 91 Frequently, the observed pupil dilation in response to rare events is biphasic and it has been 92 suggested that the two peaks reflect the overlapping contributions of the sphincter muscle 93 relaxation by parasympathetic inhibition and of the dilator muscle constriction by sympathetic 94 activation (Steinhauer & Hakerem, 1992). Steinhauer and Hakerem (1992) hypothesized that 95 overlapping sympathetic and parasympathetic contributions should be separable by means of 96 factor analysis. A biphasic response to several environmental distractor sounds was also 97 observed in infants and adults (Wetzel et al., 2016). Two main components were extracted 98 using a principal component analysis (PCA), however, the attribution of components to 99 changes in parasympathetic and sympathetic activity remained unclear. A PCA was also 100 applied to pupillary data by Geuter, Gamer, Onat, and Büchel (2014). The components were, 101 however, not related to pupil physiology but used to predict pain ratings by a regression based 102 approach. Together with their original hypothesis Steinhauer and Hakerem (1992) already 103 suggested a possible validation of this attribution by variation of lighting conditions: the 104 parasympathetic tone, but not sympathetic tone, is minimal in darkness (Loewenfeld, 1958; 105 and the sphincter muscle maximally relaxed). Thus, in darkness, a component related to 106 parasympathetic inhibition should be reduced in comparison to bright lighting conditions, 107 while a component related to sympathetic activation is not supposed to be modulated by 108 lighting conditions. The contributions of the parasympathetic and the sympathetic pathway to 109 pupil dilation during sustained processing have already been successfully separated by the 110 variation of ambient lighting as well as by pharmacological manipulations (Steinhauer, 111 Siegle, Condray, & Pless, 2004). However, for the phasic PDR observed in response to rare 112 (sound) events the separation of the contributions of parasympathetic inhibition and 113 sympathetic activation by means of factor analysis or PCA including a validation by lighting 114 conditions has−to our knowledge−not yet been empirically tested. 115 116 Also the P3-family of event-related potential (ERP) responses associated with processes of 117 attention and memory (for review see, e.g., Alho, Escera, & Schröger, 2003; Polich, 2007) 118 has been suggested to be related to LC-NE system activity. More specifically, a current theory 119 postulates that P3 and the autonomic component of the orienting response do reflect the co- 120 activation of the locus coeruleus-norepinephrine (LC-NE) system and the peripheral 121 sympathetic nervous system (SNS; Nieuwenhuis, De Geus, & Aston-Jones, 2011). The P3a 4 bioRxiv preprint doi: https://doi.org/10.1101/250084; this version posted January 18, 2018. 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