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The Spontaneous Brain From the Mind Body to the World Brain Problem Georg Northoff
The Interoceptive Mind From Homeostasis to Awareness
Edited by Manos Tsakiris
Helena De Preester
1
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Preface
Interoception is the body-to-brain axis of signals originating from the internal body and visceral organs (such as gastrointestinal, respiratory, hormonal, and circulatory systems). It plays a unique role in ensuring homeostasis. Interoception therefore refers to the sensing of the state of the inner body and its homeostatic needs, to the ever-fluctuating state of the body beneath its sensory (exteroceptive) and musculoskeletal sheath. By bringing together the perspectives of experimental psychology and cognitive neuroscience, psychophysiology, psychiatry, clinical psychology, and philosophy, this volume aims to go beyond the known role of interoception for homeostasis in order to ask, and hopefully provide, important insights on the role that interoception plays for our mental life and lived experience, for awareness, affect, and cognition.
The perspectives in the ensuing 17 chapters largely fall within the embodied cognition approach that attempted to ground cognition and the self in the body. Over the last three decades, modern psychology and cognitive neurosciences have focused on the importance of the body as the starting point for a science of the self and the subject. However, this focus concerned the body as perceived from the outside, as, for example, when we recognize ourselves in the mirror, or when the brain integrates sensorimotor information to create our sense of body ownership and agency, or even when we perceive other people’s bodies and thereby their mental states via processes of embodied simulation. A first step toward that direction was to consider the role that sensorimotor signals play for the experience and the awareness of one’s self, which goes beyond their well-known role in motor control and sensory perception. For example, research on the sense of agency over one’s actions and the sense of ownership of one’s body demonstrates how these fundamental experiences rely on specific processes of sensorimotor interaction and multisensory integration, respectively (Haggard, 2005; Tsakiris, 2010). Another, closely related step in that direction was the recognition of the proprioceptive dimension of the body for agency, ownership, and the embodied self (Gallager & Cole, 1995; Bermúdez, Marcel, & Eilan, 1995). In the prolific field of social cognitive neuroscience, similar considerations regarding the role of observable sensorimotor events have been extended to social cognition and our understanding of other minds (Gallese, Keysers, & Rizzolatti, 2004). Such theoretical advances have been instrumental in explaining key aspects of the bodily self and its social cognition.
Notwithstanding the influential research that accumulated in this area, it is clear that our fields have neglected another important dimension of the body, namely the interoceptive body, which is the body as perceived from the inside. This visceral dimension of embodiment has, of course, a long-standing history of predominantly physiological investigations during the last century, but it was only relatively recent that interoception
has gained a rapidly expanding interest in the study of human mind. The seminal work of Bud Craig (2009) and Antonio Damasio (1999), despite their differences, placed the visceral milieu, its homeostatic functioning, and our interoceptive awareness thereof at the center stage of self-awareness. In parallel, the development of new methods to measure, not simply interoceptive signaling but our awareness thereof opened up the field of interoceptive research to psychologists and cognitive neuroscientists. In parallel with the exponential increase in the number of publications on the topic, researchers and scholars across physiology, cognitive neuroscience, psychology, philosophy, and medicine are working on interoception without necessarily sharing the same conceptual base or necessarily realizing how their investigations link with the findings and insights of other disciplines and methodologies.
Despite recent advances (Garfinkel et al., 2015; Kleckner et al., 2015), there is consensus that interoception research must develop psychologically relevant and philosophically sound theoretical foundations, a wider and more grounded measurement model and a fuller characterization of the links between different interoceptive dimensions and systems if it is to achieve its appropriate place within the life and mind sciences. This ambitious aim necessitates wide-ranging, dedicated, and systematic theoretical and methodological enquiries into the hierarchical relations in interoceptive processing, the horizontal relations across interoceptive modalities, and the causal relations between interoception and awareness. For example, psychological research into interoceptive awareness has mainly used tasks that quantify our accuracy in detecting single heartbeats. However, as the influential work of Garfinkel, Seth, Barrett, Suzuki, and Critchley (2015) shows, we must be aware of the hierarchical levels of interoception, from interoceptive sensibility, to accuracy and eventual awareness, and how these may impact cognition in health and in illness. Similarly, in relation to horizontal relations, classic approaches to interoception focus on four systems—the cardiovascular, respiratory, gastrointestinal, and urogenital (Adam, 1998; Cameron, 2002), but a fundamental question concerns the interrelation of awareness across different interoceptive systems and the potentially distinctive role that each system plays for cognition. Finally, unlike exteroception, it is particularly difficult to have experimental control over the inputs to the interoceptive system and/or to interfere causally with it, and therefore developing paradigms and theoretical approaches that can probe the causal links between interoception and cognition will accelerate our knowledge.
The contributions collected in this multidisciplinary volume represent an attempt to provide a reference for the conceptualization of this excitingly deep connection between our body and mind. As such it offers an overview of the state-of-art in psychological and neuroscience research, of recent developments in clinical-psychological models for normal and pathological functioning, and of new theories that frame interoception at the intersection between philosophy of mind and the broader context of embodied cognition. To that end, its scope ranges from the psychology and neuroscience of interoception (Part I), to clinical implications of recent research taking into account interoception (Part II), and to theoretical-philosophical frameworks and models of interoception (Part III).
The introductory chapter by Berntson, Gianaros, and Tsakiris goes straight into the heart of the matter by providing the historical context that led to the development of a science of interoception and a state-of-the-art overview of the organizational principles of the interoceptive system. First, it is explained that the autonomic nervous system is not only or even primarily an efferent motor system (historically the predominant view) but constitutes an elaborate afferent system. Second, the authors explain that the interoceptive system does not operate independently of higher brain functions. By addressing the top-down and bottom-up organizational principles that underpin interoception, this introductory chapter sets the stage for the subsequent chapters in the volume.
Part I, Mentalizing interoception: Advances and challenges focuses on recent advances in experimental psychology and cognitive neuroscience that highlight the role that interoceptive signals and awareness thereof play for our mental life, beyond their known role for homeostasis. Allen and Tsakiris consider the implications of the embodied predictive processing account for the conceptualization of interoceptive signals as “first priors” and their role in providing the mind with a biologically plausible model of one’s body and self. Babo-Rebelo and Tallon-Baudry review recent electrophysiological studies that extend the role of interoception to show how the cortical processing of cardiac signals may generate a subject-centered reference frame that may underlie different and perhaps distinct facets of the self, such as thought generation and visual consciousness. Wittmann and Meissner discuss the embodiment of subjective time and present evidence to show how the accumulation of physiological signals forms the basis for the subjective impression of time. Aziz and Ruffle delve deeper into the viscera to describe the bi-directional brain−gut axis whose function underpins the generation of “gut-feelings.” Such feeling states are important for sensations but also the experience of distinct and often salient experiences such as pain, nausea, and appetite. The last chapter of this first part by Von Morh and Fotopoulou focuses on the homeostatically relevant experiences of pain and pleasure, in particular affective touch, and discuss their peripheral neurophysiological specificity (i.e. bottom-up) and their top-down social modulations within a predictive coding framework.
Part II: From health to disease: Interoception in physical and mental health considers the role of interoceptive processes and their corresponding psychological concepts across a range of clinical conditions, from aberrant emotional processing to anxiety, eating disorders, symptom perception and overall well-being. Recent experimental findings are presented and reviewed in the context of hypotheses about the integration of peripheral afferent signals with central cognitive operations and their role in shaping subjective experience in health and disease.
Quadt, Critchley, and Garfinkel provide an overview of the influence of internal bodily states on emotion. By presenting a predictive coding account of interoceptive predictions errors, they highlight the distinct ways in which deficits in interoceptive abilities may underpin aberrant emotional processes characteristic of several clinical conditions. Khalsa and Feinstein focus on the regulatory battle for control that ensues in the central nervous system when there is a discrepancy between predicted and current bodily states (i.e. when
somatic error signals are present). They argue that anxiety disorders are driven by somatic errors that chronically fail to be adaptively regulated. Herbert and Pollatos use a predictive coding framework analogous to the one introduced by Quadt, Critchley, and Garfinkel, and apply it to our understanding of eating behavior. They characterize anorexia and bulimia nervosa as a profound impairment of the “self,” with dysfunctional interoception at its core. Yoris and colleagues explore the interoceptive dysfunctions following neurological damage or neurodegeneration and emphasize the significance of interoception to promote a hitherto missing synthesis of simultaneous autonomic, emotional, and social cognition deficits in neurology. Van den Bergh, Zacharioudakis, and Petersen focus on interoception and the perception of bodily sensations in the context of symptom perception, and spell out the consequences of the highly variable relationship between symptoms and physiological dysfunction for the disease model. Farb and Logie focus on the appraisal of interoceptive signals and its consequences for subjective well-being. The modifying role of attention for habitual appraisals of interoceptive signals is presented, along with a novel breathing-focused task for measuring interoceptive awareness.
