Interoception Relates to Sleep and Sleep Disorders

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Interoception relates to sleep and sleep disorders

1 1,2,3

Yishul Wei and Eus JW Van Someren

The central nervous system senses and responds to afferent conﬁned to visceral sensations but has expanded to

signals arising from the body. These interoceptive afferents are encompass other sensory modalities that inform the

essential to physiological homeostatic control and are known CNS about the physiological states across the body, most

to inﬂuence an individual’s momentary affect, cognition, notably thermoception and nociception [1 ,2]. Intero-

motivation, and conscious experiences. Both sleep and ceptive information arising from body tissues is conveyed

interoception are tightly connected to physical and mental well- to the CNS via neural and humoral pathways as well as

being. This review outlines the current knowledge about the through indirect signaling involving immune cells and

interactions between interoception and sleep. It is neurovascular coupling [4,5]. Ascending neural pathways

demonstrated that there are complex, dynamic relations interface with the central autonomic network at multiple

between sleep and sensory processes within each modality of spinal and subcortical levels and ultimately deliver inter-

interoception, including thermoception, nociception, visceral oceptive information to the ‘neuromatrix’ within the

sensations, and subjective feelings about these sensations. A cerebral cortex [5,6]. Neuronal signaling along the path-

better understanding and appreciation of the intricate ways is subject to descending facilitation and inhibition

interrelations may facilitate management of functional somatic from the brain and modulated by assorted hormonal and

symptoms, chronic pain, insomnia, and other sleep and mental inﬂammatory factors [7]. Interoceptive sensitivity is thus

disorders. determined by not only the neuro-endocrino-immuno-

logical condition but also the affective, cognitive, moti-

Addresses vational, and arousal state of the individual.

Department of Sleep and Cognition, Netherlands Institute for

Neuroscience (NIN), an Institute of the Royal Netherlands Academy of

The aim of this review is to provide a synopsis of the

Arts and Sciences, Amsterdam, The Netherlands

Department of Integrative Neurophysiology, Center for Neurogenomics current knowledge about the interactions between

and Cognitive Research (CNCR), Amsterdam Neuroscience, VU sleep—which has prominent bidirectional relationship

University Amsterdam, Amsterdam, The Netherlands

with all of the mentioned factors [8,9]—and the intero-

Amsterdam UMC, Vrije Universiteit, Psychiatry, Amsterdam

ceptive systems. Both sleep and interoception are multi-

Neuroscience, Amsterdam, The Netherlands

dimensional constructs. For instance, subjective sleep

Corresponding author: Van Someren, Eus JW ([email protected]) quality and interoceptive feelings are often uncorrelated

with objective measures of sleep and interoception. Thus

far the relationship between each dimension of sleep and

Current Opinion in Behavioral Sciences 2019, 33:1–7

each dimension of interoception has not been equally

This review comes from a themed issue on Cognition and perception

investigated. The present review discusses the most

- *sleep and cognition*

representative themes in the current literature, including:

Edited by Michael Chee and Philippe Peigneux

impacts of interoception on sleep initiation, the roles of

interoception during sleep, impacts of sleep deprivation

on interoception, associations between interoception and

habitual sleep, and altered interoception in sleep disor-

https://doi.org/10.1016/j.cobeha.2019.11.008

ders (notably insomnia disorder).

2352-1546/ã 2019 The Authors. Published by Elsevier Ltd. This is an

open access article under the CC BY-NC-ND license (http://creative-

commons.org/licenses/by-nc-nd/4.0/).

Interoception affects sleep initiation

Noxious or stressful stimuli naturally increase arousal and

hinder sleep. In contrast, certain types of interoceptive

Introduction stimuli appear somnogenic. For example, gastrointestinal

Central nervous system (CNS) processing of bodily sig- stimulation has been shown to reduce sleep onset latency,

nals, broadly known as interoception, has become an mirroring the familiar phenomenon of postprandial sleep-

integral topic in the current discourse of affective, cogni-

iness [2,10]. It has also been observed in both animals and

tive, behavioral, social, and clinical neurosciences [1 anesthetized humans that carotid sinus stimulation

,2,3]. The notion of interoception was traditionally

Following the nomenclature recently proposed by the Human Affectome Project, we use the term interoceptive feelings to refer to subjective

experiences regarding body parts (or the body as a whole) that may derive from interoceptive afferents but may also integrate other sensory (e.g. tactile

[69]) information and may even originate within the CNS itself [1 ]. Interoceptive feelings can manifest as symptoms or complaints in clinical

settings.

