MINI REVIEW published: 16 July 2019 doi: 10.3389/fpsyg.2019.01634 Implicit Affect and Autonomous Nervous System Reactions: A Review of Research Using the Implicit Positive and Negative Affect Test Anna-Sophie Weil 1 , Gina Patricia Hernández 2,3 , Thomas Suslow 1* † and Markus Quirin 3,4† 1 Department of Psychosomatic Medicine and Psychotherapy, Leipzig University, Leipzig, Germany, 2 Stress and Health Research Group, Department of Basic Psychology, Universitat Autònoma de Barcelona, Barcelona, Spain, 3 School of Management, Technical University of Munich, Munich, Germany, 4 PFH Göttingen, Göttingen, Germany In everyday life, affective processes occur spontaneously and typically go along with an automatic activation of action tendencies and physiological responses. Because self- reports of affect are also known to be biased by various factors, including deficits in introspection or impression management strategies, an indirect measure, the Implicit Positive and Negative Affect Test (IPANAT), was developed to assess implicit affect and to circumvent these difficulties. In this review, findings from neurobiological and clinical Edited by: Maurizio Codispoti, studies administering the IPANAT are revised, we focus on the link between implicit affect University of Bologna, Italy and psychophysiological reactions to affective stimuli and stressors. Specifically, implicit Reviewed by: affect as measured by the IPANAT was found to predict cardiovascular, endocrine, and Andrea De Cesarei, University of Bologna, Italy functional neuroimaging correlates of stress or fear beyond explicit affect. The present Carmelo Mario Vicario, evidence strongly suggests the usage of implicit affect measures in future research on University of Messina, Italy stress and psychopathology. *Correspondence: Thomas Suslow Keywords: implicit affect, dual-processing model, implicit positive and negative affect test, autonomous nervous suslow@medizin.uni-leipzig.de system reactions, cardiovascular responses † These authors have contributed equally to this work as senior authors INTRODUCTION Specialty section: This article was submitted to Affects refer to basic, evolutionary conserved processes (Penner and Stoddard, 2018) as one of their Emotion Science, many purposes is to provide information about our situation, including information about whether a section of the journal our goals may be thwarted or attained (Montag and Panksepp, 2017). There is agreement that affects Frontiers in Psychology comprise different components such as situation appraisal, subjective feelings, expressive behavior, Received: 11 March 2019 physiological responses, and action preparation (Scherer and Moors, 2019). Accepted: 28 June 2019 Although the details of affective experience are thought to be molded by individual Published: 16 July 2019 familiarity with the encountered situation and socialization, the basic affective reactions Citation: are most likely evolutionary shaped processes (Damasio, 2002; Mason and Capitanio, Weil A-S, Hernández GP, 2012). As parts of affect, cognition, physiology, as well as individual and situational Suslow T and Quirin M (2019) Implicit differences play an important role in the affective experience. Furthermore, cultural influences Affect and Autonomous Nervous System Reactions: A Review of (Quigley and Feldman Barrett, 2014) coupled with language and verbal manifestations Research Using the Implicit Positive (Cacioppo et al., 2000) have to be considered when trying to understand affect. In and Negative Affect Test. Front. Psychol. 10:1634. Abbreviations: ANS, autonomous nervous system; INA, implicit negative affect; IPA, implicit positive affect; IPANAT, doi: 10.3389/fpsyg.2019.01634 implicit positive and negative affect test. Frontiers in Psychology | www.frontiersin.org 1 July 2019 | Volume 10 | Article 1634 Weil et al. Implicit Affect and Physiology general, we can divide affect into two broader groups of positive theories of affect are in line with a dual-processing view (e.g., and negative valence (i.e., dimensional approach), or we can Clore and Ortony, 2000). According to this view, information see it as a rather small number of basic and distinct affects can be processed with propositions and rules, which convey (i.e., categorical approach) (Panksepp and Watt, 2011; Tracy one or more appraisal values. Alternatively, information can be and Randles, 2011). Contemporary appraisal theories define processed in an associative way, activating learned associations affects as processes rather than states. The basic premise is that between representations of the stimuli and previously stored affects are adaptive responses that reflect appraisals of features appraisal outputs (Moors, 2013). of the environment that are important for the survival of the There is a debate about whether these two types of processes organism (Moors, 2013). Therefore, the study of the nature of are conscious or unconscious (Moors, 2010). As mentioned these processes (i.e., if they are conscious or unconscious) is above, Lieberman (2019) argues for the possibility that appraisal critical for emotion research. Another notion is that appraisal processes are automatic but also conscious. According to processes may be automatic and conscious at the same time this author’s view, there are at least two types of conscious (Lieberman, 2019), a conceptualization where conscious affective processes, reflective and pre-reflective, collectively they constitute experiences are considered to be composed