Anterior insular cortex and emotional awareness

Abstract

This paper reviews the foundation for a role of the human anterior insular cortex (AIC) in emotional awareness, defined as the conscious experience of emotions. We first introduce the neuroanatomical features of AIC and existing findings on emotional awareness. Using empathy, the awareness and understanding of other people's emotional states, as a test case, we then present evidence to demonstrate: 1) AIC and anterior cingulate cortex (ACC) are commonly coactivated as revealed by a meta-analysis, 2) AIC is functionally dissociable from ACC, 3) AIC integrates stimulus-driven and top-down information, and 4) AIC is necessary for emotional awareness. We propose a model in which AIC serves two major functions: integrating bottom-up interoceptive signals with top-down predictions to generate a current awareness state and providing descending predictions to visceral systems that provide a point of reference for autonomic reflexes. We argue that AIC is critical and necessary for emotional awareness.

Keywords: anterior insular cortex; bottom-up; emotional awareness; empathy; fMRI; meta-analysis; predictive coding; top-down.

Figure 1

Meta-analysis of fMRI studies of empathy processing. A: Empathy for all three emotions examined (pain, negative, positive). B: Empathy for pain. C: Empathy for negative emotions. D: Empathy for positive emotions. Color intensity represents ALE value. Note that AIC bilaterally are commonly involved in all conditions (x = −38 and 38) and that ACC is involved in all but empathy for positive emotions. See Tables (2–5) for details regarding coordinates and ALE values.

Figure 2

Empathetic pain as a test case to study the AIC–awareness relationship. A: Visual stimuli and task conditions used in empathetic pain paradigms (modified from Gu et al., 2010, 2013). B: After controlling for cognitive load, only AIC, and not ACC, showed increased activation for empathetic pain (modified from Gu et al., 2010). C: Cognition–emotion interaction effect in AIC (modified from Gu et al., 2013). D: AIC lesions, but not ACC lesions, are associated with diminished sensitivity to others’ pain in the explicit empathy task (left, indexed by smaller d′ based on signal detection theory) and lack of task–stimulus interference in the implicit empathy task (right, indexed by d′_painful − d′_nonpainful; for details see Gu et al., 2012). AIC, anterior insular cortex; ACC, anterior cingulate cortex; NC, neurologically intact controls; BDC, brain-damaged controls; TP, task painl; TL, task laterality; TB, task body part. * P < 0.05, **P < 0.01.

Figure 3

Hypothetical model of insula and awareness. In this hierarchical scheme, each lower-level structure receives descending predictions from and sends ascending prediction errors to higher-level regions. Anterior insular cortex (AIC) serves two major processes in this model (center): 1) integrating bottom-up interoceptive prediction errors with top-down predictions from high-order brain regions such as the anterior cingulate cortex (ACC) and prefrontal cortex (PFC), analogous to the role of sensory cortices (e.g., visual and auditory areas) in exteroceptive processing (left) and 2) sending descending predictions to the autonomic system via smooth muscles to provide a point of reference for autonomic reflexes, similar to the role of motor cortex in generating proprioceptive output via striated muscles (right).