Part III Toward a philosophy of interoception: subjectivity and experience approaches interoception from a theoretical and philosophical perspective. Because until now the field of interoception has been driven mainly by scientists rather than philosophers, this part represents a highly novel departure for philosophy of mind and subjectivity, often starting from a phenomenological point of view. The relation between subjective experience and physiological processes is an intricate and complicated one. Both the notion of “arousal” in emotion and the experiential dimension of interoception more generally stand in need of descriptive analysis and theoretical framing.
Colombetti and Harrison disentangle the physiology and the experience of “arousal” in emotion and argue for the recognition of the multiple systems and pathways involved in emotional arousal, including not only the autonomic nervous system but also pathways of the endocrine and immune system, somatic sensations, and “background” bodily feelings. Empirical studies in interoception have profound consequences for the way the self or subjectivity is conceived of and conceptualized. The interoceptive dimension of the embodied subject forces us to rethink phenomena such as body ownership and the self, the relation between interoception and exteroception, and the coming about of subjectivity itself. De Vignemont discusses the many ways the notion of interoception is understood, and considers the contribution of interoception for the awareness of one’s body as one’s own. She approaches body ownership in affective terms and as rooted in self-regulatory interoceptive feelings such as hunger and thirst. Corcoran and Hohwy consider the limitations of homeostasis and favor a reconciliatory position in which homeostasis and allostasis are conceived as equally vital but functionally distinct modes of physiological control to account for the sophisticated regulatory dynamics observed in complex organisms. De Preester focuses on a basis form of subjectivity and its origin in interoceptive processes. She argues that the topographic representation of interoceptive body states in the brain is unfit for explaining the coming about of subjectivity, and offers
directions for another model that takes into account the inherent characteristics of subjectivity. Leder closes the volume, offering a phenomenology of inner-body experience and explaining how this experience is influenced by models drawn from the outer world. In line with insights gained in the first and the second part, he points out the importance of inner-body experience for health and well-being.
The different chapters included across the three parts are interrelated in various ways, and the synergy between the chapters crosses the boundaries of the disciplines, opening up opportunities for fruitful dialog between fields that otherwise remain too often separate. For example, attention to subjectivity and subjective experience, to selfawareness and the experience of self, are common threads throughout the volume, together with the intricate role of emotions and their relation to interoception. Similarly, several chapters are motivated by recent predictive coding accounts (Clark, 2013; Friston, 2010) that have been extended from cognition and attention to affect (Critchley & Garfinkel, 2017), bodily self-awareness (Apps & Tsakiris, 2014; Seth, 2013), and mental disorders (Feldman Barrett & Simmons, 2015). A concern for human wellbeing and human health and suffering is also noticeable in all the chapters, and the capacity to contribute to one’s own well-being by paying attention to in-depth bodily signals is a recurrent theme. The chapters thus share a common concern for what it means to experience oneself, for the crucial role of emotions, and for issues of health and well-being, discussed on the joint basis of our bodily existence and interoception, resulting in a more than usual attention for the phenomenology of subjective experience in disciplines outside philosophy. Together, the chapters show that disciplinary specialization is not a hindrance for dialogue but can result into mutual enrichment. We hope that the scholarly research presented in this volume will further motivate the much-anticipated coming of age of interoceptive research in psychology, cognitive neurosciences, and philosophy.
Helena De Preester Manos Tsakiris
References
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Garfinkel, S. N., Seth, A. K., Barrett, A. B., Suzuki, K., and Critchley, H. D. (2015). Knowing your own heart: Distinguishing interoceptive accuracy from interoceptive awareness. Biological Psychology, 104, 65–74. <https://doi.org/10.1016/j.biopsycho.2014.11.004>
Haggard, P. (2005). Conscious intention and motor cognition. Trends in Cognitive Sciences, 9(6), 290–5. <https://doi.org/10.1016/j.tics.2005.04.012>
Kleckner, I. R., Wormwood, J. B., Simmons, W. K., Barrett, L. F., and Quigley, K. S. (2015). Methodological recommendations for a heartbeat detection-based measure of interoceptive sensitivity. Psychophysiology, 52, 1432–40. <https://doi.org/10.1111/psyp.12503>
Seth, A. K. (2013). Interoceptive inference, emotion, and the embodied self. Trends in Cognitive Sciences, 17(11), 565–73. <https://doi.org/10.1016/j.tics.2013.09.007>
Tsakiris, M. (2010). My body in the brain: A neurocognitive model of body-ownership. Neuropsychologia, 48(3), 703–12. <https://doi.org/10.1016/j.neuropsychologia.2009.09.034>
Acknowledgments
We would like to thank our colleague and friend Ophelia Deroy who introduced us to Martin Baum, Senior Commissioning Editor for Psychology and Neuroscience at Oxford University Press. We are grateful to Martin for supporting and selecting our proposal for this volume among the many high-quality proposals that OUP receives. We are also grateful to April Peake for her assistance during the early stages of preparation and to Charlotte Holloway for her assistance during the final production stages. We would also like to acknowledge the NOMIS Foundation Distinguished Scientist Award to Manos Tsakiris and a research grant from the University College Ghent to Helena De Preester that provided the editors with the time and space of mind needed for the timely development of this volume.
Of course, this volume wouldn’t exist without the excellent and timely contributions made by all the authors who fully engaged with our vision for this volume and its multiand cross-disciplinary emphasis. We also thank the authors for acting as referees for each other’s chapters along with Vivien Ainley, Laura Crucianelli, Chris Dijkerman, Karl Friston, Philip Gerains, Rebekka Hufendiek, Peter Reynaert, Roy Salomon, Stefan Sütterlin, and Dan Zahavi who generously devoted their precious time in reviewing several chapters.
Last, but not least, the co-editors would like to thank each other for a seamless mutually enriching and supportive collaboration over the last two years.