by a pre-reflective the basis of our immediate conscious experience, but pre- (i.e., automatic) and a reflective (i.e., rational) process. In reflective processes share the computational features of automatic this line of inquiry, the IPANAT (Quirin et al., 2009a) has processes. Accordingly, affective experience would initially be been developed for the assessment of implicit affect, here a pre-reflective process with several simultaneous automatic conceptualized as the automatic and pre-reflective component of processes giving rise to not-yet-reflected upon experience. This the affective experience. automatic connection between perceptual and body response To shed more light on the physiological components of systems constitutes first manifestations of affect. emotions and how they may relate to the development of In line with an approach toward affect as information psychological and psychosomatic disease, previous research processing, implicit affect is conceptualized as the automatic investigated relationships between self-reports of affect activation of cognitive representations of affective experiences and ANS reactivity. However, the literature is inconsistent, (Quirin et al., 2009a). For the authors, implicit affect, albeit which can partly be attributed to the multifunctionality not processed on the level of reflective cognition, is nonetheless and complexity of ANS processes, but also to introspective considered to be based on cognitive representations of affective limitations concerning different emotional components (e.g., experiences processed in a pre-conceptual mode rather than Kreibig, 2010). Because of these introspective limitations, it a conceptual mode (Quirin et al., 2009a). That is, on the can be considered informative to investigate the link between basis of an associative processing system, the stimulation automatic (“implicit”) components of affect with ANS reactivity of one representation within the system is spreading in a and its potential consequences for health (Brosschot et al., way that a larger network of representations is activated 2014; van der Ploeg et al., 2016). This is particularly the case as (Gyurak et al., 2011). Within appraisal theories this associative automatic affective processes influence behavior over and above mechanism is viewed as an automatic activation of learned affect self-reports (Winkielman et al., 2005; Gainotti, 2012). The associations between stimulus representations and previously present article provides an overview of initial empirical evidence stored appraisal outputs (Moors, 2013). Where explicit affect on this link, with most of the reviewed studies capitalizing on (i.e., reflecting on our affective state) is not necessarily the IPANAT to assess implicit affect. We hope to stimulate congruent to pre-reflective states, and can even alter them enhanced usage of implicit measurement in future research on (Lieberman, 2019). physiological components of affect. The IPANAT relates to this pre-reflective dimension of affect, using affect priming of judgments as a method to assess implicit affect. Specifically, the test draws on the principle of IMPLICIT AFFECT AND ITS affect infusion, according to which affect exerts an impact on THEORETICAL BACKGROUND evaluative processes influencing the judgments of unrelated objects. It has been shown that judgments about ambiguous Behavioral research has for a long time been struggling with objects such as artificial words require a constructive cognitive measuring important constructs without tapping into problems process that capitalizes on a vast amount of currently accessible associated with explicit measurements. Explicit measures or self- information (Forgas, 1992). The more ambiguous a stimulus is reports, directly accessing the constructs in question, deal with and the less of a predefined meaning it has for an individual, problems like social desirability and lack of introspection. To the smaller is the amount of available knowledge directly avoid such problems, researchers developed implicit measures. related to the stimulus, leaving more space for affective states These new approaches used methods like priming, reaction to automatically influence judgments of the stimulus (Bower, time techniques or word-fragment completion tasks intending 1981). Thus, the goal of the test is to capture the pre- to assess and operationalize concepts like attitudes, self-concepts reflective affective process expressed in the participants’ biased and affect from another angle (Fazio and Olson, 2003). judgments via the principle of affect infusion. According to Often, dual-processing models have been used as a rationale the authors, the fact that participants are not asked to reflect for distinguishing implicit from explicit measurement, which can or to give information about their affective states adds to also be applied to the case of implicit affect. Most appraisal the meaning of implicitness for the test. This is even more Frontiers in Psychology | www.frontiersin.org 2 July 2019 | Volume 10 | Article 1634 Weil et al. Implicit Affect and Physiology so the case as the rates of participants’ suspicion that the 2012). Accordingly, implicit affect constitutes a construct of IPANAT might measure affect is lower than one percent strong relevance in psychophysiological and clinical research (Quirin et al., 2009a). as well as beyond. Accordingly, the IPANAT uses participants’ ratings of the degree to which six artificial words (SAFME, VIKES, TUNBA, TALEP, BELNI, and