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The Physiological Study of Emotional Piloerection: a Review and Guide for Future Research

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The Physiological Study of Emotional Piloerection: a Review and Guide for Future Research The physiological study of emotional piloerection: A review and guide for future research Jonathon McPhetres Durham University Word count: 8,322 Abstract This paper provides an accessible review of the biological and psychological evidence to guide new and experienced researchers in the study of emotional piloerection in humans. I first discuss the mechanisms and function of non-emotional and emotional piloerection. A systematic review (N = 27) reveals that indices of sympathetic activation are abundant, suggesting emotional piloerection occurs with increased skin conductivity and heart rate. Measures of emotions and parasympathetic activation are lacking and no clear conclusions can be drawn. Finally, I provide an overview of the methodological possibilities and I highlight some pressing questions researchers may wish to answer in future studies. Keywords: Emotion; physiology; biology; piloerection; methodology; systematic review 2 Introduction Piloerection—also known as goosebumps or goose pimples—is the contraction of small muscles at the base of hair follicles resulting in visible erection of hair. Piloerection has many different functions in different species. In mammals, piloerection most commonly serves as a form of temperature regulation (Chaplin, Jablonski, Sussman, & Kelley, 2014; Tansey & Johnson, 2015). In non-human animals, piloerection is also a method of making animals appear larger in response to threat. In humans, however, piloerection also occurs in response to a wide variety of emotional stimuli. This emotional piloerection is not well understood and raises many interesting questions about the psychology and physiology of emotion. The goal of this review is to provide an accessible guide to the scientific study of piloerection from both biological and psychological perspectives. Some of the research questions from these two perspectives are similar, but many diverge widely. However, they can both inform each other and it is my goal to synthesiZe this information to make cooperation between the two fields easier. Therefore, in this article, I provide an overview of biological foundations of non-emotional piloerection and discuss how it can be used to inform the study of emotional piloerection from a psychological perspective. This review is organiZed into three main sections. First, I discuss the biological mechanisms of piloerection and introduce piloerection as a temperature regulation mechanism. In the second section, I discuss the psychology of emotional piloerection and its physiological correlates. In the final section, I provide an overview of the current methodological state of the art and suggest some ideas for how researchers may move forward in this area. A note on terminology. Many terms are used to refer to piloerection across the literature, and this can be confusing. In this manuscript, I use the term piloerection to refer to the physical 3 contraction of the muscles resulting in hair erection, regardless of the cause. The term goosebump is used when referring to piloerection colloquially—for example, when describing the experience subjectively or relying on self-reports. The term the chills is used almost exclusively in the context of listening to music and often refers to a self-reported sensation; if a paper refers to the chills, I also use this terminology. However, one corollary goal of this paper will also be to determine the similarities and differences between chills and piloerection. Non-emotional Piloerection Biological mechanisms The mechanisms of piloerection have been well-understood since the mid-1800s. For example, in Darwin’s book The expression of emotion in man and animals (Darwin, 1872, pp.101-103), he cites a variety of biological evidence describing piloerection in non-human animals (e.g., Lister, 1853). In the years since, scientific evidence has further illuminated our understanding of the physiological mechanisms underlying piloerection. Presumably, both non-emotional and emotional piloerection rely on the same neurological and molecular mechanisms. In this first section, those mechanisms will be identified briefly so that they can then be applied to the understanding of emotional piloerection. Specifically, it is hoped that researchers can implement this theoretical understanding of piloerection into their research along with a focus on physiological measurement in place of relying purely on self-report. Muscular mechanisms. Piloerection is the result of the contraction of arrector pili muscles (APM), which reside in the dermis layer of skin. APM are smooth muscle bundles between the hair follicle and the connective dermal tissue, and are present