A common role of insula in feelings, empathy and uncertainty

Although accumulating evidence highlights a crucial role of the insular cortex in feelings, empathy and processing uncertainty in the context of decision making, neuroscientific models of affective learning and decision making have mostly focused on structures such as the amygdala and the striatum. Here, we propose a unifying model in which insula cortex supports different levels of representation of current and predictive states allowing for error-based learning of both feeling states and uncertainty. This information is then integrated in a general subjective feeling state which is modulated by individual preferences such as risk aversion and contextual appraisal. Such mechanisms could facilitate affective learning and regulation of body homeostasis, and could also guide decision making in complex and uncertain environments.

Introduction

Human insular cortex is a large and highly interconnected structure embedded deep in the brain (Box 1). Despite neuroimaging observations of insula engagement across multiple tasks, the contribution of this region has been largely neglected within neuroscientific theories and models. The emergence of affective and social neuroscience has accumulated evidence implicating insular cortex, particularly its most anterior portion (the anterior insula, AI), in visceral representation and emotional experience. Commentaries emphasize the activation of AI by motivationally important changes in bodily states as diverse as autonomic arousal, sensual touch, air hunger, taste, craving and pain 1, 2, 3, 4, 5, 6. Furthermore, AI activity reflects the subjective intensity of both one's own and others’ emotional experiences, for example, when one experiences distress, pain or disgust [7] or when one empathizes with others who are in these emotional states 8, 9, 10. Finally, neuroeconomics, which studies motivational decision making, has recently strongly linked AI activity to processing, representing and learning information about risk and uncertainty 11, 12, 13, 14.

Until now, however, no model of insula function has integrated its contribution to physiological and emotional states with empathic understanding or behavioural risk processing. Here, we propose a novel account of the role of insula in which predictions and realizations of bodily and affective states are integrated with predictions and realizations of uncertainty, to engender an integrated feeling state that is shaped by individual risk preference and appraisal of the context. Before outlining our model and its implications, we will first summarize relevant studies illustrating insula involvement in: (i) bodily awareness, (ii) self-related and empathic feelings, (iii) risk and uncertainty processing (for earlier extensive reviews of the literature in these respective domains, see for example Refs. 1, 2, 4, 15, 16, 17, 18, 19).