SUKOV) sound like six mood adjectives AUTONOMOUS NERVOUS SYSTEM (happy, cheerful, energetic, helpless, tense, and inhibited). Thus, the test is composed of 36-items, which are scored on a The ANS, as a major component of the human nervous system, 4-point Likert scale, ranging from doesn’t fit at all to fits is working involuntarily and without consciousness. According very well. From the responses, a summary over all negative to many evolutionary theories, affects organize the activity of judgments is calculated as an indicator for INA, and over the ANS (Levenson, 2014). As a “highly sophisticated system all positive words as an indicator for IPA. Evidence for of control“ (Brindle et al., 2014, p. 113), it regulates in balance internal consistency, test-retest reliability, stability, criterion, with the central nervous system vital bodily functions like construct and etiological validity of the IPANAT has been respiration, cardiovascular responses, digestion, metabolism, and shown (Quirin et al., 2009a,b; Brosschot et al., 2014; Quirin organ functions as important parts of homeostatic adjustments and Bode, 2014; Mossink et al., 2015; van der Ploeg et al., and various emergency situations (Folkow, 2000). It is partly 2016). Recently, proof for cross-cultural validity emerged located in the central and peripheral nervous system, while (Quirin et al., 2018). we distinguish between a sympathetic (performance-enhancing) We might question how the IPANAT is comparable to and a parasympathetic (relaxation-promoting) branch (Cacioppo other measures of implicit affective processes. For example, the et al., 2000; Critchley et al., 2000; Quigley and Feldman Barrett, Implicit Association Test (IAT; Greenwald et al., 2003) has been 2014). Its complexity and fine interactions are illustrated through developed to indirectly assess attitudes on the basis of delays the interplay of hormonal and neuronal pathways (Folkow, versus facilitations in response to key presses that have double 2000) as well as sympathetic and parasympathetic branches meanings. In the case of the IAT-Anxiety (Egloff and Schmukle, (Brindle et al., 2014). That is why we renounce from a detailed 2002) participants are instructed to make a series of category description of either its various functions or multifaceted ways judgments (referring to different pairs of the target categories of working and concentrate on giving an overview of the most “self ” vs. “other” and “anxiety” vs. “calmness”). Accordingly, the common ways to measure ANS indices and its significance IAT can measure implicit self-concepts (attitude toward oneself) for psychophysiology. of affect rather than affect immediately. A similar argument can As such, the ANS also influences cardiovascular responses, be made for differentiating the measurement of the IPANAT from is connected to the system of heart and blood vessels. Heart that of the Affect Misattribution Procedure (AMP; Payne et al., rate and blood pressure, which are typically applied to assess 2005), which measures attitudes (rather than affect immediately) the functioning of these systems, are multiply determined end via key response to Chinese ideographs following pictures of the points of bodily functions. It is not quite clear how exactly attitude target. heart rate and blood pressure are modulated but the ANS, In addition, the IPANAT differs from these two procedures sympathetic activation in particular, seems to play a central in that it does not treat positive and negative as two role. A metabolically driven increase in heart rate and blood poles of one dimension but as two different dimensions, pressure can be observed due to physiological demands, but which has been consistently replicated with factor analyses also as a response to psychological stress (Brindle et al., (Quirin et al., 2009a, 2018; Sulejmanov and Spasovski, 2018). 2014). Heart rate variability is commonly used to investigate This is in line with two-dimensional models of affect (e.g., autonomic vascular control. While a decrease of heart rate Watson et al., 1988) and enables to investigate differential variability power is thought to signal a sympathetic activation, relationships of positive versus negative affect with other variables an increase is interpreted as the opposite (Reyes del Paso (Quirin et al., 2009a,b, 2011). Therefore, the procedure of et al., 2013). Total peripheral resistance is used to measure the IPANAT itself lends to higher levels of construct validity the resistance of vessels and blood viscosity against the blood with respect to measuring affect (instead of attitudes or self- stream generated by the heart as an index of vasoconstrictive and concepts). Still, this leaves open the question of what kind elastic properties of the peripheral vasculature. Heightened total of connections we will find when comparing the implicit peripheral resistance is considered a way to measure sympathetic measurements empirically. activity (Hill et al., 2013). Finally, there are findings indicating the neurobiological Also widely used for exploring autonomous physiological and behavioral relevance of the concept of implicit affect. For reactions is cortisol as hormonal end product of the example, the construction of affective experiences is discussed hypothalamus-pituitary-adrenal axis mediating many metabolic as an interplay between and integration of explicit and implicit processes (e.g., enhancing cardiovascular output, respiration, affect (Quirin et al., 2011; Quirin and