List of Contributors xv
Part I Introduction
1 Interoception and the autonomic nervous system: Bottom-up meets top-down 3
Gary G. Berntson, Peter J. Gianaros, and Manos Tsakiris
Part II Mentalizing interoception: Advances and challenges
2 The body as first prior: Interoceptive predictive processing and the primacy of self-models 27
Micah Allen and Manos Tsakiris
3 Interoceptive signals, brain dynamics, and subjectivity 46
Mariana Babo-Rebelo and Catherine Tallon-Baudry
4 The embodiment of time: How interoception shapes the perception of time 63
Marc Wittmann and Karin Meissner
5 The neurobiology of gut feelings 80
Qasim Aziz and James K. Ruffle
6 The cutaneous borders of interoception: Active and social inference of pain and pleasure on the skin 102
Mariana von Mohr and Aikaterini Fotopoulou
Part III From health to disease: Interoception in physical and mental health
7 Interoception and emotion: Shared mechanisms and clinical implications 123
Lisa Quadt, Hugo D. Critchley, and Sarah N. Garfinkel
8 The somatic error hypothesis of anxiety 144
Sahib S. Khalsa and Justin S. Feinstein
9 The relevance of interoception for eating behavior and eating disorders 165
Beate M. Herbert and Olga Pollatos
10 Cardiac interoception in neurological conditions and its relevance for dimensional approaches 187
Adrián Yoris, Adolfo M. García, Paula Celeste Salamone, Lucas Sedeño, Indira García-Cordero, and Agustín Ibáñez
11 Interoception, categorization, and symptom perception 212
Omer Van den Bergh, Nadia Zacharioudakis, and Sibylle Petersen
12 Interoceptive appraisal and mental health 227
Norman A. S. Farb and Kyle Logie
Part IV Toward a philosophy of interoception:
Subjectivity and experience
13 From physiology to experience: Enriching existing conceptions of “arousal” in affective science 245
Giovanna Colombetti and Neil Harrison
14 Was Descartes right after all? An affective background for bodily awareness 259
Frédérique de Vignemont
15 Allostasis, interoception, and the free energy principle: Feeling our way forward 272
Andrew W. Corcoran and Jakob Hohwy
16 Subjectivity as a sentient perspective and the role of interoception 293
Helena De Preester
17 Inside insights: A phenomenology of interoception 307
Drew Leder
Author Index 323
Subject Index 333
Contributors
Micah Allen
Institute of Cognitive Neuroscience, University College London, United Kingdom
Wellcome Centre for Human Neuroimaging, University College London, United Kingdom
Qasim Aziz
Barts and the London School of Medicine & Dentistry, Queen Mary University of London, United Kingdom
Mariana Babo-Rebelo
Laboratoire de Neurosciences Cognitives, Département d’Etudes Cognitives, Ecole Normale Supérieure (ENS), PSL Research University, INSERM, Paris, France
Gary G. Berntson
Department of Psychology, Ohio State University, United States
Giovanna Colombetti
Department of Sociology, Philosophy and Anthropology, University of Exeter, United Kingdom
Andrew W. Corcoran
Cognition & Philosophy Laboratory, Department of Philosophy, Faculty of Arts, Monash University, Melbourne, Australia
Hugo D. Critchley
Department of Neuroscience, Brighton and Sussex Medical School (BSMS), University of Sussex, Brighton, United Kingdom
Helena De Preester
School of Arts, University College Ghent, Belgium
Department of Philosophy and Moral Sciences, Faculty of Arts and Philosophy, Ghent University, Belgium
Frédérique de Vignemont
Institut Jean Nicod, ENS-CNRS-EHESS, Department of cognitive studies, École Normale Supérieure, PSL, Paris, France
Norman A. S. Farb
Department of Psychology, University of Toronto Mississauga, Mississauga, Canada
Justin S. Feinstein
Laureate Institute for Brain Research, Tulsa, Oklahoma, United States Oxley College of Health Sciences, University of Tulsa, Tulsa, Oklahoma, United States
Aikaterini Fotopoulou
Research Department of Clinical, Educational and Health Psychology, Faculty of Brain Sciences, University College London, United Kingdom
Adolfo M. García
Laboratory of Experimental Psychology and Neuroscience (LPEN), Institute of Cognitive and Translational Neuroscience (INCYT), INECO Foundation, Favaloro University, Buenos Aires, Argentina
National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina
Faculty of Education, National University of Cuyo (UNCuyo), Mendoza, Argentina
Indira García-Cordero
Laboratory of Experimental Psychology and Neuroscience (LPEN), Institute of Cognitive and Translational Neuroscience (INCYT), INECO Foundation, Favaloro University, Buenos Aires, Argentina
National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina
Sarah N. Garfinkel
Psychiatry, Department of Neuroscience, Brighton and Sussex Medical School (BSMS), University of Sussex, Brighton, United Kingdom
Sackler Centre for Consciousness Science, University of Sussex, Brighton, United Kingdom
Sussex Partnership NHS Foundation Trust, United Kingdom
Peter J. Gianaros
Department of Psychology, University of Pittsburgh, United States
Neil Harrison
Department of Neuroscience, Brighton & Sussex Medical School, University of Sussex, United Kingdom
Sussex Partnership NHS Foundation Trust, Swandean, United Kingdom
Beate M. Herbert
Clinical Psychology & Psychotherapy, Department of Psychology, Eberhard
Karls University of Tübingen, Germany
Jakob Hohwy
Cognition & Philosophy Laboratory, Department of Philosophy, Faculty of Arts, Monash University, Melbourne, Australia
Agustín Ibáñez
Laboratory of Experimental Psychology and Neuroscience (LPEN), Institute of Cognitive and Translational Neuroscience (INCYT), INECO Foundation, Favaloro University, Buenos Aires, Argentina
National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina
Universidad Autónoma del Caribe, Barranquilla, Colombia
Center for Social and Cognitive Neuroscience (CSCN), School of Psychology, Universidad Adolfo Ibañez, Santiago, Chile
Centre of Excellence in Cognition and its Disorders, Australian Research Council (ACR), Sydney, Australia
Sahib S. Khalsa
Laureate Institute for Brain Research, Tulsa, Oklahoma, United States
Oxley College of Health Sciences, University of Tulsa, Tulsa, Oklahoma, United States
Drew Leder
Department of Philosophy, Loyola University Maryland, Baltimore, United States
Kyle Logie
Department of Psychology, University of Toronto Mississauga, Mississauga, Canada
Karin Meissner
Institute of Medical Psychology, LudwigMaximilian University, Munich, Germany
Division Integrative Health Promotion, University of Applied Sciences, Coburg, Germany
Sibylle Petersen
Health Psychology, KU Leuven–University of Leuven, Leuven, Belgium
Olga Pollatos
Clinical & Health Psychology, Institute of Psychology and Education, Ulm University, Germany
Lisa Quadt
Psychiatry, Department of Neuroscience, Brighton and Sussex Medical School (BSMS), University of Sussex, Brighton, United Kingdom
James K. Ruffle
Centre for Neuroscience and Trauma, Blizard Institute, Wingate Institute of Neurogastroenterology, Barts and the London School of Medicine & Dentistry, Queen Mary University of London, London, United Kingdom
Paula Celeste Salamone
Laboratory of Experimental Psychology and Neuroscience (LPEN), Institute of Cognitive and Translational Neuroscience (INCYT), INECO Foundation, Favaloro University, Buenos Aires, Argentina
National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina
Lucas Sedeño
Laboratory of Experimental Psychology and Neuroscience (LPEN), Institute of Cognitive and Translational Neuroscience (INCYT), INECO Foundation, Favaloro University, Buenos Aires, Argentina
National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina
Catherine Tallon-Baudry
Laboratoire de Neurosciences Cognitives, Département d’Etudes Cognitives, Ecole Normale Supérieure (ENS), PSL Research University, INSERM, Paris, France
Manos Tsakiris
Lab of Action & Body, Department of Psychology, Royal Holloway University of London, United Kingdom
The Warburg Institute, School of Advanced Study, University of London, United Kingdom
Omer Van den Bergh
Health Psychology, KU Leuven–University of Leuven, Leuven, Belgium
Mariana von Mohr
Research Department of Clinical, Educational and Health Psychology, Faculty of Brain Sciences, University College London, United Kingdom
Marc Wittmann
Institute for Frontier Areas of Psychology and Mental Health, Freiburg, Germany Institute of Medical Psychology, LudwigMaximilian University, Munich, Germany
Adrián Yoris
Laboratory of Experimental Psychology and Neuroscience (LPEN), Institute of Cognitive and Translational Neuroscience (INCYT), INECO Foundation, Favaloro University, Buenos Aires, Argentina
National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina
Nadia Zacharioudakis
Health Psychology, KU Leuven–University of Leuven, Leuven, Belgium
ParT I Introduction
chapter 1
Interoception and the autonomic nervous system: Bottom-up meets top-down
Gary G. berntson, Peter J. Gianaros, and Manos Tsakiris
1.1 Introduction
Interoception is a multidimensional construct, broadly encompassing the processing of afferent (sensory) information arising from internal organs, tissues, and cells of the body. This afference contributes to the regulation of homeostatic reflexes, and, as we will see in this chapter and throughout this volume, more broadly to the generation and regulation of cognitive and emotional behaviors.
Interoception can be encompassed by the broader construct of bodily afference. The latter includes both visceral afference and somatic afference. We use the term visceral afference to refer to the processing of internal sensory information derived from interoceptors that are located in the organs and tissues of the main cavities of the body (i.e. the viscera), as well as from olfactory and gustatory receptors, all being generally associated with the limbic system and the autonomic nervous system. We use the term somatic afference to refer to the processing of sensory information (e.g. proprioceptive input and tactile sensitivity) derived from components of the somatic system (e.g. muscles, joints, skin). This distinction between somatic and visceral afference does not imply a complete independence. Indeed, in many cases, there is an integration of multiple modes of bodily or somatosensory information derived, for example, from metabolic changes in active muscle tissue. Hence, the term somatovisceral afference is more appropriately applied to integrated, multimodal, or otherwise nonspecific internal sensory input from within the body (e.g. see Yates & Stocker, 1998). In these regards, the construct of interoception itself is more specifically aligned with that of visceral afference, referring to the processing of sensory information from interoceptors that are located within the visceral organs and from interoceptors located elsewhere in the body that provide for local energy needs. Thus, in contrast to exteroceptors, interoceptors are tuned to sense internal events (Cameron, 2002).