at the base of the hair (Barcaui, Piñeiro-Maceira, & De Avelar Alchorne, 2002; Narisawa & Kohda, 1993). Multiple 4 follicular units can share a single muscle (Poblet, Ortega, & JiméneZ, 2002; Song, Hu, & Koh, 2005). When the muscle contracts, the hair follicle is pulled and the hair shaft becomes erect (Hanukoglu et al., 2017; Torkamani, Rufaut, Jones, & Sinclair, 2014). As a result, the skin bunches up and forms little bumps, reducing the surface area and reducing heat loss. The density of hair follicles also differs across bodily sites, with estimates suggesting 14 follicles per cm2 on the calf, 17 on the thigh, 18 on the forearm, 29 on the back, and 32 on the upper arm (Otberg et al., 2004). Most mammals have APM, with some exceptions (Chaplin et al., 2014; Starcher, Aycock, & Hill, 2005). However, birds have feather muscles which are different from the APM in mammals (Homberger & Silva, 2000; Stettenheim, 1972). Thus, while the functions (e.g., increased siZe, temperature regulation) may be the same as that of mammals, the mechanism is not strictly identical. Neurochemical mechanisms. The APM are innervated by the sympathetic nervous system (Hellmann, 1963). Specifically, postganglionic class C nerve fibres provide both adrenergic and cholinergic innervation to dermal organs, including the APM. Some cholinergic fibres were reported in the muscles and are believed to represent parasympathetic fibres (Donadio et al., 2019), though they are sparse and it is unclear whether they are directly responsible for APM functioning. Although the APM are generally believed to be under sympathetic control, they have muscarinic receptors, which are mainly associated with the parasympathetic nervous system. Muscarinic receptors are divided into multiple types, named M1-M5; each are located in different muscle subtypes, can be both excitatory or inhibitory, and are encoded by different genes corresponding to their type (Bonner, Buckley, Young, & Brann, 1987). Specifically, M1, M3, and 5 M5 are excitatory, while M2 and M4 are inhibitory. The APM have M3 receptors, which are found in smooth muscle groups around the body; for example, they are also found in sweat glands, eyes, and the urinary tract. These receptors are unique because, paradoxically, they use acetylcholine (Glatte, Buchmann, HijaZi, Illigens, & Siepmann, 2019) but are under sympathetic control (Chen et al., 2020; Urso et al., 2019). However, M2 receptor activation has also been observed to cause piloerection in mice on at least one occasion (Hoss et al., 1990). In short, acetylcholine is received by the M3 receptor which begins an intracellular signaling process (Qin, Dong, Chunmin, Wu, & Lambert, 2011) that ultimately results in smooth muscle contraction (Carlson & Kraus, 2019). In humans, direct injection of acetylcholine (Rothman & Coon, 1940) and iontophoresis of phenylephrine causes piloerection (Siepmann et al., 2012). Relation to the sympathetic and parasympathetic nervous system. The primary function of the autonomic nervous system is to adjust the body’s function to changes in the external environment. For example, external threats require modifications to blood and oxygen flow by regulating smooth muscle (e.g., as in the “fight or flight” response of the sympathetic nervous system). Additionally, temperature changes require activation of sweat glands to cool the body (in humans) or to trap in a layer of heat (in non-human animals) and promote vasoconstriction (Chaplin et al., 2014; Glatte et al., 2019). The APM appear to be related with both the sympathetic and parasympathetic nervous systems—this is particularly due to their role in temperature regulation but also for a variety of other reasons. For example, the arrector pili muscles are innervated by the sympathetic class C fibres. However, they use muscarinic receptors, which mainly control parasympathetic functions. There is also some evidence of parasympathetic fibres (Donadio et al., 2019). Only a few 6 experimental studies have been published showing deliberate induction of piloerection via direct sympathetic nerve activation (e.g., HijaZi et al., 2020). Muscarinic receptors are responsible for controlling many parasympathetic functions— the “rest and digest” bodily functions—and many of these functions oppose the sympathetic nervous system. For example, muscarinic receptors are found in smooth muscles around the body and act to slow the heart rate, increasing the cardiac refractory period (Dhein, Van Koppen, & Brodde, 2001) and to stimulate intestinal function and contract the airways in the bronchioles, reducing airflow (Carlson & Kraus, 2019). While most sympathetic and parasympathetic functions oppose each other, thermoregulation is unique and is the key function of piloerection (Chaplin et al., 2014). The parasympathetic thermoregulation functions do not necessarily oppose sympathetic functions (Shibasaki
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