Lane, 2012), its value energy delivery, modulating immune responses) to adapt to for cognition (Quirin et al., 2011; Kazén et al., 2015), decision environmental challenges. Cortisol is released following a diurnal making (Tamir et al., 2015), influence on behavior without rhythm, meaning cortisol levels reach short and high peaks, eliciting explicit affect (Gendolla, 2012; Tamir et al., 2015), especially during the second half of the night. In addition, there and effort-related cardiac responses (Freydefont and Gendolla, is an increase within 20–30 min after awakening in the morning, Frontiers in Psychology | www.frontiersin.org 3 July 2019 | Volume 10 | Article 1634 Weil et al. Implicit Affect and Physiology called the cortisol awakening response. The exact function of the ambulatory study, while explicit affect had no predictive power. cortisol awakening response remains an open question, but it is Implicit sadness was positively related to next day’s cortisol discussed as part of anticipation processes regarding upcoming awakening response, indicating that implicit sadness could play demands of the day (Fries et al., 2009). a role in the anticipation reactions of next day’s stressors. In sum, the latter findings indicate that implicit compared to explicit affect has a higher predictive value for processes of cortisol CONNECTIONS BETWEEN IMPLICIT secretion and regulation. AFFECT AND AUTONOMOUS NERVOUS Another avenue of research focused on the associations SYSTEM between implicit affect and cardiovascular stress response and recovery. Specifically, Brosschot et al. (2014) found that blood According to Cacioppo et al. (1993) the relationship between pressure recovery after harassment induction was faster for affect and more broadly investigated physiological reactions individuals high in implicit positive or low in INA. van der Ploeg is to some degree ambiguous and highly context-dependent et al. (2016) demonstrated that high INA was related to higher (see also Mauss et al., 2005; Bradley and Lang, 2007; Kreibig, systolic blood pressure, lower heart rate variability and total 2010). According to Evers et al. (2014) weaknesses of response peripheral resistance after harassment, while there was no such coherence across multiple affect components might depend on linkage for explicit measures. Low IPA was partly related to slower the degree responses take place automatically or involve reflective recovery. This is in line with dual process models, which postulate cognitive processes. Thus, implicit affect as part of a pre- two distinct modes of information processing, implicit versus reflective process could shed light on the connection between explicit, operating relatively independent from each other and ANS reactions and different affect components. For example, showing different effects on physiological and behavioral outputs limbic-system structures such as amygdala, hypothalamus, and (e.g., Evers et al., 2014). All in all, the above-mentioned findings the mesolimbic dopaminergic system play a major role in suggest that low IPA and high INA as assessed by the IPANAT physiological and endocrine components of affect (e.g., Cacioppo could play independently from each other roles in prolonged et al., 1999). At the same time, cortical and paralimbic areas such cardiovascular stress recovery. as ventromedial prefrontal cortex, ventral and pregenual anterior cingulate cortex, anterior insula, somatosensory cortex, and right parietal cortex play a major role in the generation of implicit affect LIMITATIONS AND CONSIDERATIONS or “background feelings” (Lane, 2008). Still, distributed network FOR FUTURE STUDIES models of the emotional brain emphasize the interplay between a large range of neural systems participating in affective processes To our knowledge, this is the first review focusing on implicit and relativize the functional specialization of specific cerebral affect (measured by the IPANAT) and physiological processes. areas (Pessoa, 2013). Although we have not fully understood the way implicit affect, Although implicit affect and physiological reactions as measured by the IPANAT, intertwines with explicit affect, to affective stimuli are different components of affective ANS functions and other human reactions, it is certain that the experiences, affect-related physiological responses, cognitive outlined findings and models regarding implicit affect point to appraisals, subjective feelings, and expressive behavior a promising approach of gaining more knowledge about affect, are considered to activate implicit affect representations, functions of the ANS and their interplay. via increments in the accessibility of valence-congruent To further specify what kind of information we can obtain cognitive representations (Quirin et al., 2009a). In fact, from the IPANAT more research is needed to analyze the there is first evidence that implicit affect is related to relations to other implicit measures or linkages to subtle, affective-physiological experiences. involuntary facial expressions, for example measured by the According to Suslow et al. (2015) INA as measured by the Facial Action Coding system (Ekman and Friesen, 1978). IPANAT is associated with activation of subcortical, striatal areas The findings for associations between cardiovascular responses in response to briefly shown threatening body language and its and implicit affect are also raising the question whether the recognition, demonstrating the potential usefulness of implicit connection