www.sciencedirect.com Current Opinion in Behavioral Sciences 2020, 33:1–7

2 Cognition and perception - *sleep and cognition*

triggers EEG activity resembling slow waves that are sleep. However, it has been demonstrated that subtle skin

characteristic of sleep [2,11]. warming during sleep can promote SWS without chang-

ing core body temperature [17], thus supporting direct

The link between thermoception and the sleep–wake impacts of skin temperature on SWS expression.

behavior has attracted particularly widespread attention

[12,13 ,14]. Mild skin warming within the thermoneutral Studies on the nociceptive laser-evoked potential (LEP)

zone during wakefulness reduces vigilance and promotes and the heartbeat-evoked potential (HEP) during sleep

sleep onset [13 ], although the effect appears compro- have shown that cortical processing of interoceptive

mised in the elderly, likely due to the age-related decline information is present but attenuated as compared to

in thermosensitivity [15]. More intense heat as well as wakefulness [18,19]. Interestingly, the presence of a late

cold exposure at bedtime impedes sleep. However, body positive component of the LEP predicts a subsequent

heating a few hours before bedtime reduces sleep onset arousal, indicating that nociceptive input can elicit higher

latency and increases slow-wave sleep (SWS), colloquially order cognitive evaluation even during sleep [18].

known as the ‘warm bath effect’ and likely to involve a

cascade of thermoregulatory processes [14]. This shows The roles of interoception in dreams and rapid eye

that sleep propensity depends on both magnitudes and movement (REM) sleep are particularly elusive. Intero-

timing of the thermal stimuli. ceptive feelings in dreams are rare [1 ,18]. REM sleep is

characterized by apparently CNS-initiated autonomic

Based on these ﬁndings, an extension of the traditional swings with minimal interoceptive feedback control, giv-

two-process model of sleep has been proposed [14]. In the ing rise to erratic heart rate, blood pressure, and breathing

extended model, sleep propensity is not only determined patterns [8,11,12,16]. The HEP however indicates

by homeostatic sleep pressure and the circadian phase but increased cortical processing of cardiovascular input dur-

also dependent on sensory gating signals. An interesting ing REM sleep relative to non-REM sleep [19]. This

hypothesis is that sleep homeostasis may itself involve processing during REM sleep has been found to be

interoceptive mechanisms. For instance, sleep depriva- elevated in people with nightmare disorder—regardless

tion is known to elevate blood pressure and distal skin of whether a nightmare during the assessment night

temperature [11,13 ]. These changes could in turn be actually occurred [20]. Interoception, interoceptive feel-

picked up by carotid baroreceptors and skin thermore- ings, and autonomic output thus seem dissociated during

ceptors, generating feedback input that promotes sleepi- dreams and REM sleep.

ness. Likewise, the circadian component may itself also

involve interoceptive mechanisms, for example, through Sleep deprivation

the thermoregulatory effects of melatonin [13 ]. Acute or chronic sleep deprivation results in alterations in

interoceptive feelings. This is most clearly demonstrated

Interoception during sleep in the pain literature, where various sleep deprivation

Stable sleep is marked by profound suppression of various paradigms (e.g. total sleep deprivation, sleep restriction,

behavioral defense responses (e.g. hypoxic/hypercapnic SWS disruption, and sleep fragmentation) have been

ventilatory responses, coughing, swallowing, shivering, shown to increase sensitivity to painful stimuli as well

and withdrawal reﬂexes) against adverse conditions or as spontaneous pain [21]. An increase in somatic com-

stimuli, and occurrences of such responses typically plaints besides pain following sleep deprivation has also

involve arousals or awakenings [8,10,12,16]. In addition been reported [22]. More generally, the ‘feeling of sleep

to sleep-induced muscle hypotonia, changes associated deprivation’ that many readers are familiar with can be

with sleep within the sensory systems are believed to characterized by fatigue, negative mood, and an overall

contribute to suppression of these responses [8,12,16]. perception of unwellness [23], resembling in several

The changes in interoceptive sensitivity prevent arousals respects the feeling state of sickness [1 ,4,9]. Interest-

and protect sleep. Unfortunately, such mechanisms nec- ingly, a sleep-deprived person is indeed likely to be

essarily render body tissues vulnerable to adverse physi- judged as being sick by others [24].