The so-called general visceral afferents (GVAs) that relay internal sensory information from interoceptors are carried by several cranial nerves, the most notable being the vagus
nerve. These afferents carry information (e.g. pressor receptor activity from blood vessels) originating from the gut and the viscera more generally (i.e. organs and tissues located in the thoracic, abdominal, and pelvic cavities, as well as blood vessels and muscles). By comparison, special visceral afferents (SVAs) convey gustatory senses (i.e. taste) and olfaction (i.e. smell and pheromonal senses). Although the SVAs detect environmental stimuli, they do so by virtue of those stimuli impinging on the internal bodily environment. Hence, they differ from exteroceptors; for example, conveying information related to touch or audition. Furthermore, the visceral senses have common central projections to cell groups in the brainstem, including the nucleus tractus solitarius (NTS), midbrain, and thalamus, that are distinct from those of somatic exteroceptors, and they link anatomically and functionally with a distinct set of central neural systems and processes (Craig, 2014; Saper, 2002). Moreover, they share biochemical markers in common with GVAs and with autonomic neurons (see Squire et al., 2012). There are other classes of sensory systems, such as proprioceptors, that sense joint position, and vestibuloceptors, that sense body orientation in gravitational space. These might be considered interoceptors as they are internal to the body. Yet, they are closely linked with somatic motor systems anatomically and functionally, and they have biochemical markers more in concert with somatic motor systems. Hence, they are sometimes considered within the unique class of proprioceptors, or otherwise just included within the general class of exteroceptors. What is important to consider is that both exteroceptive and interoceptive information can powerfully influence cognitive and emotional processes, and, importantly, vice versa. Moreover, as will be developed later in this chapter, visceral afferents carrying interoceptive information have a constitutional link with central neural systems underlying cognitive and emotional processes, and they thus impact these behavioral processes (e.g. Tsakiris & Critchley, 2016a; see also the entire Theme issue, Tsakiris & Critchley, 2016b). This is clearly apparent in the positive and negative (e.g. disgust) hedonic effects of tastes and smells. As detailed in the remaining chapters of this volume, it is thus doubtful that interoception can be meaningfully parsed or dissociated from cognitive, emotional, and behavioral processes. Indeed, a recent meta-analysis of fMRI (functional MRI) studies revealed considerable overlap in systems co-activated by interoceptive signaling, emotional regulation and low-level social cognition, and convergent results were found for the effects of lesions (Adolfi et al., 2017).
1.2 Historical perspectives
Claude Bernard is generally credited with developing the concept of the “fixity” or relative stability of the internal fluid matrix (milieu intérieur) as a necessary condition for what he termed the free and independent life (Bernard, 1878). Walter Cannon, chair of the Department of Physiology at Harvard around the turn of the twentieth century, further elaborated on this concept and coined the term homeostasis (Cannon, 1932/ 1939). He believed that the autonomic nervous system (ANS) plays an important part in maintaining this homeostatic stability. Although Cannon recognized the importance of visceral afferents in homeostatic reflexes, the predominant view of the ANS was as an
efferent, lower-level, reflexive motor system. Cannon further asserted that the ANS is termed “ ‘autonomic’ because it acts automatically, without direction from the cerebral cortex” (Cannon, 1939, p. 250). This misconception was perhaps understandable, as it would be another half century before the existence of direct, monosynaptic projections from cortical and other telencephalic areas to lower brainstem autonomic source nuclei and reflex substrates would be documented (e.g. Barbas et al., 2003; Cechetto & Saper, 1990; Dum, Levinthal, & Strick, 2016; Neafsey, 1990).
In retrospect, this misconception is also somewhat surprising in view of the work of Cannon’s friend, contemporary, and Nobel Laureate, Ivan Pavlov (see Figure 1.1). Here, it is often underappreciated that much of Pavlov’s work on learning centered on the modification of an autonomic and homeostatic reflex that involves the processing of interoceptive information in preparation for digestion—the cephalic vagal reflex, or the cephalic phase insulin release to a stimulus which had previously been paired with food. Indeed, this work contributed to a foundation for understanding how interoceptive phenomena can be powerfully related to learning and other processes instantiated in higher brain systems that can jointly influence visceral control, including systems within the cerebral cortex. This includes experience-based acquired responses that can both modulate
Figure 1.1 Walter b cannon with Ivan Pavlov at the 1929 International Physiological congress. Photograph reproduced with the acquiescence of the curator (Harvard Medical library in the francis a countway library of Medicine).
ongoing visceral processes as well as anticipate and prospectively guide adaptive autonomic, cognitive, and emotional responses (Cameron, 2002; Dworkin, 1993).
Well before the existence of long descending pathways linking brain and viscera had been established, functional studies revealed autonomic representations in multiple higherlevel diencephalic and telencephalic areas of the forebrain. The 1949 Nobel Laureate, Walter Hess, for example, had reported striking autonomic responses elicited by stimulation of telencephalic (e.g. the amygdala and septal area) and diencephalic structures, including the hypothalamus, which Hess considered the head-ganglion of the autonomic nervous system (Hess, 1954; see also Ranson, Kabat, & Magoun, 1935). The Canadian neurosurgeon, Wilder Penfield, also reported autonomic responses to cortical stimulation in conscious human patients (Penfield & Jasper, 1954). At this point, we recognize a broad central autonomic network comprising a number of forebrain areas, including the insular cortex, cingulate cortex, medial prefrontal cortex, amygdala, and hippocampus, as well as caudal cell groups in the midbrain periaqueductal gray, pons, cerebellum, and medulla (Benarroch, 1993; Cechetto & Saper, 1990; Critchley, 2005; Dampney, 2015; Loewy, 1991; Neafsey, 1990; Saper, 2002; Shoemaker & Goswami, 2015). This network highly overlaps and interacts with systems implicated in complex cognitive, skeletomotor, and affective processes (Annoni et al., 2003; Critchley, 2005; Myers, 2017; Saper, 2002).
Another legacy from the Cannon era that did not survive the test of time is the view that the ANS is primarily an efferent motor system, with minimal visceral afferents necessary to support homeostatic reflex functions. In his influential book, The Wisdom of the Body, Cannon stated: “The nerve fibers of the autonomic nervous system, which are mostly efferent, pass out of the central nervous system” (Cannon, 1939, p. 252). Similarly, John Newton Langley, who coined the term autonomic nervous system1 (Langley, 1898) viewed the ANS largely as a motor system, although he recognized that one might “consider as afferent autonomic fibers those which give rise to reflexes in autonomic tissues . . . [but are] . . . incapable of directly giving rise to sensation” (Langley, 1903, p. 2). As early as the mid-1930s, however, there were quantitative studies demonstrating that the majority of fibers in the vagus are sensory (Foley & DuBois, 1937; Heinbecker & O’Leary, 1933). This is consistent with contemporary estimates that 70–90% of vagal fibers, about 2–20% of fibers in the splanchnic (sympathetic) nerves, and about 2% in spinal nerves are visceral afferents2 (Berthoud & Neuhuber, 2000; Cameron, 2002; Jänig & Morrison, 1986).
Historically, there were also notable conceptual challenges to the notion that the ANS is primarily a motor system. In contrast to the view that emotions precede and trigger bodily reactions, William James (1884) proposed that exciting events induce bodily
1 “We propose the term ‘autonomic nervous system,’ for the sympathetic system and the allied nervous system of the cranial and sacral nerves, and for the local nervous system of the gut” (p. 270).
2 Although some of these afferents run with parasympathetic and sympathetic efferents, it is not appropriate to consider them “parasympathetic” and “sympathetic” afferents (Freire-Maia & Azevedo,1990; Jänig & Häbler, 1995). They are general visceral afferents that are not strictly coupled to an autonomic branch.
changes (including autonomic responses) and that our subsequent feeling of these changes constitutes the emotion. Shortly thereafter, Carl Lange (1885) independently proposed a vascular theory of emotion, which held that vasomotor responses are the primary effects of affectations, and subjective sensations of emotion arise secondarily. Both of these perspectives converged into a view of visceral afference as fundamental for the generation and experience of emotion.
This view came under severe assault from two notable figures: Walter Cannon (1927, 1931), often considered the “father of the autonomic nervous system” and Sir Charles Sherrington (1900)—a notable turn-of-the-century physiologist and a recipient of the Nobel Prize in Physiology or Medicine (1932) for “discoveries regarding the functions of neurons.” At least the strong form of the James–Lange concept (emotions as the mere perception of visceral feedback) was largely discredited at that time. There were a number of arguments against the James–Lange perspective. Cannon, for example, argued that the viscera have few afferents and are relatively insensate. However, it is now recognized that visceral afferents in fact outnumber efferents. Additionally, it was argued that (a) visceral responses are too slow to underlie emotion; (b) similar visceral changes may occur across different emotions and even non-emotional states; (c) inducing autonomic responses does not necessarily invoke emotions; and (d) that autonomic denervations of various types do not prevent emotional reactions. None of those are particularly telling arguments unless one wants to assert an identity relationship between visceral afference and emotion. James (1884), in fact, viewed emotions as being multiply determined, and to include cognitive contributions. He stipulated in his 1884 article that the only emotions that he will “consider here are those that have a distinct bodily expression” (p. 189)—the so-called coarser emotions. It is well established that there are multi-level hierarchical and heterarchical representations in neurobehavioral systems and central autonomic networks (see Berntson, Cacioppo, & Bosch, 2016; Norman, Berntson, & Cacioppo, 2014), and there are multiple determinants of affective processes. What will become apparent through the chapters of this volume is that there are powerful interactions between cognitive and emotional processes, somatic and autonomic outflows, and interoceptive feedback. Consequently, the effects of interoceptive feedback would not be expected to be invariant but to show notable brain-state and context dependencies (e.g. see Cacioppo, Berntson, & Klein, 1992).