is due to the state or trait part of implicit affect affect measures in predicting spontaneous brain reactions to measured by the IPANAT (Brosschot et al., 2014; van der Ploeg affective stimuli. In addition, and in line with the theory that et al., 2016). More studies are needed to provide such insights unconscious (prolonged) stress plays an important role within into the nature of implicit affect. the etiology of psychiatric diseases (Davis et al., 2017), there is To further explore links between ANS reactions and implicit evidence for a connection between implicit affect and automatic affect, we advise to consider different ways of measuring ANS psychophysiological stress responses. functions. Regarding measurements already used, heart rate For example, Quirin et al. (2009b) found that INA but not variability is thought to be an adequate index of affective explicit negative affect and IPA predicted cortisol responses responsivity only if the stimuli have strong affective value (Choi to immediate noise threats. By contrast, IPA was reversely et al., 2017) and is also a controversial measure of sympathetic related to the cortisol awakening response but unrelated to tone (Reyes del Paso et al., 2013). Against this background, it INA. Compatibly, Mossink et al. (2015) observed an indirect might be valuable to use other kinds of physiological measures. connection between INA, IPA, and cortisol levels in a 24-h For example, Kreibig (2010) points out the importance of Frontiers in Psychology | www.frontiersin.org 4 July 2019 | Volume 10 | Article 1634 Weil et al. Implicit Affect and Physiology respiratory indices, especially for investigating distinct affects (2018) found hints for dysfunctional implicit affective regulation like fear and anger. Skin conductance is also an essential index in individuals with high anxiety. INA predicted a bias for gaze for affective and physiological reactions (Hill et al., 2013). behavior toward sad faces in healthy young individuals without a Moreover, salivary secretion, influenced by sympathetic and history of clinical depression (Bodenschatz et al., 2018). Because parasympathetic nerves (Proctor and Carpenter, 2007), also negative attentional biases are thought to represent important shows sensitivity to affective reactions in terms of declining when trait-like characteristics of individuals vulnerable to depression the individual is disgusted (Vicario et al., 2017) or in a tense, (Gotlib and Joormann, 2010), the finding of Bodenschatz et al. concentrated state (Gemba et al., 1996). (2018) demonstrates the potential utility of implicit affectivity In addition, it may be helpful to control characteristics of measures in studying depression-relevant cognitive vulnerability. the task such as time within the day, sex, age, and race. This is Additionally, dissociations between implicit and explicit affect because these variables can significantly influence ANS reactions can also help to gain insights into the functions of affective (Fries et al., 2009; Hill et al., 2013; Brindle et al., 2014; Choi symptoms. For individuals with borderline personality disorder et al., 2017) or diminish the accuracy of the IPANAT, e.g., due to higher explicit negative affect but similar INA in comparison to repetition (Brosschot et al., 2014) or small manipulation effects healthy individuals was found, adding evidence to the assumption (Quirin et al., 2009b). Furthermore, combining the IPANAT with that negative affect in borderline personality disorder can have neurotransmitter measurements seems to be promising because appellative functions (Dukalski et al., 2017). Malhi et al. (2007) there is evidence that neurotransmitter circuits, underlying found that euthymic bipolar patients are less responsive to affective and autonomous nervous functions, are overlapping implicit affect induction. Not least, Marwood et al. (2018) (Ehlers and Todd, 2017). Another open question remains the suggested using implicit affect measures to validate therapy kind of role different areas and networks of the brain play in success, which seems to be a promising approach as supplement processing implicit affect. For example, it has been argued that of self-report and explicit measures of affect. The value of this cognitive judgments are influenced by concurrent physiological approach might be demonstrated by Remmers et al. (2016) parameters that may be recognized in interoceptive brain areas showing that mindfulness improves implicit affect regulation. (e.g., insula; Lane, 2008; Craig, 2009) and integrated with In summary, the IPANAT as an economic instrument for the cognitive aspects in the ventromedial prefrontal cortex as an assessment of implicit affect has been shown to be associated affective-cognitive convergence zone (Lane, 2008), however, with ANS functioning such as stress-related cardiovascular these assumptions still need to be tested. In view of the diverse activity and cortisol secretion, beyond explicit methods adding findings and sometimes small effect sizes for linkages between another interesting dimension with its own explanatory value. affect measured by the IPANAT as well as explicit affect with Accordingly, it appears essential to differentiate between implicit ANS reactions, more research should be conducted looking for and explicit pathways of affective processing. The IPANAT possible moderator or mediator variables (Cacioppo et al., 2000), represents a promising research tool that may help to broaden for example implicit memory