ological conditions or events (e.g. gastroesophageal reﬂux

[10]), which could lead to severe clinical complications A recent study evaluated the effects of chronic sleep

should those events become frequent during sleep. restriction with intermittent weekend recovery sleep

for up to three weeks. Multiple measures tapping differ-

It has been shown that manipulation of ambient temper- ent pain-related processes were assessed. It was found

ature during sleep is able to alter the core body tempera- that the heat pain threshold is lowered by sleep restriction

ture rhythm as well as sleep architecture. As a result of the during the ﬁrst week but normalizes afterwards. In con-

use of insulating clothing and bedding, sleep is more trast, increased CNS cold pain facilitation and reduced

easily disturbed by heat than by cold exposure [12]. At cold pain habituation could only be observed in the later

present it is unclear whether alterations in skin tempera- weeks of sleep restriction [25 ]. The study highlights that

ture or in core body temperature exert more inﬂuences on the observed effects of acute sleep deprivation may not

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Sleep and interoception Wei and Van Someren 3

generalize to chronic sleep deprivation, as each type of medial orbitofrontal cortex being the common neural

sleep deprivation may differentially affect the multiple substrate.

processes involved in pain perception.

Investigating the intra-individual relationship between

Sleep deprivation may induce hyperalgesia through sev- ﬂuctuations in sleep and somatic complaints could pro-

eral neurochemical pathways including the opioid, mono- vide more mechanistic insights into their interactions.

amine, orexin, and endocannabinoid systems as well as Several studies in the pain literature, mostly carried out in

endocrine and immune mechanisms [26 ]. Neuroimag- patients with assorted somatic pain conditions, have

ing studies probing the brain substrates of sleep depriva- consistently pointed to sleep (assessed with daily self-

tion-induced changes in pain processing have just begun reports and sometimes with actigraphy) as a more reliable

to emerge. One recent study found ampliﬁed reactivity of predictor of subsequent pain than vice versa [39]. The

the primary somatosensory cortex and blunted reactivity same ‘microlongitudinal’ paradigm has also been applied

of the nucleus accumbens (NAcc), thalamus, and insula in to the study of irritable bowel syndrome, a functional

response to heat pain stimulation following a night of total gastrointestinal disorder characterized by hypersensitivity

sleep deprivation. Moreover, the sleep deprivation- [7]. It was found that poor self-reported sleep quality is

induced changes in reactivity of the primary somatosen- associated with next-day abdominal pain but not with

sory cortex and thalamus predict corresponding lowering non-pain gastrointestinal symptoms [40]. Therefore,

of the heat pain threshold [27]. Another study reported across heterogeneous conditions, it seems that the asso-

that a night of fragmented sleep attenuates and delays ciation between poor self-reported sleep and next-day

NAcc responses to heat pain stimulation [28]. Involve- pain is especially robust.

ment of the NAcc as implicated by both studies suggests

that processes related to affective valuation and cognitive A recent community-based study assessed how people

control are likely to be engaged in the relationship themselves perceive daytime pain to associate with sub-

between sleep and pain. sequent sleep and vice versa. Interestingly, the perceived

sleep–pain associations are asymmetric: Sleep worsens

more after a day with more-than-usual pain than it

Interoception covaries with habitual sleep improves after a day with less-than-usual pain. Also, pain

It is not uncommon to ﬁnd sleep disturbances to accom- worsens more after a night of worse-than-usual sleep than

pany somatic complaints. The experimental evidence it improves after a night of better-than-usual sleep. This

summarized above would imply bidirectional relations asymmetry becomes stronger in people with more severe

between somatic discomfort and poor sleep. Longitudinal habitual insomnia (Figure 1) or pain [35 ]. The study

studies have repeatedly shown that self-reported sleep highlights the possibility that the effects of better and

disturbances predict new-onset pain conditions and vice worse nights of sleep on pain are not of equal magnitudes,

versa [29]. Conversely, good sleep quality has been shown which could potentially explain why treatments targeting

to predict (partial) resolution of pain [30]. Pain however insomnia only marginally alleviate pain in patients with

does not seem to predict persistence versus remission of comorbid insomnia and chronic pain [41].

insomnia [31]. Longitudinal data for the bidirectional

relationship between poor sleep and somatic complaints Studies have also linked habitual sleep to laboratory test

besides pain are lacking, but cross-sectional data have results on interoceptive feelings. One seminal popula-

demonstrated robust associations between them across tion-based study found reduced cold pain tolerance in

different populations [32–34,35 ]. people reporting longer sleep onset latency, lower sleep

efﬁciency, and more severe and frequent insomnia [42].

