|Frederike Hermi Petzschner et al. (2022), Scholarpedia, 17(5):55569.||doi:10.4249/scholarpedia.55569||revision #197497 [link to/cite this article]|
Interoception is the sense of the body's internal physiological variables, their integration and interpretation. It is implicated in homeostasis and allostasis, as well as in emotional and self-related processes.
Sherrington introduced the term interoceptive to refer to internal sensing, which he distinguished from external sensing and muscle proprioception (Sherrington, 1907). A more recent definition describes interoception as “the overall process of how the nervous system (central and autonomic) senses, interprets and integrates signals originating from within the body, providing a moment-by-moment mapping of the internal landscape of the body across conscious and nonconscious levels.” (Berntson & Khalsa, 2021, Khalsa et al., 2018). These internal signals reflect physiological parameters, such as bodily temperature or the contents, distention and movement of visceral organs, including blood composition and blood pressure.
There are unresolved issues regarding the boundaries of interoception, regarding for instance the inclusion or not of proprioception. Another issue is whether one should consider a sharp boundary, or rather a gradient, between what is internal or external. Discrepancies between authors reflect whether interoception is operationalized according to transducer location, anatomical pathways to the central nervous system, or functional role of the inputs.
Variety of input signals and pathways
Interoceptive information, resulting from the activity of mechanoreceptors, thermoceptors, or chemoceptors, is conveyed via several different pathways. Neural pathways (via unmyelinated (C) or thin (Að) sensory fibres) predominantly travel to the brain via cranial nerves, notably the Vagus Nerve, and via spinal pathways (Berntson & Khalsa, 2021). Humoral information reflecting the chemical composition of blood can also be detected directly by the brain notably via either specialised circumventricular organs or through transport across the blood brain barrier. In addition, the brain may sample its immediate environment, for example, neurons in the preoptic hypothalamus sense local temperature (Tan & Knight, 2018). Inputs may also arise from sensors outside the typical interoceptive domain, e.g. the transduction of respiration via pressure receptors in the nose (Grosmaitre et al., 2007) or the detection of heartbeats by somatosensory pathways (Khalsa et al., 2009, Bishop, 1983, Azzalini et al., 2019).
As compared to exteroception, detailed mechanisms of transduction and anatomo-functional pathways are less well known, notably because they are more difficult to measure experimentally. Finally, signal transduction in interoception occurs on a wider spectrum of time scales, from milliseconds (heartbeat) to several minutes (osmolarity) up to hours (nutrients).
Interoception informs the brain about bodily states, thereby providing the basis for appropriate action selection to regulate these states (Dworkin, 1993). Regulation of bodily states comes in two forms: reactive control (homeostasis) or prospective control (allostasis) (Sterling, 2014). Reactive control occurs when a physiological variable deviates from a normal set range, e.g. sweating in the heat. Prospective control refers to actions that are taken in anticipation of a homeostatic challenge, e.g. increasing the heart rate before running.
Reward and Motivation
Interoceptive states also underpin the determination of rewards and preferences. For instance, depending on the internal state, foods might be considered to be rewarding or aversive (Small et al., 2001). In addition, the willingness or motivation to exert effort to obtain a reward depends on the internal homeostatic need, e.g. increased drive for salty over sweet foods during a state of low osmolarity (Cone et al., 2016), or the amount of energy available to an organism.
Learning and Memory
Interoceptive signals can also promote learning and memory function. For instance, both neural (via the vagus nerve) and endocrine (e.g., hormones that fluctuate with energy status) signalling from the gut to the brain enhances learning and memory function, whereas interference with these signalling pathways has the opposite effect (Suarez et al., 2019).
Interoceptive states are also related to emotions since both subjective emotional feelings and objective behavioural expression of emotions are typically coupled with a change in physiological state (Feldman Barrett, 2018, Damasio, 2004). The directionality of the link between interoception and emotion has long been debated (Cannon, 1927): emotions could drive bodily changes or be a consequence of those bodily changes. In fact, the debate has revealed that there are likely to be two-way, even circular interactions.
Self and Consciousness
The constant (conscious or unconscious) monitoring of interoceptive states by the brain has also been proposed to be a basis for a basic form of self—the organism which needs to be fed, regulated and protected (Damasio, 2010). Consciousness, defined as the ability to have subjective experiences, presupposes the existence of an experiencer, which might be related to the basic interoceptive self (Park & Tallon-Baudry, 2014). There is now some experimental evidence that the neural representation of interoceptive (and proprioceptive) variables contributes to consciousness (Azzalini et al., 2019, Seth & Tsakiris, 2018).
In addition, bodily cycles, such as the cardiac or respiratory cycles, affect the perception-cognition-action loop - for instance, a visual or auditory stimulus may not be perceived in the same way at the beginning or at the end of the cardiac cycle (Garfinkel & Critchley, 2016). We have increasing experimental evidence for such interactions across different physiological axes. However, the nature of the link between e.g. the cardiac or respiratory cycle and perception, action and cognition remains to be fully elucidated.