biases (Mossink et al., 2015). our knowledge about ANS functioning, affective processes and As IPA and INA show different patterns of relations for their interplay in both healthy individuals and those with example with cortisol reactions (Quirin et al., 2009b; Mossink mental disorders. et al., 2015), it is also possible that we can observe complex connection patterns, depending on the valence of implicit affect we measure, the bodily response in question or point of time AUTHOR CONTRIBUTIONS within the cycle of the physiological reaction. Also there are mixed findings concerning distinct patterns of ANS functions for TS, A-SW, and MQ conceived the outline for this review. basic explicit affects (Cacioppo et al., 2000; Kreibig, 2010; Quigley A-SW wrote the manuscript with revisions and contributions and Feldman Barrett, 2014). Possibly, within this research context from GPH, TS, and MQ. a special variant of the IPANAT assessing discrete affects (Quirin and Bode, 2014) could be administered. The assessment of implicit affect could also provide more FUNDING insight into the etiology and treatment processes of psychiatric diseases. For example, there is evidence that (long term) both This work was partially made possible through a grant unconscious stress and IPA (as a “stress buffer”) play an from the Templeton Rlg. Trust (TRT 0119) supporting MQ; important role in stress recovery, and therefore in handling by the National Council for Science and Technology of stressful situations (Quirin et al., 2009b; Brosschot, 2010; Mexico (CONACyT) and the Spanish Government (under Grant Brosschot et al., 2014; van der Ploeg et al., 2016). Liu et al. PSI2016-76411-R) supporting GPH. REFERENCES Psychiatry Res. 265, 48–54. doi: 10.1016/j.psychres.2018.04.007 doi: 10.1016/ j.psychres.2018.04.007 Bodenschatz, C. M., Skopinceva, M., Kersting, A., Quirin, M., and Suslow, T. Bower, G. H. (1981). Mood and memory. Am. Psychol. 36, 129–148. (2018). Implicit negative affect predicts attention to sad faces beyond self- Bradley, M. M., and Lang, P. J. (2007). “The International Affective Picture reported depressive symptoms in healthy individuals: an eye-tracking study. System (IAPS) in the study of emotion and attention,” in Handbook of Emotion Frontiers in Psychology | www.frontiersin.org 5 July 2019 | Volume 10 | Article 1634 Weil et al. Implicit Affect and Physiology Elicitation and Assessment, eds J. A. Coan and J. J. B. Allen (New York, NY: Fries, E., Dettenborn, L., and Kirschbaum, C. (2009). The cortisol awakening Oxford University Press), 29–46. response (CAR): facts and future directions. Int. J. Psychophysiol. 72, 67–73. Brindle, R. C., Ginty, A. T., Phillips, A. C., and Carroll, D. (2014). A tale of two doi: 10.1016/j.ijpsycho.2008.03.014 mechanisms: a meta-analytic approach toward understanding the autonomic Gainotti, G. (2012). Unconscious processing of emotions and the right hemisphere. basis of cardiovascular reactivity to acute psychological stress. Psychophysiology Neuropsychologia 50, 205–218. doi: 10.1016/j.neuropsychologia.2011.12.005 51, 964–976. doi: 10.1111/psyp.12248 Gemba, H., Teranaka, A., and Takemura, K. (1996). Influences of emotion upon Brosschot, J. F. (2010). Markers of chronic stress: prolonged physiological parotid secretion in human. Neurosci. Lett. 211, 159–162. doi: 10.1016/0304- activation and (un)conscious perseverative cognition. Neurosci. Biobehav. Rev. 3940(96)12741-5 35, 46–50. doi: 10.1016/j.neubiorev.2010.01.004 Gendolla, G. H. E. (2012). Implicit affect primes effort: a theory and research Brosschot, J. F., Geurts, S. A. E., Kruizinga, I., Radstaak, M., Verkuil, B., Quirin, M., on cardiovascular response. Int. J. Psychophysiol. 86, 123–135. doi: 10.1016/j. et al. (2014). Does unconscious stress play a role in prolonged cardiovascular ijpsycho.2012.05.003 stress recovery? Stress Health 30, 179–187. doi: 10.1002/smi.2590 Gotlib, I. H., and Joormann, J. (2010). Cognition and depression: current status and Cacioppo, J. T., Berntson, G. G., Larsen, J. T., Poehlmann, K. M., and Ito, T. A. future directions. Annu. Rev. Clin. Psychol. 6, 285–312. doi: 10.1146/annurev. (2000). “The Psychophysiology of Emotion,” in Handbook of Emotions, 2nd clinpsy.121208.131305 Edn, eds R. Lewis, J. M. Haviland-Jones, M. Lewis, and J. M. Haviland-Jones Greenwald, A., Nosek, B., and Banaji, M. (2003). Understanding and using the (New York: Guilford Press), 173–191. implicit association test: I. An improved scoring algorithm. J. Personal. Soc. Cacioppo, J. T., Gardner, W. L., and Berntson, G. G. (1999). The affect system Psychol. 85, 197–216. doi: 10.1037/0022-3514.85.2.197 has parallel and integrative processing components: form follows function. Gyurak, A., Gross, J. J., and Etkin, A. (2011). Explicit and implicit emotion J. Personal. Soc. Psychol. 76, 839–855. doi: 10.1037//0022-3514.76.5.839 regulation: a dual-process framework. Cogn. Emot. 25, 400–412. doi: 10.1080/ Cacioppo, J. T., Klein, D. J., Berntson, G., and Hatfield, E. (1993). “The 02699931.2010.544160 Psychophysiology of Emotion,” in Handbook of Emotion, eds R. Lewis and J. M. Hill, L., Sollers Ill, J. J., and Thayer, J. F. (2013). Resistance reconstructed: Haviland (New York, NY: Guilford Press). estimation of total peripheral resistance from computationally-derived cardiac Choi, K.-H., Kim, J., Kwon, O. S., Kim, M. J., Ryu, Y. H., and Park, J.-E. (2017). Is output. Biomed. Sci. Instrum. 