1.3 A case report
Visceral afference can powerfully modulate cognitive and emotional processes, as illustrated by the following case report on MM (personal communication). MM is a graphic artist and videographer who was working on a documentary about a historical kidnapping and murder. She had extensively researched and documented the story and had located and interviewed most of the characters involved (except for the perpetrator, who had killed himself). The story was ready for filming (January 2007), but, alas, filming never happened: I handed the story back to the producer when it became clear that I could not work the script (kept repeating the same scenes), as I was able to keep it all in my head for only about 3 pages—few
minutes, and no amount of colour coordinated storylines and Post-It notes were going to save me when I was not able to make a simple decision on spot (calculating what days we had available for shooting whom . . . etc.).
What led to this transformation (February 2007)? It was endoscopic thoracic sympathectomy (ETS), the surgical destruction or disabling of the upper spinal sympathetic (autonomic) nerve trunk, for hyperhidrosis (excessive sweating). Thereafter, MM’s life (she was 39 years old at the time) was dramatically changed3:
It is my experience that following this surgery there is a shift in personality and how emotions are experienced. It is, however, not only emotional blunting but also an impaired impulse control and disinhibition (as if a grown-up brain has been replaced by a primitive, and at times manic brain, that affects higher functioning). I am not sure how to describe it really . . . There is an indifference and striking lack of fear . . . I witnessed within myself once I got into my car and started driving around, or in general danger situations any urbanite encounters. My emotions are blunted, and there is an unsettling deadness and indifference towards my prior life and aspirations, goals. This indifference and emotional blunting was present as soon as I woke up from the surgery and has not left me since.
In general, the procedure led to a personality change, in some aspects subtle, in others a profound shift that I find exceedingly difficult to accept—a kind of physiological expression of how I was feeling, zombie-like.
I was described by one (video) critic as a human seismograph, recording the finest shifts in mood/ tone . . . (now) I have problems in social settings, where I generally might appear antisocial. I force myself to ask questions and engage in “banter”, but more often I forget. I would say that it has changed how I relate to people: I do not relate.
Tragically, this outcome was not unique to MM. There is a considerable literature documenting a range of post-sympathectomy complications including cognitive deficits, altered mood, emotional blunting, fatigue, and neuropathic complications (e.g. Furlan, Mailis, & Papagapious, 2000; Goldstein, 2012; Mailis & Furlan, 2003). Indeed, a support group, the Sympathetic Association (FfSo), was formed in Karlstad, Sweden, by people who found themselves disabled by serious side effects of sympathectomies (<http://home.swipnet.se/sympatiska/index3.htm>). We will return to the case of MM in section 1.4.2.
1.4 Central visceral pathways and the visceral cortex
An important integrative site in the forebrain for visceral afference is the insular cortex, which could be considered a primary visceral cortical site. The insula, in turn, is highly interconnected with cortical and subcortical areas involved in cognition, emotion, and
3 There was no pre-surgical history of psychopathology. The patient elected the procedure to reduce excessive sweating, and to some extent, this was achieved. However, as is common with ETS (Furlan et al., 2000), she did experience periodic “compensatory” sweating.
motivation, including the prefrontal cortex, the cingulate cortex, and the amygdala (Allen et al., 1991; Augustine, 1996; Nieuwenhuys, 2012; Oppenheimer & Cechetto, 2016). The insula receives input from all visceral afference and, as will be seen throughout this volume, contributes to the integration of this afference with neurobehavioral processes (Tsakiris & Critchley, 2016a), and anomalies in insular function are associated with a wide range of cognitive, emotional, and behavioral disturbances (Gasquoine, 2014).
1.4.1 Special visceral afferents: The chemical senses—Olfaction and gustation
Olfaction is a special visceral sense closely linked with both positive and negative hedonics. This is especially true in lower animals where it plays a central role in guiding behavior. The olfactory system is closely linked with a medial central brain network that was historically referred to as the rhinencephalon (nose brain). Paul Broca (1878) referred to the medial central components of the brain as the great limbic lobe (le grand lobe limbique) because they arch around the central encephalon (“limbique” in French translates as “hoop” or “curve”). Papez (1937) proposed that limbic areas and associated structures are an important central network in emotion (often referred to as Papez circuit). This concept was further developed by Paul MacLean (1954) who coined the term “limbic system” and viewed this system as an evolutionary heritage (the paleomammalian brain) that regulates emotion, motivation, and survival-related behaviors, as well as links these phenomena with vulnerability to chronic health conditions (e.g. hypertension, asthma). Olfactory afferents play an important role in emotion, motivation, and survivalrelated behavioral processes. Although the olfactory system more directly projects to a number of cortical areas, olfactory information is also relayed via the thalamus and other cortical areas to the insular cortex (which itself is often considered to be a part of the limbic system). Odors can modulate mood, cognition, and behavior, and many of these effects appear to be mediated by the insula (for reviews see Miranda, 2012; Saive, Royet, & Plailly, 2014; Soudry et al., 2011).
The primary gustatory cortex lies in the anterior insula. Gustatory afferents (cranial nerves VII, IX, and X) terminate in a medullary nucleus, the NTS, and then are relayed via the midbrain parabrachial nucleus to the ventroposteromedial thalamus, which issues direct projections to the anterior insula (Saper, 2002). A similar functional pattern emerges in the literature to that of olfaction (Rolls, 2015). There are potent insular contributions to the processing of taste hedonics and attentional and memorial processes associated with taste, and insular cortex abnormalities are associated with disturbances in these processes (Frank, Kullmann, & Veit, 2013; Maffei, Haley, & Fontanini, 2012).
1.4.2
General visceral afferents
As is the case with gustatory afferents, all GVAs in cranial nerves project to the NTS in the brainstem, to the parabrachial nucleus in the midbrain, and then via the ventroposteromedial (VPM) nucleus of the thalamus to the insular cortex. In his classic studies, Wilder Penfield reported that electrical stimulation of the insula induced a
variety of visceral sensory experiences (Penfield & Jasper, 1954; Penfield & Faulk, 1955). In addition to cranial nerves, GVAs carrying nociceptive, temperature, and chemosensory information from the body enter the spinal cord via dorsal spinal roots and terminate in the dorsal horn (especially in lamina I). Until around the turn of the twenty-first century, the general belief was that small-diameter nociceptive (i.e. sensory information about tissue damage)/temperature afferents were part of the somatosensory system and were ultimately relayed to the somatosensory cortex in the parietal lobe. Indeed, this view persists. In their 2016 textbook on neuroscience, Bear, Connors, and Paradiso assert that the “spinothalamic pathway is the major route by which pain and temperature information ascend to the cerebral cortex” (2016, p. 444). In fact, it is now well established that the small diameter fibers carrying nociceptive, temperature, and chemical senses project from the VPM not to the somatosensory cortex but to the insula (Craig, 2014; Saper, 2002). This accounts for the fact that in Wilder Penfield’s studies, patients never reported pain on stimulation of the somatosensory cortex (Penfield & Jasper, 1954; Penfield & Faulk; 1955). Moreover, surgeons do not extirpate the somatosensory cortex for pain syndromes. In contrast, however, Mazzola and colleagues (2012) report induced pain with stimulation of the insular cortex, and painful “somatosensory” seizures appear to arise not from the somatosensory cortex but from the opercular-insular cortex (Montavont et al., 2015).
This general visceral afference, and the top-down and bottom-up integration of insular cortical systems, underlie the cognitive-emotional processes that reflect the broad integrative contributions of the insula (Tsakiris & Critchley, 2016a). Insula lesions, for example, result in diminished emotional arousal to affective pictures, and a reduced ability to even recognize the affective picture content (Berntson et al., 2011). Although the literature on insular involvement in emotion and emotional processing is quite consistent (Uddin, Nomi, & Hébert-Seropian, 2017), there appears to be some diversity in the effects of insular lesions.4 In addition to its role in emotion and motivation, the insula appears to play a pivotal role in the sense of self, agency, and indeed, consciousness (Craig, 2014; Strigo & Craig, 2016; Tsakiris & Critchley, 2016a, b; see also Chapters 2, 3, and 16 in the present volume). Thus, insula activation is correlated with the sense of body ownership and agency (Farrer, Franck, & Georgieff, 2003; Tsakiris et al., 2007). In accord, lesions of the insula can lead to a disturbed sense of body ownership, including somatoparaphrenia or the denial of body ownership (Cogliano et al., 2012; Gandola et al., 2012; Karnath & Baier, 2010; Moro et al., 2016).
