Challenges and Opportunities for the Affective Sciences
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Fox et al., Research Agenda for the Affective Sciences 1 Challenges and Opportunities for the Affective Sciences Andrew S. Fox* Department of Psychology and California National Primate Research Center, University of California, Davis, CA USA Regina C. Lapate* Helen Wills Neuroscience Institute, University of California, Berkeley, CA USA Richard J. Davidson Center for Healthy Minds, University of Wisconsin—Madison, Madison, WI USA Alexander J. Shackman* Department of Psychology, Neuroscience and Cognitive Science Program, and Maryland Neuroimaging Center, University of Maryland, College Park, MD USA * contributed equally Word Count: Title (7 words); Main Text (3,909/3,500); References (107) Additional Elements: 1 Figure and 1 Box Abstract: 94 words Keywords: affective neuroscience; biological psychiatry; emotion; individual differences; neuroimaging Address Correspondence to: Andrew S. Fox ([email protected]) –or– Alexander J. Shackman ([email protected]) Fox et al., Research Agenda for the Affective Sciences 2 ABSTRACT (94 words) Emotion is a core feature of the human condition, with profound consequences for health, wealth, and wellbeing. Over the past quarter-century, improved methods for manipulating and measuring different features of emotion have yielded steady advances in our scientific understanding emotional states, traits, and disorders. Yet, it is clear that most of the work remains undone. Here, we highlight key challenges facing the field of affective sciences. Addressing these challenges will provide critical opportunities not just for understanding the mind, but also for increasing the impact of the affective sciences on public health and well-being. Fox et al., Research Agenda for the Affective Sciences 3 INTRODUCTION Emotions play a central role in human experience and there is an abiding interest—among scientists, clinicians, and the public at large—in understanding their nature and determining their impact on health and disease. Over the past quarter-century, improved methods for manipulating and measuring emotion and its underlying neurobiology have yielded a steady stream of new insights and stimulated the development of new theoretical frameworks, as outlined in recent reviews, books, and edited volumes [1- 9]. Despite this progress, our understanding remains far from complete. Rather than a comprehensive review, in this perspective we selectively highlight several major challenges facing the affective sciences. In some cases, addressing these challenges promises to fundamentally change our basic understanding of emotion, while addressing others has the potential to transform how affective science is applied in the clinic and everyday life. Understanding What Emotions Are, and the Mechanisms Linking Emotional Stimuli and Responses Affective scientists agree that emotions are central features of daily life, and that they evolved to be more adaptive than not [10]. But beyond this limited agreement, recent years have witnessed a vigorous and persistent debate about the nature of emotion, with leading theorists challenging the canon of facts and shared conceptual assumptions that has inspired and guided the field for the past quarter-century [1, 3, 11-14]. At the heart of this debate lies a fundamental question, What are emotions and how should we define them? Are they ‘basic’ natural kinds waiting to be discovered and catalogued (like stars) or are they ‘constructed’ by humans and imposed on the natural world (like constellations)? How one chooses to define emotions has direct ramifications for other fundamental questions about the nature of emotion (Box 1) [15]. Fox et al., Research Agenda for the Affective Sciences 4 Students of emotion agree that emotionally charged stimuli can spark a range of responses—thoughts, behaviors, peripheral physiological changes, and, of course, feelings. Yet, aside from simple kinds of conditioned threat, we still know relatively little about the cascade of biological and psychological processes that mediate these responses. Although a number of theoretical placeholders have been proposed—including cognitive appraisals [14], ‘emotional evaluations’ [16], and ‘pattern detectors’ [17]—we still do not really understand the processes that determine whether a particular emotion is generated in response to a specific challenge, and, if so, how it is expressed and experienced. Existing models do not fully describe how ecologically relevant information, including foreground cues (e.g., seeing a bear), contextual cues (e.g., escape route), and interoceptive cues (e.g., fatigue) are evaluated, integrated, and collectively used to bias or select among competing responses (e.g., freezing vs. flight) (Figure 1) [18]. It is also unclear whether these processes are consistent across putative emotion states (e.g., fear vs. disgust), or whether it will be necessary to have separate models for each [19]. Thus, there is a clear need for testable, biologically plausible hypotheses that address the complex mapping between emotional antecedents and their consequences, and the ways in which these mappings can differ across contexts [20, 21]. Already, some valuable clues are beginning to emerge. For instance, researchers have identified populations of mutually inhibitory neurons in the central nucleus of the amygdala (Ce) that respond to the identical threat, but initiate opposing responses, freezing or fleeing [22-24]. Determining how the brain transforms the sensory processing stream into discrete emotional behaviors and understanding how it selects among competing responses is important, and would provide a means of adjudicating between different theories of emotion. These studies may reveal that different features of an emotional response are independently controlled by the brain, with no clear distinctions between putative emotions (‘many-to-many’), which would be consistent with a pure constructivist view [2]. Or, they could reveal circumscribed biological triggers for coordinated emotional responses (‘one-to-many’), which would be more consistent with a basic emotions perspective [8, 25]. A third, and perhaps more Fox et al., Research Agenda for the Affective Sciences 5 likely outcome, is that neither position is altogether correct. Recent work has revealed a degree of biological complexity that goes well beyond that embodied in contemporary models of emotion. For example, as noted above, the Ce plays a key role in determining how an animal responds to threat, with particular populations of neurons promoting one set of responses, while simultaneously inhibiting neighboring populations responsible for triggering others. These observations reveal a circumscribed mechanism that orchestrates multiple aspects of the emotional response (‘one-to-many’). This is consistent with basic emotions theory, which conceptualizes emotions as natural kinds waiting to be discovered. On the other hand, these and other observations are inconsistent with a basic, irreducible state of ‘fear’ (cf. Figure 1; although they may be compatible with a more complex family of fear-related states). But, basic emotions theory is not the only one that is lacking. These findings are also inconsistent with pure constructivist theories, which describe a many-to-many mapping between the brain and emotional responses and do not account for regional cell populations triggering the same complex response across individuals. They are also inconsistent with two-parameter models (e.g., valence/arousal, reinforcer/omission-presentation [10]), which do not explain qualitative transitions in emotion responses (e.g., freezing, fleeing, defensive attack) across different contexts (Figure 1). A critical challenge for the future will be to determine how these brain systems develop and the degree to which their function is stable over time, clarify their sensitivity to context and specificity to particular elicitors and responses, and ultimately probe their role in the kinds of subjective experiences that have shaped contemporary scientific models of emotion and emotional disorders. Understanding the biological and psychological mechanisms that link emotion elicitors to emotional responses promises to reveal the parameters on which emotional experience is formulated—be they basic, constructed, or something else. Doing so would provide valuable clues about the best way to conceptualize emotions, their function, and their dysfunction. Fox et al., Research Agenda for the Affective Sciences 6 The Interplay and Integration of Emotion and Cognition In everyday experience, emotion and cognition seem fundamentally different. Emotion is hot, bright, and quick; infused with feelings of pleasure or pain and manifesting in readily discerned changes in the body. By comparison, cognition—calculating a tip, preparing a report, studying for an examination—often feels cold, gray, and slow; devoid of clear hedonic, motivational, or somatomotor features. From classical times to the present, these apparent differences in phenomenological experience and peripheral physiology have led lay people and many scholars to treat emotion and cognition as categorically distinct, even oppositional, mental faculties [26]. But today, there is a growing scientific consensus that emotion and cognition are deeply interwoven in the fabric of both the mind and the brain [10, 27, 28]. This should not be surprising—after all, the human brain did not evolve to optimize performance on laboratory measures of cognition or to passively respond to experimental manipulations of emotion.