49, 216–223. heart rate variability (HRV) an adequate tool for evaluating human emotions? A Kazén, M., Kuhl, J., and Quirin, M. (2015). Personality interacts with implicit affect focus on the use of the International Affective Picture System (IAPS). Psychiatry to predict performance in analytic versus holistic processing. J. Personal. 83, Res. 251, 192–196. doi: 10.1016/j.psychres.2017.02.025 251–261. doi: 10.1111/jopy.12100 Clore, G. L., and Ortony, A. (2000). “Cognitive Neuroscience of Emotion,” in Series Kreibig, S. D. (2010). Autonomic nervous system activity in emotion: a review. Biol. in Affective Science. Cognitive Neuroscience of Emotion, eds R. D. R. Lane, L. Psychol. 84, 394–421. doi: 10.1016/j.biopsycho.2010.03.010 Nadel, G. L. Ahern, J. Allen, and A. W. Kaszniak (Oxford: Oxford University Lane, R. D. (2008). Neural substrates of implicit and explicit emotional processes: a Press), 24–61. unifying framework for psychosomatic medicine. Psychosom. Med. 70, 214–231. Craig, A. D. B. (2009). How do you feel–now? The anterior insula and human doi: 10.1097/PSY.0b013e3181647e44 awareness. Nat. Rev. Neurosci. 10, 59–70. doi: 10.1038/nrn2555 Levenson, R. W. (2014). The autonomic nervous system and emotion. Emot. Rev. Critchley, H. D., Corfield, D. R., Chandler, M. P., Mathias, C. J., and Dolan, R. J. 6, 100–112. doi: 10.1177/1754073913512003 (2000). Cerebral correlates of autonomic cardiovascular arousal: a functional Lieberman, M. D. (2019). Boo! The consciousness problem in emotion. Cogn. neuroimaging investigation in humans. J. Physiol. 523, 259–270. doi: 10.1111/j. Emot. 33, 24–30. doi: 10.1080/02699931.2018.1515726 1469-7793.2000.t01-1-00259.x Liu, B., Wang, Y., and Li, X. (2018). Implicit emotion regulation deficits in Trait Damasio, A. R. (2002). “A Second Chance for Emotion,” in Series in Affective Anxiety: an ERP study. Front. Hum. Neurosci. 12:382. doi: 10.3389/fnhum.2018. Science. Cognitive Neuroscience of Emotion, eds R. D. Lane and L. Nadel 00382 (Oxford: Oxford University Press). Malhi, G. S., Lagopoulos, J., Owen, A. M., Ivanovski, B., Shnier, R., and Sachdev, Davis, M. T., Holmes, S. E., Pietrzak, R. H., and Esterlis, I. (2017). Neurobiology of P. (2007). Reduced activation to implicit affect induction in euthymic bipolar chronic stress-related psychiatric disorders: evidence from molecular imaging patients: an fMRI study. J. Affect. Disord. 97, 109–122. doi: 10.1016/j.jad.2006. studies. Chronic Stress 1, 1–32. doi: 10.1177/2470547017710916 06.005 Dukalski, B., Quirin, M., Kersting, A., Suslow, T., and Donges, U.-S. (2017). Marwood, L., Wise, T., Perkins, A. M., and Cleare, A. J. (2018). Meta-analyses of the Implicit affectivity in patients with borderline personality disorder. Riv. neural mechanisms and predictors of response to psychotherapy in depression Psichiatr. 52, 83–89. doi: 10.1708/2679.27444 and anxiety. Neurosci. Biobehav. Rev. 95, 61–72. doi: 10.1016/j.neubiorev.2018. Egloff, B., and Schmukle, S. C. (2002). Predictive validity of an implicit association 09.022 test for assessing anxiety. J. Personal. Soc. Psychol. 83, 1441–1455. doi: 10.1037/ Mason, W. A., and Capitanio, J. P. (2012). Basic emotions: a reconstruction. Emot. 0022-3514.83.6.1441 Rev. 4, 238–244. doi: 10.1177/1754073912439763 Ehlers, M. R., and Todd, R. M. (2017). Genesis and maintenance of attentional Mauss, I. B., Levenson, R. W., McCarter, L., Wilhelm, F. H., and Gross, J. J. biases: the role of the Locus Coeruleus-noradrenaline system. Neural Plast. (2005). The tie that binds? Coherence among emotion experience, behavior, and 2017, 6817349. doi: 10.1155/2017/6817349 physiology. Emotion 5, 175–190. doi: 10.1037/1528-3542.5.2.175 Ekman, P., and Friesen, W. (1978). Facial Action Coding System: Investigator’s Montag, C., and Panksepp, J. (2017). Primary emotional systems and personality: Guide. Palo Altom: Consulting Psychologists Press. an evolutionary perspective. Front. Psychol. 8:464. doi: 10.3389/fpsyg.2017. Evers, C., Hopp, H., Gross, J. J., Fischer, A. H., Manstead, A. S. R., and Mauss, I. B. 00464 (2014). Emotion response coherence: a dual-process perspective. Biol. Psychol. Moors, A. (2010). Automatic constructive appraisal as a candidate 98, 43–49. doi: 10.1016/j.biopsycho.2013.11.003 cause of emotion. Emot. Rev. 2, 139–156. doi: 10.1177/175407390935 Fazio, R. H., and Olson, M. A. (2003). Implicit measures in social cognition. 1755 research: their meaning and use. Annu. Rev. Psychol. 54, 297–327. doi: 10.1146/ Moors, A. (2013). On the causal role of appraisal in emotion. Emot. Rev. 5, 132–140. annurev.psych.54.101601.145225 doi: 10.1177/1754073912463601 Folkow, B. (2000). Perspectives on the integrative functions of the ‘sympatho- Mossink, J. C. L., Verkuil, B., Burger, A. M., Tollenaar, M. S., and Brosschot, J. F. adrenomedullary system’. Auton. Neurosci. 83, 101–115. doi: 10.1016/S1566- (2015). Ambulatory assessed implicit affect is associated with salivary cortisol. 0702(00)00171-5 Front. Psychol. 6:111. doi: 10.3389/fpsyg.2015.00111 Forgas, J. P. (1992). “Affect in social judgments and decisions: A multi- process Panksepp, J., and Watt, D. (2011). What is basic about basic emotions? lasting model,” in Advances in experimental social psychology, ed. M. P. Zanna (San lessons from affective neuroscience. Emot. Rev. 3, 387–396. doi: 10.1177/ Diego, CA: Academic Press), 227–275. doi: 10.1016/s0065-2601(08)60285-3 1754073911410741 Freydefont, L., and Gendolla, G. H. E. (2012). Incentive moderates the impact of Payne, B. K., Cheng, C. M., Govorun, O., and Stewart, B. D. (2005). An inkblot implicit anger vs. sadness cues on effort-related cardiac response. Biol. Psychol. for attitudes: affect misattribution as implicit measurement. J. Personal. Soc. 91, 120–127. doi: 10.1016/j.biopsycho.2012.04.002 Psychol. 