These findings and further results addressed in the present volume indicate that visceral afferent input to the insula appears to be critical in cognitive and emotional processes.
4 Garcia and colleagues (2016) report minimal cognitive or socio-emotional deficits in a single case report after extensive vascular lesion damage, including the insular cortex. The authors, however, emphasize how unusual this case was as there were also minimal disturbances in sensorimotor and other functions. The literature on disgust, especially, is quite variable, but Uddin and colleagues (2017) report consistent socio-emotional deficits with insular lesions, but they also emphasize the considerable functional heterogeneity in this brain region.
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Who came at length, with proud presumpteous[390] gate, xiv
Into the field, as if he fearelesse were, All armed in a cote of yron plate, Of great defence to ward the deadly feare, And on his head a steele cap he did weare Of colour rustie browne, but sure and strong; And in his hand an huge Polaxe did beare, Whose steale[391] was yron studded, but not long, With which he wont to fight, to iustifie his wrong.
Of stature huge and hideous he was, xv
Like to a Giant for his monstrous hight, And did in strength most sorts of men surpas, Ne euer any found his match in might; Thereto he had great skill in single fight: His face was vgly, and his countenance sterne, That could haue frayd one with the very sight, And gaped like a gulfe, when he did gerne, That whether man or monster one could scarse discerne.
Soone as he did within the listes appeare, xvi
With dreadfull looke he Artegall beheld, As if he would haue daunted him with feare, And grinning griesly, did against him weld His deadly weapon, which in hand he held. But th’Elfin swayne, that oft had seene like sight, Was with his ghastly count’nance nothing queld, But gan him streight to buckle to the fight, And cast his shield about, to be in readie plight.
The trompets sound, and they together goe, xvii
With dreadfull terror, and with fell intent; And their huge strokes full daungerously bestow, To doe most dammage, where as most they ment. But with such[392] force and furie violent, The tyrant thundred his thicke blowes so fast, That through the yron walles their way they rent,
And euen to the vitall parts they past, Ne ought could them endure, but all they cleft or brast.
Which cruell outrage when as Artegall xviii
Did well auize, thenceforth with warie heed
He shund his strokes, where euer they did fall, And way did giue vnto their gracelesse speed: As when a skilfull Marriner doth reed
A storme approching, that doth perill threat, He will not bide the daunger of such dread. But strikes his sayles, and vereth his mainsheat, And lends vnto it leaue the emptie ayre to beat.
So did the Faerie knight himselfe abeare, xix
And stouped oft his head from shame to shield; No shame to stoupe, ones head more high to reare, And much to gaine, a litle for to yield; So stoutest knights doen oftentimes in field. But still the tyrant sternely at him layd, And did his yron axe so nimbly wield, That many wounds into his flesh it made, And with his burdenous blowes him sore did ouerlade.
Yet when as fit aduantage he did spy, xx
The whiles the cursed felon high did reare
His cruell hand, to smite him mortally, Vnder his stroke he to him stepping neare, Right in the flanke him strooke with deadly dreare, That the gore bloud thence gushing grieuously, Did vnderneath him like a pond appeare, And all his armour did with purple dye; Thereat he brayed loud, and yelled dreadfully.
Yet the huge stroke, which he before intended, xxi
Kept on his course, as he did it direct, And with such monstrous poise adowne descended, That seemed nought could him from death protect: But he it well did ward with wise respect,
And twixt him and the blow his shield did cast, Which thereon seizing, tooke no great effect, But byting deepe therein did sticke so fast, That by no meanes it backe againe he forth could wrast.
Long while he tug’d and stroue, to get it out, xxii And all his powre applyed thereunto, That he therewith the knight drew all about: Nathlesse, for all that euer he could doe, His axe he could not from his shield vndoe. Which Artegall perceiuing, strooke no more, But loosing soone his shield, did it forgoe, And whiles he combred was therewith so sore, He gan at him let driue more fiercely then afore.
So well he him pursew’d, that at the last, xxiii He stroke[393] him with Chrysaor on the hed, That with the souse thereof full sore aghast, He staggered to and fro in doubtfull sted. Againe whiles he him saw so ill bested, He did him smite with all his might and maine, That falling on his mother earth he fed: Whom when he saw prostrated on the plaine, He lightly reft his head, to ease him of his paine.
Which when the people round about him saw, xxiv They shouted all for ioy of his successe, Glad to be quit from that proud Tyrants awe, Which with strong powre did them long time oppresse; And running all with greedie ioyfulnesse To faire Irena, at her feet did fall, And her adored with due humblenesse, As their true Liege and Princesse naturall; And eke her champions glorie sounded ouer all.
Who streight her leading with meete maiestie xxv Vnto the pallace, where their kings did rayne,
Did her therein establish peaceablie, And to her kingdomes seat restore agayne; And all such persons, as did late maintayne
That Tyrants part, with close or open ayde, He sorely punished with heauie payne; That in short space, whiles there with her he stayd, Not one was left, that durst her once haue disobayd.
During which time, that he did there remaine, xxvi
His studie was true Iustice how to deale, And day and night employ’d his busie paine How to reforme that ragged common-weale:
And that same yron man which could reueale
All hidden crimes, through all that realme he sent, To search out those, that vsd to rob and steale, Or did rebell gainst lawfull gouernment; On whom he did inflict most grieuous punishment.
But ere he could reforme it thoroughly, xxvii
He through occasion called was away, To Faerie Court, that of necessity
His course of Iustice he was forst to stay, And Talus to reuoke from the right way, In which he was that Realme for to redresse.
But enuies cloud still dimmeth vertues ray. So hauing freed Irena from distresse, He tooke his leaue of her, there left in heauinesse.
Tho as he backe returned from that land, xxviii
And there arriu’d againe, whence forth he set, He had not passed farre vpon the strand, When as two old ill fauour’d Hags he met, By the way side being together set, Two griesly creatures; and, to that their faces
Most foule and filthie were, their garments yet Being all rag’d and tatter’d, their disgraces Did much the more augment, and made most vgly cases.
The one of them, that elder did appeare, xxix
With her dull eyes did seeme to looke askew, That her mis-shape much helpt; and her foule heare Hung loose and loathsomely: Thereto her hew Was wan and leane, that all her teeth arew, And all her bones might through her cheekes be red; Her lips were like raw lether, pale and blew, And as she spake, therewith she slauered; Yet spake she seldom, but thought more, the lesse she sed.
Her hands were foule and durtie, neuer washt xxx In all her life, with long nayles ouer raught, Like puttocks clawes: with th’one of which she scracht Her cursed head, although it itched naught; The other held a snake with venime fraught, On which she fed, and gnawed hungrily[394] , As if that long she had not eaten ought; That round about her iawes one might descry The bloudie gore and poyson dropping lothsomely
Her name was Enuie, knowen well thereby; xxxi Whose nature is to grieue, and grudge at all, That euer she sees doen prays-worthily, Whose sight to her is greatest crosse, may fall, And vexeth so, that makes her eat her gall. For when she wanteth other thing to eat, She feedes on her owne maw vnnaturall, And of her owne foule entrayles makes her meat; Meat fit for such a monsters monsterous dyeat.
And if she hapt of any good to heare, xxxii That had to any happily betid, Then would she inly fret, and grieue, and teare Her flesh for felnesse, which she inward hid: But if she heard of ill, that any did, Or harme, that any had, then would she make Great cheare, like one vnto a banquet bid;
And in anothers losse great pleasure take, As she had got thereby, and gayned a great stake.
The other nothing better was, then shee; xxxiii
Agreeing in bad will and cancred kynd, But in bad maner they did disagree: For what so Enuie good or bad did fynd, She did conceale, and murder her owne mynd; But this, what euer euill she conceiued, Did spred abroad, and throw in th’open wynd. Yet this in all her words might be perceiued, That all she sought, was mens good name to haue bereaued.
For what soeuer good by any sayd, xxxiv
Or doen she heard, she would streightwayes inuent, How to depraue, or slaunderously[395] vpbrayd, Or to misconstrue of a mans intent, And turne to ill the thing, that well was ment. Therefore she vsed often to resort, To common haunts, and companies frequent, To hearke what any one did good report, To blot the same with blame, or wrest in wicked sort.
