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Physiological Feelings T ⁎ Edward F Neuroscience and Biobehavioral Reviews 103 (2019) 267–304 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev Review article ☆ Physiological feelings T ⁎ Edward F. Pace-Schotta, , Marlissa C. Amoleb, Tatjana Auec, Michela Balconid, Lauren M. Bylsmab, Hugo Critchleye, Heath A. Demareef, Bruce H. Friedmang, Anne Elizabeth Kotynski Goodingf, Olivia Gosseriesh, Tanja Jovanovici, Lauren A.J. Kirbyj, Kasia Kozlowskak, Steven Laureysh, Leroy Lowel, Kelsey Mageef, Marie-France Marinm, Amanda R. Mernerf, Jennifer L. Robinsonn, Robert C. Smitho, Derek P. Spanglerp, Mark Van Overveldq, Michael B. VanElzakkerr a Harvard Medical School, Boston, MA, USA b University of Pittsburgh, Pittsburgh, PA, USA c University of Bern, Bern, Switzerland d Catholic University of Milan, Milan, Italy e University of Sussex, Sussex, UK f Case Western Reserve University, Cleveland, OH, USA g Virginia Tech, Blacksburg, VA, USA h University of Liege, Liege, Belgium i Emory University, Atlanta, GA, USA j University of Texas at Tyler, Tyler, TX, USA k University of Sydney, Sydney, Australia l Neuroqualia (NGO), Truro, Nova Scotia, Canada m Université du Québec à Montréal, Montreal, Canada n Auburn University, Auburn, AL, USA o Michigan State University, East Lansing, MI, USA p United States Army Research Laboratory, Aberdeen, MD, USA q Erasmus University Rotterdam, Rotterdam, the Netherlands r Massachusetts General Hospital, Boston, MA, USA ARTICLE INFO ABSTRACT Keywords: The role of peripheral physiology in the experience of emotion has been debated since the 19th century fol- Emotion lowing the seminal proposal by William James that somatic responses to stimuli determine subjective emotion. Feelings Subsequent views have integrated the forebrain's ability to initiate, represent and simulate such physiological Interoception events. Modern affective neuroscience envisions an interacting network of “bottom-up” and “top-down” sig- Somatic markers naling in which the peripheral (PNS) and central nervous systems both receive and generate the experience of Emotion regulation emotion. “Feelings” serves as a term for the perception of these physical changes whether emanating from actual Autonomic nervous system Insula somatic events or from the brain's representation of such. “Interoception” has come to represent the brain's receipt and representation of these actual and “virtual” somatic changes that may or may not enter conscious awareness but, nonetheless, influence feelings. Such information can originate from diverse sources including endocrine, immune and gastrointestinal systems as well as the PNS. We here examine physiological feelings from diverse perspectives including current and historical theories, evolution, neuroanatomy and physiology, de- velopment, regulatory processes, pathology and linguistics. Introduction bodily sensations. Indeed, if one accepts the notion that consciousness is grounded in biological processes (Crick, 1994; Damasio, 1994; Conscious emotional experience is closely bound to changes in Pinker, 2018), emotional experience must, by its nature, be ☆ Please note: Co-author listing is based on alphabetical order. ⁎ Corresponding author at: Harvard Medical School, Massachusetts General Hospital – East, CNY 149 13th Street Room 2605, Charlestown, MA 02129, USA. E-mail address: [email protected] (E.F. Pace-Schott). https://doi.org/10.1016/j.neubiorev.2019.05.002 Received 13 November 2018; Received in revised form 27 March 2019; Accepted 3 May 2019 Available online 22 May 2019 0149-7634/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). E.F. Pace-Schott, et al. Neuroscience and Biobehavioral Reviews 103 (2019) 267–304 physiological. However, the direction of causality and the specificity of are deployed as predictions of probable interoceptive experience, to relationships between physiological processes and emotional experi- yield ‘prediction errors’, i.e., the difference between an expected in- ence have been topics of debate since at least the 19th century. This ternal state and afferent interoceptive data (Barrett and Simmons, review focuses on interaction between subjective emotional experience 2015; Paulus and Yu, 2012; Saxe and Houlihan, 2017; Seth and Friston, and the body. Specifically, we address how emotional feelings are in- 2016). One remarkable corollary of this perspective is that, when pre- formed by physiological processes that are detected by peripheral organ diction errors are small, interoceptive experience may be generated ‘interoceptors’, encoded and transmitted from the peripheral nervous largely by what our brain expects to feel rather than by actual afferent system (PNS), to be