Interoceptive dysfunction: Toward an integrated framework for understanding somatic and affective disturbance in depression.

Abstract

Depression is characterized by disturbed sleep and eating, a variety of other, nonspecific somatic symptoms, and significant somatic comorbidities. Why there is such close association between cognitive and somatic dysfunction in depression is nonetheless poorly understood. An explosion of research in the area of interoception—the perception and interpretation of bodily signals—over the last decade nonetheless holds promise for illuminating what have until now been obscure links between the social, cognitive-affective, and somatic features of depression. This paper reviews rapidly accumulating evidence that both somatic signaling and interoception are frequently altered in depression. This includes comparative studies showing vagus-mediated effects on depression-like behaviors in rodent models as well as studies in humans indicating both dysfunction in the neural substrates for interoception (e.g., vagus, insula, anterior cingulate cortex) and reduced sensitivity to bodily stimuli in depression. An integrative framework for organizing and interpreting this evidence is put forward which incorporates (a) multiple potential pathways to interoceptive dysfunction; (b) interaction with individual, gender, and cultural differences in interoception; and (c) a developmental psychobiological systems perspective, emphasizing likely differential susceptibility to somatic and interoceptive dysfunction across the lifespan. Combined with current theory and evidence, it is suggested that core symptoms of depression (e.g., anhedonia, social deficits) may be products of disturbed interoceptive-exteroceptive integration. More research is nonetheless needed to fully elucidate the relationship between mind, body, and social context in depression.

Symptoms and the body: Taking the inferential leap

“…Through close connections with the anterior cingulate cortex, these multi-modal representations also involve affective-motivational components and associated approach-avoidance tendencies, consistent with the close connection between interoceptive inference about bodily states and feelings and emotions (Seth, 2013;Zaki et al, 2012). Other structures involved in processing the affective value of interoceptive stimuli are the orbitofrontal (Barrett and Bar, 2009) and ventromedial prefrontal cortex, which, together with parts of the cingulate cortex, are thought to constitute a stimulus valuation network (Harshaw, 2015) that engages behavioral control systems when local physiological regulation fails (e.g., gasping for air and opening the window when breathless).…”

“…Several brain structures and circuits are critical in constructing and representing a conscious state of the body (e.g., Craig, 2002Craig, , 2009) forming an interoceptive nervous system (Harshaw, 2015). For example, the anterior insular cortex is generally considered to play a central role in constructing a multimodal representation of the internal state of the body, integrating hormonal, immunological, metabolic, thermal, autonomic, visceromotor, proprioceptive, exteroceptive, motivational and cognitive sources of information (Craig, 2009;Critchley and Harrison, 2013).…”

“…Another important feature is that agranular visceromotor cortices are a central hub sending efferent copies of predictions to multiple sensory systems across the brain, and thus subserve "a multisensory representation of the world from the perspective of someone with a body" (Barrett and Simmons (2015, p. 424)). This architecture contributes to embodiment of perception, cognition and emotion, and to bi-directional penetrance (i.e., cross-fertilisation) of interoceptive and exteroceptive information (Harshaw, 2015; for examples). These neurobiological findings place important constraints on theories of symptom perception, which is evidently highly sensitive to prior expectations and contextual cues.…”

“…Examples of such symptoms include fatigue, inflammation-induced "malaise" and somatic input from stress-related HPA-axis activation. Imprecise prediction errors may also result from various types of interoceptive dysfunction that influence the quality and resolution of the somatic signals that eventually determine conscious symptom perception (Harshaw, 2015;Schulz and Vögele, 2015). For example, there is experimental evidence that both cytokines (Eisenberger et al, 2009;Harrison et al, 2009a,b) and stress/HPA-axis activation influence structural and/or functional characteristics of interoceptive brain areas (Stein et al, 2007;Liston et al, 2009;Gianaros et al, 2007).…”

“…Genderrelated differences in symptom appraisal, socialization processes and gender roles, as well as gender biases in research and clinical practices, may also account for some of the effect . However, two additional observations are important in this respect: First, in laboratory environments, women are consistently found to be less accurate than men at detecting physiological changes in, for example, heart rate, blood glucose, blood pressure, respiration, and gastrointestinal sensations (Pennebaker and Roberts, 1992;Roberts and Pennebaker, 1994), which may be due to gender-related structural and functional differences in the interoceptive network in the brain (Naliboff et al, 2003;Fairclough and Goodwin, 2007;Harshaw, 2015). Second, this laboratory difference in interoceptive accuracy disappears in natural environments, which may be related to women being more sensitive to contextual cues when determining their internal state (see Pennebaker and Roberts, 1992;Roberts and Pennebaker, 1994;Pennebaker, 1995).…”