Interoceptive information from the body is conveyed neurally via sensory afferents that travel to the brain via cranial nerves (notably vagus (X) and glossopharyngeal (IX) nerves) and via spinothalamic tracts (Craig, 2009). Interoceptive information primarily targets the brainstem Nucleus of the Solitary Tract (NTS), or directly the thalamus.
In addition, humoral information can be conveyed through transport across the blood brain barrier or detected directly by the brain’s circumventricular organs that carry chemoreceptors sensitive to osmotic, metabolic, and inflammatory status with reciprocal connections to the NTS and hypothalamus (Siso, 2010).
Interoceptive information from the NTS projects through (mainly ventroposterior) medial thalamus to cortex, branching to synapse within pons and midbrain (e.g. parabrachial nucleus, locus coeruleus, hypothalamus) to influence neuromodulatory pathways and subcortical substrates of motivational behaviour (Berntson & Khalsa, 2021).
While there is a fairly good representation of these connections up until the brainstem there are several knowledge gaps with respect to the neural basis of interoceptive information processing beyond that. Several cortical areas have been associated with the (multi-)sensory representation and control of bodily states, including but not limited to, the insula, the somato-sensory cortex, the anterior cingulate cortex and subcortical areas, including the hypothalamus, hippocampus, amygdala and the basal ganglia (Dum et al., 2009). Tracing studies between the periphery and cortex are beginning to bridge this gap (Han et al., 2018).
How interoception is measured depends on the interoceptive domains (e.g, cardiac, thermal, gastric). Still, there are a number of challenges common to all domains. First, it is more difficult to manipulate interoceptive signals (e.g. timing and strength of heartbeats) than exteroceptive stimuli (e.g. light intensity) because interoceptive signals are endogenously produced, and cannot always be easily titrated. Second, any manipulation (e.g. exercise) is likely to have multiple consequences at different levels of the system (afferent, integrative, efferent). Third, interoceptive processing is often delayed, with responses occurring within milliseconds up to several hours depending on the system or intervention (e.g. food intake).
Interoceptive measures can be roughly divided into objective vs. subjective as well as direct vs. indirect measures. Subjective measures typically entail asking a (most often human) subject to rate how he or she perceives an interoceptive stimulus or state (e.g., heartbeat tracking, feeling of thirst), or questionnaires about everyday life interoceptive feelings. Objective measures are peripheral (e.g. sweat produced in response to a thermal stimulation), neural (e.g. amplitude of the heartbeat evoked response) or behavioral (e.g. the number of licks in liquid-deprived animals). While all the above are examples of direct measures, there are also indirect measures, such as response time differences as a function of the cardiac cycle phase or changes in choice preferences for more salty liquids during states of low osmolarity.
Disorders related to interoception can arise from misperception or misrepresentation of interoceptive states. Such misrepresentation can in turn lead to altered motivational or emotional states, or to downstream changes in the regulation of the body which can result in states of chronic dyshomeostasis (Khalsa et al., 2018, Petzschner et al., 2017).
Anxiety and Panic Disorders
Humans with anxiety and panic disorders express threat-related bodily arousal responses and are associated with exaggerated interoceptive attention and often a misinterpretation of the meaning of interoceptive sensations, e.g. catastrophizing about heart rate acceleration.
Food intake is guided by the perception and discrimination of interoceptive sensations of hunger and satiety, by unconscious hormonal communication, and by subliminal reinforcing signals that are generated in the periphery (gastrointestinal tract and hepatoportal system) during nutrient digestion to directly regulate central dopamine circuits. Consequently, perturbation of these processes can underlie or maintain eating disorders, including obesity and anorexia nervosa.
In addition, interoceptive dysfunction is proposed to contribute to the etiology and maintenance of stress-sensitive medical disorders (e.g. irritable bowel syndrome, chronic pain and fatigue syndromes), functional neurological conditions (e.g. non-epileptic attacks or functional movement disorder), mood disorders (e.g. depression) and psychiatric symptoms (e.g. disturbances of conscious experience).
Despite taking its roots in Sherrington’s work in 1907, the scientific study of interoception is relatively young and has burgeoned in the last 10-20 years, yielding more questions than definite answers. Here, we list a few:
- What are the optimal approaches for quantifying perceptual processing of interoceptive information across functional axes (e.g. cardiac, respiratory, gastric)?
- Is interoception a unified system (as the visual, or the auditory system) or should it be decomposed by organs or functions?
- Is there a (cortical) representation of an integrated interoceptive state, or distributed coding?
- What are the mechanisms underlying top-down bodily regulation?
- What is the role of non-neuronal structures and cell types in interoception?
- What is the developmental trajectory of interoception? Is there maternal interoception of the foetus?
- What is the link between interoception and emotion?
- What is the link between interoception and the self?
- How does interoception influence exteroception, and conversely?
- What are the boundaries of interoception - are they determined anatomically, functionally?
- What is the link between interoception and chronic diseases, like cancer?
- How does the brain sense the amount of energy that is available for effort?
- How to measure interoception from behavior?
This article was supported by the Interoception Research Network, an NIH/NCI-organized workgroup on interoception.
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