represented at specific levels of the central nervous neural signals from the periphery (Barrett and Simmons, 2015; Seth and system (CNS). We additionally address how emotional experience may Friston, 2016). Also the ‘top-down’ efferent neural drive to the PNSto encompass the prediction, as well as feedback, of physiological change the internal bodily state supports ‘active inference’, whereby changes, through efferent responses from CNS to PNS that change prediction errors are minimized by changing the input (feedback) at bodily physiology as an obligatory component of an emotive response. source. These counterintuitive possibilities capture the key function of This work is undertaken as part of ‘The Human Affectome Project’, interoception in the maintenance of physiological homeostasis (Seth an initiative organized in 2016 by a non-profit organization called and Friston, 2016). Thus, centrally-generated predictions of physiolo- Neuroqualia. The project aims to produce a series of overarching re- gical states are expressed in autonomic reflexes. Unpredicted inter- views that summarize current knowledge about affective neuroscience oceptive inputs generate prediction errors, which trigger both emo- and the language that we use to convey feelings and emotions. The tional feelings and homeostatic responses (Seth and Friston, 2016). projects comprise twelve teams, organized into a task force with the Although this review will not describe in detail the theoretical and aim of developing a comprehensive and integrated model of affect to computational models of predictive coding, active inference or Baye- serve as a common focal point for future affective research. To that end, sian analyses of the physiology of emotions, it is crucial to bear in mind our team was specifically tasked to review neuroscience research onthe that the reality of perceived emotions (including their interoceptive relationship between subjective experiences of emotion and associated components) encompasses more than the direct representation of per- physiological processes. We were also asked to review the language that ipheral states and includes central predictions of peripheral physiology. people use to express feelings that relate to physiological processes and Another important, but difficult distinction is between emotion and consider whether or not feelings that people convey in language might mood (Beedie et al., 2005). Typically these are operationally dis- inform the way we approach neuroscience research on these topics. An tinguished by duration and sometimes by intensity or reactivity (Beedie important reason to focus on the physiology of emotional experience et al., 2005; Kaplan et al., 2016), but consensus regarding cutoffs on and expression along with consideration of emotional language is the any dimension is lacking. This review conceptualizes emotion as a well-documented imprecision inherent in self-report instruments for phasic response, yet recognizes its overlap with the enduring phe- such experiences (Harmon-Jones et al., 2016; Mauss and Robinson, nomenon of mood (particularly when describing interoceptive influ- 2009). Moreover, emotion is a multi-component process hence it is ences of tonic or gradually changing physiological state including the important to examine from different levels, including physiology, fluctuating hormonal milieu, pain, sickness and inflammation). Indeed, which is complementary to self-reported experience and behavior. mood states are perhaps the affective phenomena most strongly influ- A unifying theme of this review is that the subjective experience of enced by interoception and are recognizably a powerful biasing factor emotion is influenced, and often determined by CNS representations of for the subjective experience and regulation of affective feelings in both afferent sensory input from peripheral organs and tissues –con- normal emotion (Ritchie et al., 2009; Sereno et al., 2015) and psy- ventionally termed interoception (Craig, 2016; Critchley and Garfinkel, chopathology (Gilbert et al., 2013). 2017; Damasio and Carvalho, 2013). We strive to follow Damasio and This review will not seek to provide an exhaustive account of the Carvalho's (Damasio and Carvalho, 2013) distinction between ‘emotion’ physiology of emotion or the phenomenon of interoception. Instead, we – an adaptive, patterned neural response akin to physiological drives highlight a sample of important theories and discoveries with an ap- such as hunger and thirst, and ‘feeling’ – internal sensations resulting preciation for their historical precedents and clinical relevance. The from these patterned responses as well as from other interoceptive following
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