89, 277–293. doi: 10.1037/0022-3514.89.3.277 Frontiers in Psychology | www.frontiersin.org 6 July 2019 | Volume 10 | Article 1634 Weil et al. Implicit Affect and Physiology Penner, A. E., and Stoddard, J. (2018). Clinical affective neuroscience. J. Am. Acad. Sulejmanov, F., and Spasovski, O. (2018). Psychometric properties of the Child Adolesc. Psychiatr. 57, 906–908. Macedonian version of the Implicit Positive and Negative Affect Test (IPANAT– Pessoa, L. (2013). The Cognitive-Emotional Brain. From Interactions to Integration. M). Rev. Psychol. 24, 39–44. doi: 10.21465/RP0024.0004 Cambridge: MIT Press. Suslow, T., Ihme, K., Quirin, M., Lichev, V., Rosenberg, N., Bauer, J., Proctor, G. B., and Carpenter, G. H. (2007). Regulation of salivary gland function et al. (2015). Implicit affectivity and rapid processing of affective body by autonomic nerves. Auton. Neurosci. 133, 3–18. doi: 10.1016/j.autneu.2006. language: an fMRI study. Scand. J. Psychol. 56, 545–552. doi: 10.1111/sjop. 10.006 12227 Quigley, K. S., and Feldman Barrett, L. (2014). Is there consistency and specificity of Tamir, M., Bigman, Y. E., Rhodes, E., Salerno, J., and Schreier, J. (2015). An autonomic changes during emotional episodes? Guidance from the conceptual expectancy-value model of emotion regulation: implications for motivation, act theory and psychophysiology. Biol. Psychol. 98, 82–94. doi: 10.1016/j. emotional experience, and decision making. Emotion 15, 90–103. doi: 10.1037/ biopsycho.2013.12.013 emo0000021 Quirin, M., and Bode, R. C. (2014). An Alternative to Self-Reports of Trait and State Tracy, J. L., and Randles, D. (2011). Four models of basic emotions: a review of Affect. Eur. J. Psychol. Assess. 30, 231–237. doi: 10.1027/1015-5759/a000190 Ekman and Cordaro, Izard, Levenson, and Panksepp and Watt. Emot. Rev. 3, Quirin, M., Bode, R. C., and Kuhl, J. (2011). Recovering from negative events 397–405. doi: 10.1177/1754073911410747 by boosting implicit positive affect. Cogn. Emot. 25, 559–570. doi: 10.1080/ van der Ploeg, M. M., Brosschot, J. F., Thayer, J. F., and Verkuil, B. (2016). 02699931.2010.536418 The Implicit positive and negative affect test: validity and relationship with Quirin, M., Kazén, M., and Kuhl, J. (2009a). When nonsense sounds happy or cardiovascular stress-responses. Front. Psychol. 7:425. doi: 10.3389/fpsyg.2016. helpless: the implicit positive and negative affect test (IPANAT). J. Personal. Soc. 00425 Psychol. 97, 500–516. doi: 10.1037/a0016063 Vicario, C. M., Sommer, W., Kuran, K. A., and Rafal, R. D. (2017). Salivary Quirin, M., Kazén, M., Rohrmann, S., and Kuhl, J. (2009b). Implicit but not explicit secretion and disgust: a pilot study. Acta Psychol. 178, 18–24. doi: 10.1016/j. affectivity predicts circadian and reactive cortisol: using the implicit positive actpsy.2017.05.007 and negative affect test. J. Personal. 77, 401–425. doi: 10.1111/j.1467-6494.2008. Watson, D., Clark, L. A., and Tellegen, A. (1988). Development and validation 00552.x of brief measures of positive and negative affect: the PANAS scales. Quirin, M., and Lane, R. D. (2012). The construction of emotional experience J. Personal. Soc. Psychol. 54, 1063–1070. doi: 10.1037//0022-3514.54.6. requires the integration of implicit and explicit emotional processes. Behav. 1063 Brain Sci. 35, 159–160. doi: 10.1017/S0140525X11000446 Winkielman, P., Berridge, K. C., and Wilbarger, J. L. (2005). Unconscious affective Quirin, M., Wróbel, M., Norcini Pala, A., Stieger, S., Brosschot, J., Kazén, M., reactions to masked happy versus angry faces influence consumption behavior et al. (2018). A cross-cultural validation of the implicit positive and negative and judgments of value. Personal. Soc. Psychol. Bull. 31, 121–135. doi: 10.1177/ affect test (IPANAT). Eur. J. Psychol. Assess. 34, 52–63. doi: 10.1027/1015-5759/ 0146167204271309 a000315 Remmers, C., Topolinski, S., and Koole, S. L. (2016). Why being mindful may have Conflict of Interest Statement: The authors declare that the research was more benefits than you realize: mindfulness improves both explicit and implicit conducted in the absence of any commercial or financial relationships that could mood regulation. Mindfulness 7, 829–837. doi: 10.1007/s12671-016-0520-1 be construed as a potential conflict of interest. Reyes del Paso, G. A., Langewitz, W., Mulder, L. J. M., van Roon, A., and Duschek, S. (2013). The utility of low frequency heart rate variability as an index of Copyright © 2019 Weil, Hernández, Suslow and Quirin. This is an open-access article sympathetic cardiac tone: a review with emphasis on a reanalysis of previous distributed under the terms of the Creative Commons Attribution License (CC BY). studies. Psychophysiology 50, 477–487. doi: 10.1111/psyp.12027 The use, distribution or reproduction in other forums is permitted, provided the Scherer, K. R., and Moors, A. (2019). The emotion process: event appraisal and original author(s) and the copyright owner(s) are credited and that the original component differentiation. Annu. Rev. Psychol. 70, 719–745. doi: 10.1146/ publication in this journal is cited, in accordance with accepted academic practice. No annurev-psych-122216-011854 use, distribution or reproduction is permitted which does not comply with these terms. Frontiers in Psychology | www.frontiersin.org 7 July 2019 | Volume 10 | Article 1634