Box 2 | Influential theories of brain–viscera interactions

From the following article:

Gut feelings: the emerging biology of gut–brain communication

Emeran A. Mayer

Nature Reviews Neuroscience 12, 453-466 (August 2011)

doi:10.1038/nrn3071

The first comprehensive scientific theory of brain–viscera interactions was formulated in the 1880s by William James and Carl Lange and was based on the central concept that stimuli that induce emotions such as fear, anger or love initially induce changes in visceral function through autonomic nervous system output, and that the afferent feedback of these peripheral changes to the brain is essential in the generation of specific emotional feelings8. According to this theory, we feel anxious because we perceive our heart beating faster, because we become aware of our respiration becoming more frequent and shallower, or because we feel 'butterflies' in our stomach. In the late 1920s, Walter Cannon challenged the James–Lange theory, postulating that emotional feelings are generated directly by subcortical brain regions rather than from the feedback of situational bodily changes. He proposed that such bodily changes that are associated with emotional states are simply by-products of these brain changes, and that the visceral responses are too slow to play any part in the subjective experience of emotional feelings7.

Modern theories of emotion and consciousness that were proposed in the form of the 'somatic marker' hypothesis by Antonio Damasio81, and the 'homeostatic emotion' hypothesis by A. D. Craig78 have re-emphasized the importance of interoceptive feedback in emotional states and cognitive processes, and have largely overcome the long lasting controversy about the directionality of brain–viscera interactions in the generation of emotions.

For example, Damasio eloquently proposed that somatic markers (for example, memories of body states associated with previous feeling states) arise from positive or negative emotional feeling states being associated with visceral and other bodily responses (body loops) to certain contextual situations. According to this theory, these body loops, or their meta-representations in the orbitofrontal cortex (OFC), may play a part not only in how somebody feels at a given moment but may also influence future planning and intuitive decision making. For example, according to Damasio, somatic markers may covertly result in “undeliberated inhibition of a response learned previously ... [or] the introduction of a bias in the selection of an aversive or appetitive mode of behavior”81, 149.

Craig's homeostatic emotion hypothesis postulates that, in humans and anthropoid primates, an image of the homeostatic state of the body is created in the primary interoceptive cortex (dorsal posterior insula) through lamina I spinothalamic and vagal afferent tract projection to a specific thalamocortical relay nucleus in the posterolateral thalamus77. This interoceptive cortex contains modality-selective representations of all afferent activity from lamina I (that is, sympathetic afferent input) and from the nucleus tractus solitarius (parasympathetic input). According to Craig, re-representation of the image from the posterior insula to the mid and anterior insula, and modulation by inputs from affective, cognitive and reward-related brain circuits creates a feeling about the homeostatic state of the body in the anterior insula78, 80. Together with the parallel processed signal in the anterior cingulate cortex (ACC), a homeostatic emotion arises, made up of a feeling dimension represented in the anterior insula and a motivation dimension represented in the ACC78.