The somatic marker hypothesis: revisiting the role of the ‘body-loop’ in decision-making

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Highlights

  • An update on mechanisms supporting the ‘body-loop’ of the somatic marker hypothesis.

  • Anterior insula, anterior cingulate, and vmPFC are visceromotor control regions.

  • The vagus nerve is a primary conduit by which interoceptive states influence cognition.

  • Visceral states can alter the activity of brainstem neurotransmitter cell bodies.

  • Bio-regulatory phases interact with cognition on a dynamic temporal range.

The somatic marker hypothesis is one of the most influential neurocognitive theories of emotion and decision-making. A key aspect of the somatic marker hypothesis is the ‘body-loop’, which is the claim that emotive events that are expressed in the body can influence decision-making via afferent feedback to the brain. The body-loop has often been the subject of debate. However, evidence for the neural and peripheral mechanisms that support interactions between bodily states and cognitive functions has consistently emerged. The purpose of this article is to outline an updated neurophysiological account of how somatic states may be triggered, and how they bias decisions through afferent feedback. We largely focus on vagus nerve-dependent feedback mechanisms, which demonstrate how interoceptive signals can shape high order cognition and goal-directed behavior.

Introduction

The somatic marker hypothesis has been one of the most influential neurocognitive theories of decision-making since its proposal by A. R. Damasio in the early 1990s [1]. The SMH is a systems-level neurocognitive framework for decision-making and its influence by emotion. The broad claim of the SMH is that decision-making is a process that is influenced by visceral and somatosensory markers that arise in bioregulatory processes, including those that express themselves in emotions and feelings. The ventromedial cortex (VMPFC), including the mesial orbitofrontal (OFC) region, is a critical component of a neural system subserving decision-making and affective processing. However, decision-making is not mediated by the VMPFC alone, it arises from large-scale systems that include other cortical and subcortical components. Such structures include the amygdala, the somatosensory and insular cortices, and the peripheral nervous system.

The SMH proposes that the VMPFC provides the substrate for learning an association between complex situations and the bio-regulatory or emotional state usually associated with that class of situation in the individual's experience, and how the VMPFC acts as a trigger region to re-activate somatic patterns when an individual faces a situation for which some aspects have been previously experienced. The re-activation can be carried out via a ‘body-loop’, in which the body changes in response to brain activity, and the ensuing changes are relayed to somatosensory and insular cortices. Alternatively, in the ‘as-if body-loop’, the body is bypassed and those re-activation signals from the VMPFC are conveyed to the somatosensory and insular cortices, which then adopt the appropriate neural pattern [2]. Most of the early empirical research on the SMH focused on how decision-making behaviors and autonomic responses were altered in patients with focal lesions to the VMPFC, amygdala, and insula [3]. These early lesion studies were able to address some aspects of the body-loop and its role in modulating decisions, such as by establishing that peripheral autonomic responses during various aspects of decision-making depend on lesion site [2]. However, these studies could not definitively demonstrate the influence of ascending feedback on decision-making. Indeed, historical criticism of the SMH has primarily concerned the plausibility of the influence of somatic feedback on high-order cognitive processes. Therefore, the purpose of this article is to provide an updated account for the body-loop by drawing from recent literature on how somatic states are triggered, and how somatic states may modulate decision-making through peripheral feedback. The evidence strongly suggests that visceral processes mediated by afferent vagus nerve signaling participate in shaping high-order cognition by influencing activity of brainstem-level neurotransmitter systems involved in learning, memory, and motivation and valuation. To begin, we review the current evidence for a system of cortical and subcortical structures which have an essential role in visceromotor and viscerosensory processing. These regions largely overlap with regions implicated in emotion and decision-making.

Section snippets

The role of ventral PFC and agranular insular cortex in triggering somatic states

The SMH proposed that primary or secondary inducers trigger somatic states. Primary inducers are sensory stimuli that are innate or learned to be pleasurable or aversive, and automatically elicit a somatic response. Secondary inducers are entities generated by the recall of a personal or hypothetical emotional event concerning a primary inducer, which, when brought to working memory, elicit a somatic state. The amygdala was shown to be important for triggering somatic states from primary

The afferent side of the body-loop: the role of the vagus nerve

Some early empirical work on the SMH suggested that the vagus nerve, rather than the spinal cord, is a critical conduit for communicating somatic states to the brain [23]. The vagus nerve is a complex autonomic, endocrine, and immune regulatory interface through which the body communicates with the brain, and the brain with the body. Primarily parasympathetic vagal efferent fibers innervate thoracic (e.g. cardiac) and abdominal organs and exert effects on these end organ systems through largely

Low-level bioregulatory phase interactions with high-order cognition

One of the old criticisms of the SMH was the time it may take to engage the body-loop. The issue surrounds whether decision-making in associative learning paradigms such as the IGT occur much faster than the time it takes to trigger, and then perceive, somatic states. It is known that slow-scale, cyclical fluctuations in sex-hormone levels modulate reward, fear learning and extinction [40, 41], but brain-body communications occur on a highly dynamic temporal range down to the scale of a few

The interoception and the insula in decision-making

A central insight of the SMH is that feedback generated by bodily states will eventually be represented in insular and somatosensory cortices, providing a substrate for representing visceral feeling states and interoceptive memories, which can then influence decision-making. Indeed, interoception appears to be highly relevant to hedonic judgments and motivational states concerning allostasis-homeostasis and goal-directed behaviors [51, 52•]. Interoceptive context affects neural processing of

Summary

Collectively, these studies broaden the empirical evidence in support of the fundamental elements of the SMH, especially those pertaining to the enactment of somatic (body) states, and the influence of patterns of bodily changes on cognition. The vagus appears to have a broad role in communicating the peripheral consequences of emotional and homeostatic events to somato-and-viscerosensory regions, which in turn, can alter motivational urges, consistent with the idea that representations of

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We would like to thank John Monterosso, Giorgio Coricelli, and Chris Baeken for their helpful comments. This work is supported by funding from NIH-NCI R01CA152062 to A. Bechara and NSF GRFP (DGE-1418060) to T. Poppa.

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