And if that any ill she heard of any, xxxv She would it eeke, and make much worse by telling, And take great ioy to publish it to many, That euery matter worse was for her melling. Her name was hight Detraction, and her dwelling Was neare to Enuie, euen her neighbour next; A wicked hag, and Enuy selfe excelling In mischiefe: for her selfe she onely vext; But this same both her selfe, and others eke perplext.
Her face was vgly, and her mouth distort, xxxvi Foming with poyson round about her gils, In which her cursed tongue full sharpe and short Appear’d like Aspis sting, that closely kils,
Or cruelly does wound, whom so she wils: A distaffe in her other hand she had, Vpon the which she litle spinnes, but spils, And faynes to weaue false tales and leasings bad, To throw amongst the good, which others had disprad.
These two now had themselues combynd in one, xxxvii
And linckt together gainst Sir Artegall, For whom they wayted as his mortall fone, How they might make him into mischiefe fall, For freeing from their snares Irena thrall, Besides vnto themselues they gotten had A monster, which the Blatant beast men call, A dreadfull feend of gods and men ydrad, Whom they by slights allur’d, and to their purpose lad.
Such were these Hags, and so vnhandsome drest: xxxviii
Who when they nigh approching, had espyde
Sir Artegall return’d from his late quest, They both arose, and at him loudly cryde, As it had bene two shepheards curres, had scryde
A rauenous Wolfe amongst the scattered flockes. And Enuie first, as she that first him eyde, Towardes him runs, and with rude flaring lockes
About her eares, does beat her brest, and forhead knockes.
Then from her mouth the gobbet she does take, xxxix
The which whyleare she was so greedily
Deuouring, euen that halfe-gnawen snake, And at him throwes it most despightfully. The cursed Serpent, though she hungrily
Earst chawd thereon, yet was not all so dead, But that some life remayned secretly, And as he past afore withouten dread, Bit him behind, that long the marke was to be read.
Then th’other comming neare, gan him reuile, xl And fouly rayle, with all she could inuent;
Saying, that he had with vnmanly guile, And foule abusion both his honour blent,
And that bright sword, the sword of Iustice lent,[396] Had stayned with reprochfull crueltie, In guiltlesse blood of many an innocent: As for Grandtorto, him with treacherie And traynes hauing surpriz’d, he fouly did to die.
Thereto the Blatant beast by them set on xli
At him began aloud to barke and bay, With bitter rage and fell contention, That all the woods and rockes nigh to that way, Began to quake and tremble with dismay; And all the aire rebellowed againe. So dreadfully his hundred tongues did bray, And euermore those hags them selues did paine, To sharpen him, and their owne cursed tongs did straine.
And still among most bitter wordes they spake, xlii Most shamefull, most vnrighteous, most vntrew, That they the mildest man aliue would make Forget his patience, and yeeld vengeaunce dew
To her, that so false sclaunders[397] at him threw. And more to make them pierce and wound more deepe, She with the sting, which in her vile tongue grew, Did sharpen them, and in fresh poyson steepe: Yet he past on, and seem’d of them to take no keepe.
But Talus hearing her so lewdly raile, xliii And speake so ill of him, that well deserued, Would her haue chastiz’d with his yron flaile, If her Sir Artegall had not preserued, And him forbidden, who his heast obserued. So much the more at him still did she scold, And stones did cast, yet he for nought would swerue From his right course, but still the way did hold To Faery Court, where what him fell shall else be told.
FOOTNOTES:
[387] i 9 enduren] endure 1596
[388] v 9 th’Eagle 1609
[389] xi 6 Artegals 1596
[390] xiv 1 presumptuous 1609 passim
[391] 8 steele 1609
[392] xvii 5 such] sure 1609
[393] xxiii 2 strooke 1609
[394] xxx 6 hungerly 1609
[395] xxxiv 3 slanderously 1609
[396] xl 5 And that bright sword the sword, of Iustice lent 1596
[397] xlii 5 slaunders 1609
THE SIXTE BOOKE OF THE FAERIE QVEENE.
Contayning
THE LEGEND OF S. CALIDORE OR OF COVRTESIE.
he waies, through which my weary steps I guyde, i this delightfull land of Faery, Are so exceeding spacious and wyde, And sprinckled with such sweet variety, Of all that pleasant is to eare or eye, That I nigh rauisht with rare thoughts delight, My tedious trauell doe forget thereby; And when I gin to feele decay of might, It[398] strength to me supplies, and chears my dulled spright.
Such secret comfort, and such heauenly pleasures, ii Ye sacred imps, that on Parnasso dwell, And there the keeping haue of learnings threasures, Which doe all worldly riches farre excell, Into the mindes of mortall men doe well,
And goodly fury into them infuse; Guyde ye my footing, and conduct me well In these strange waies, where neuer foote did vse, Ne none can find, but who was taught them by the Muse.
Reuele to me the sacred noursery iii
Of vertue, which with you doth there remaine, Where it in siluer bowre does hidden ly From view of men, and wicked worlds disdaine. Since[399] it at first was by the Gods with paine Planted in earth, being deriv’d at furst From heauenly seedes of bounty soueraine, And by them long with carefull labour nurst, Till it to ripenesse grew, and forth to honour burst.
Amongst them all growes not a fayrer flowre, iv Then is the bloosme of comely courtesie, Which though it on a lowly stalke doe bowre, Yet brancheth forth in braue nobilitie, And spreds it selfe through all ciuilitie: Of which though present age doe plenteous seeme, Yet being matcht with plaine Antiquitie, Ye will them all but fayned showes esteeme, Which carry colours faire, that feeble eies misdeeme.
But in the triall of true curtesie, v
Its now so farre from that, which then it was, That it indeed is nought but forgerie, Fashion’d to please the eies of them, that pas, Which see not perfect things but in a glas: Yet is that glasse so gay, that it can blynd The wisest sight, to thinke gold that is bras. But vertues seat is deepe within the mynd, And not in outward shows, but inward thoughts defynd.
But where shall I in all Antiquity vi So faire a patterne finde, where may be seene
The goodly praise of Princely curtesie, As in your selfe, O soueraine Lady Queene, In whose pure minde, as in a mirrour sheene, It showes, and with her brightnesse doth inflame The eyes of all, which thereon fixed beene; But meriteth indeede an higher name: Yet so from low to high vplifted is your name[400] .
Then pardon me, most dreaded Soueraine, vii That from your selfe I doe this vertue bring, And to your selfe doe it returne againe: So from the Ocean all riuers spring, And tribute backe repay as to their King. Right so from you all goodly vertues well Into the rest, which round about you ring, Faire Lords and Ladies, which about you dwell, And doe adorne your Court, where courtesies excell.
FOOTNOTES:
[398] 9 It] tI 1596
[399] iii 5 Since] Sith 1609
[400] vi 9 name] fame edd
Cant. I.
Calidore saues from Maleffort, A Damzell vsed vylde: Doth vanquish Crudor, and doth make Briana wexe more mylde.
Of Court it seemes, men Courtesie doe call, i For that it there most vseth to abound; And well beseemeth that in Princes hall That vertue should be plentifully found, Which of all goodly manners is the ground, And roote of ciuill conuersation. Right so in Faery court it did redound, Where curteous Knights and Ladies most did won Of all on earth, and made a matchlesse paragon.
But mongst them all was none more courteous Knight, ii Then Calidore, beloued ouer all, In whom it seemes, that gentlenesse of spright And manners mylde were planted naturall; To which he adding comely guize withall, And gracious speach, did steale mens hearts away. Nathlesse thereto he was full stout and tall, And well approu’d in batteilous affray,
That him did much renowme, and far his fame display
Ne was there Knight, ne was there Lady found iii In Faery court, but him did deare embrace, For his faire vsage and conditions sound, The which in all mens liking gayned place, And with the greatest purchast greatest grace: Which he could wisely vse, and well apply, To please the best, and th’euill to embase. For he loathd leasing, and base flattery, And loued simple truth and stedfast honesty
And now he was in trauell on his way, iv Vppon an hard aduenture sore bestad, Whenas by chaunce he met vppon a day With Artegall, returning yet halfe sad From his late conquest, which he gotten had. Who whenas each of other had a sight, They knew them selues, and both their persons rad: When Calidore thus first; Haile noblest Knight Of all this day on ground, that breathen liuing spright.
Now tell, if please you, of the good successe, v Which ye haue had in your late enterprize.
To whom Sir Artegall gan to expresse
His whole exploite, and valorous emprize, In order as it did to him arize.
Now happy man (sayd then Sir Calidore) Which haue so goodly, as ye can deuize, Atchieu’d so hard a quest, as few before; That shall you most renowmed make for euermore.
But where ye ended haue, now I begin vi To tread an endlesse trace, withouten guyde, Or good direction, how to enter in, Or how to issue forth in waies vntryde, In perils strange, in labours long and wide, In which although good Fortune me befall,
Yet shall it not by none be testifyde. What is that quest (quoth then Sir Artegall) That you into such perils presently doth call?
The Blattant Beast (quoth he) I doe pursew, vii
And through the world incessantly doe chase, Till I him ouertake, or else subdew: Yet know I not or how, or in what place
To find him out, yet still I forward trace.
What is that Blattant Beast? (then he replide.)[401] It is a Monster bred of hellishe race, (Then answerd he) which often hath annoyd Good Knights and Ladies true, and many else destroyd.
Of Cerberus whilome he was begot, viii And fell Chimæra in her darkesome den, Through fowle commixture of his filthy blot; Where he was fostred long in Stygian fen, Till he to perfect ripenesse grew, and then Into this wicked world he forth was sent, To be the plague and scourge of wretched men: Whom with vile tongue and venemous intent He sore doth wound, and bite, and cruelly torment.
Then since the saluage Island I did leaue,[402] ix
Sayd Artegall, I such a Beast did see, The which did seeme a thousand tongues to haue, That all in spight and malice did agree, With which he bayd and loudly barkt at mee, As if that he attonce would me deuoure.
But I that knew my selfe from perill free, Did nought regard his malice nor his powre, But he the more his wicked poyson forth did poure.
That surely is that Beast (saide Calidore) x Which I pursue, of whom I am right glad
To heare these tidings, which of none afore
Through all my weary trauell I haue had: Yet now some hope your words vnto me add. Now God you speed (quoth then Sir Artegall) And keepe your body from the daunger drad: For ye haue much adoe to deale withall.[403] So both tooke goodly leaue, and parted seuerall.
Sir Calidore thence trauelled not long, xi
When as by chaunce a comely Squire he found, That thorough some more mighty enemies wrong, Both hand and foote vnto a tree was bound: Who seeing him from farre, with piteous sound
Of his shrill cries him called to his aide.
To whom approching, in that painefull stound
When he him saw, for no demaunds he staide, But first him losde, and afterwards thus to him saide.
Vnhappy Squire, what hard mishap thee brought xii
Into this bay of perill and disgrace?
What cruell hand thy wretched thraldome wrought, And thee captyued in this shamefull place?
To whom he answerd thus; My haplesse case Is not occasiond through my misdesert, But through misfortune, which did me abase
Vnto this shame, and my young hope subuert, Ere that I in her guilefull traines was well expert.
Not farre from hence, vppon yond rocky hill, xiii
Hard by a streight there stands a castle strong, Which doth obserue a custome lewd and ill, And it hath long mayntaind with mighty wrong: For may no Knight nor Lady passe along That way, (and yet they needs must passe that way,)
By reason of the streight, and rocks among, But they that Ladies lockes doe shaue away, And that knights berd for toll, which they for passage pay.[404]
A shamefull vse as euer I did heare, xiv
Sayd Calidore, and to be ouerthrowne. But by what meanes did they at first it reare, And for what cause, tell if thou haue it knowne. Sayd then that Squire: The Lady which doth owne This Castle, is by name Briana hight. Then which a prouder Lady liueth none: She long time hath deare lou’d a doughty Knight, And sought to win his loue by all the meanes she might.
His name is Crudor, who through high disdaine xv And proud despight of his selfe pleasing mynd, Refused hath to yeeld her loue againe, Vntill a Mantle she for him doe fynd, With beards of Knights and locks of Ladies lynd. Which to prouide, she hath this Castle dight, And therein hath a Seneschall assynd, Cald Maleffort, a man of mickle might, Who executes her wicked will, with worse despight.
He this same day, as I that way did come xvi With a faire Damzell, my beloued deare, In execution of her lawlesse doome, Did set vppon vs flying both for feare: For little bootes against him hand to reare. Me first he tooke, vnhable[405] to withstond; And whiles he her pursued euery where, Till his returne vnto this tree he bond: Ne wote I surely, whether her he yet haue fond.
Thus whiles they spake, they heard a ruefull shrieke xvii
Of one loud crying, which they streight way ghest, That it was she, the which for helpe did seeke. Tho looking vp vnto the cry to lest, They saw that Carle from farre, with hand vnblest Hayling that mayden by the yellow heare, That all her garments from her snowy brest,
And from her head her lockes he nigh did teare, Ne would he spare for pitty, nor refraine for feare.
Which haynous sight when Calidore beheld, xviii
Eftsoones he loosd that Squire, and so him left, With hearts dismay and inward dolour queld, For to pursue that villaine, which had reft That piteous spoile by so iniurious theft. Whom ouertaking, loude to him he cryde; Leaue faytor quickely that misgotten weft
To him, that hath it better iustifyde, And turne thee soone to him, of whom thou art defyde.
Who hearkning to that voice, him selfe vpreard, xix
And seeing him so fiercely towardes make, Against him stoutly ran, as nought afeard, But rather more enrag’d for those words sake; And with sterne count’naunce thus vnto him spake. Art thou the caytiue, that defyest me, And for this Mayd, whose party thou doest take, Wilt giue thy beard, though it but little bee? Yet shall it not her lockes for raunsome fro me free.
With that he fiercely at him flew, and layd xx
On hideous strokes with most importune might, That oft he made him stagger as vnstayd, And oft recuile to shunne his sharpe despight. But Calidore, that was well skild in fight, Him long forbore, and still his spirite spar’d, Lying in waite, how him he damadge might. But when he felt him shrinke, and come to ward, He greater grew, and gan to driue at him more hard.
Like as a water streame, whose swelling sourse xxi
Shall driue a Mill, within strong bancks is pent, And long restrayned of his ready course; So soone as passage is vnto him lent, Breakes forth, and makes his way more violent.
Such was the fury of Sir Calidore, When once he felt his foeman to relent; He fiercely him pursu’d, and pressed sore, Who as he still decayd, so he encreased more.
The heauy burden of whose dreadfull might xxii When as the Carle no longer could sustaine, His heart gan faint, and streight he tooke his flight Toward the Castle, where if need constraine, His hope of refuge vsed to remaine. Whom Calidore perceiuing fast to flie, He him pursu’d and chaced through the plaine, That he for dread of death gan loude to crie Vnto the ward, to open to him hastilie.
They from the wall him seeing so aghast, xxiii The gate soone opened to receiue him in, But Calidore did follow him so fast, That euen in the Porch he him did win, And cleft his head asunder to his chin.
The carkasse[406] tumbling downe within the dore, Did choke the entraunce with a lumpe of sin, That it could not be shut, whilest Calidore Did enter in, and slew the Porter on the flore.
With that the rest, the which the Castle kept, xxiv About him flockt, and hard at him did lay; But he them all from him full lightly swept, As doth a Steare, in heat of sommers day,[407] With his long taile the bryzes brush away. Thence passing forth, into the hall he came, Where of the Lady selfe in sad dismay He was ymett, who with vncomely shame Gan him salute, and fowle vpbrayd with faulty blame.
False traytor Knight, (sayd she) no Knight at all, xxv But scorne of armes that hast with guilty hand
Murdred my men, and slaine my Seneschall; Now comest thou to rob my house vnmand, And spoile my selfe, that can not thee withstand? Yet doubt thou not, but that some better Knight
Then thou, that shall thy treason vnderstand, Will it auenge, and pay thee with thy right: And if none do, yet shame shal thee with shame requight.[408]
Much was the Knight abashed at that word; xxvi
Yet answerd thus; Not vnto me the shame, But to the shamefull doer it afford.
Bloud is no blemish; for it is no blame
To punish those, that doe deserue the same; But they that breake bands of ciuilitie, And wicked customes make, those doe defame
Both noble armes and gentle curtesie. No greater shame to man then inhumanitie.
Then doe your selfe, for dread of shame, forgoe xxvii
This euill manner, which ye here maintaine, And doe in stead thereof mild curt’sie showe
To all, that passe. That shall you glory gaine
More then his loue, which thus ye seeke t’obtaine. Wherewith all full of wrath, she thus replyde; Vile recreant, know that I doe much disdaine
Thy courteous lore, that doest my loue deride, Who scornes thy ydle scoffe, and bids thee be defyde.
To take defiaunce at a Ladies word xxviii
(Quoth he) I hold it no indignity; But were he here, that would it with his sword Abett, perhaps he mote it deare aby.
Cowherd (quoth she) were not, that thou wouldst fly, Ere he[409] doe come, he should be soone in place. If I doe so, (sayd he) then liberty I leaue to you, for aye me to disgrace
With all those shames, that erst ye spake me to deface.