A recent population-based study conducted in Japan In another study, healthy volunteers reporting more sleep

indicated that pain symptoms are more reliably associated difﬁculties were shown to perform worse on the intero-

with self-reported sleep insufﬁciency than with self- ceptive cardiac discrimination task. Surprisingly, the asso-

reported sleep duration per se [36]. This result is interest- ciation is reversed in people with affective disorders [43].

ing in light of a recent interventional study showing that

sleep extension beneﬁts (cold) pain tolerance, more so in Sleep disorders

people who report to habitually sleep less than needed Diagnosed sleep disorders are common among patients

[37]. In a neuroimaging study, reporting to habitually with chronic pain. The most prevalent comorbid sleep

sleep more than needed (termed ‘sleep credit’) was found disorder is insomnia disorder (ID). A recent meta-analysis

to be associated with increased gray matter volume in part estimated that the prevalence of comorbid ID among

of the medial orbitofrontal cortex, which is in turn patients with chronic pain is 72%, much higher than the

associated with less somatic complaints, depression, prevalence of comorbid restless legs syndrome (RLS,

and paranoia [38]. These converging ﬁndings suggest 32%) or obstructive sleep apnea (OSA, 32%) [44 ]. Nota-

that subjective sleep insufﬁciency is an especially impor- bly, laboratory quantitative sensory testing has conﬁrmed

tant factor involved in somatic complaints, with the increased pain sensitivity and implicated altered CNS

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4 Cognition and perception - *sleep and cognition*

Figure 1

Sleep Pain Pain Sleep More Pain 1 Better Sleep 1 After Worse Sleep After More Pain After Better Sleep After Less Pain

0.5 0.5

Pain Sleep 0 0 As Usual As Usual

–0.5 –0.5

Less Pain –1 Worse Sleep –1

0–7 8–14 15–21 22–28 0–7 8–14 15–21 22–28 Insomnia Severity Index Insomnia Severity Index

Current Opinion in Behavioral Sciences

Average perceived pain after a better night and worse night of sleep than usual (left), and average perceived sleep quality after a day with more

pain and less pain than usual (right), within subgroups of individuals defined by clinical cutoffs of the Insomnia Severity Index. Error bars indicate

95% confidence intervals. Reprinted from Ref. [35 ].

pain facilitation and/or inhibition in ID, RLS, and OSA Resting-State Questionnaire (ARSQ) [52] including

[29]. Chronic pain is also highly prevalent among patients reduced comfort, heightened health concern, height-

with narcolepsy [45]. ented subjective sleepiness, and heightened somatic

awareness as compared to healthy controls [53]. Reduced

Etiological theories of ID hypothesize that attention to comfort in people with ID is further corroborated by their

selective interoceptive or exteroceptive stimuli together deﬁcient ‘liking’ feelings throughout the day [54]. A

with other cognitive activities could lead to a hyperarousal detailed analysis of many dimensions of subjective ther-

state at bedtime that interferes with sleep initiation or moception also revealed a very different proﬁle between

maintenance [46,47]. Somatic discomfort around bedtime people with probable ID and people without sleep com-

can be assessed with the Pre-Sleep Arousal Scale— plaints [55].

Somatic subscale [48], which has indeed been found to

distinguish between people with ID, subclinical poor Strong differences between people with ID and people

sleepers, and normal sleepers and to independently con- without sleep complaints are also reﬂected in an objective

tribute to self-reported nocturnal wake time and poor measure of interoception. The later part of the frontal

sleep quality [49]. Some studies, however, suggested that HEP is enhanced in people with ID during wakeful rest

insomnia symptoms are more closely related to pre-sleep in the evening, suggesting increased processing of cardiac

cognitive activities than to pre-sleep somatic discomfort signals [56] (Figure 2a). In a follow-up study, it was found

[48,50]. It has been proposed instead that perhaps arousal- that mean EEG microstate duration speciﬁcally for micro-

promoting interoceptive input at bedtime is not maxi- state class C is shortened in people with ID [57]

mally consciously recognized by people with ID [51]. (Figure 2b). As duration of class C microstates has been

shown to negatively correlate with the somatic awareness

Altered interoceptive feelings in ID beyond the pre-sleep dimension of the ARSQ [52], this microstate alteration

period have also been demonstrated. During wakeful rest, could be a marker of heightened somatic awareness in ID.

people with ID report aberrant spontaneous mental con-

tent along several dimensions assessed by the Amsterdam

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Sleep and interoception Wei and Van Someren 5

Figure 2 (a) (b) 120 ID ID CTRL CTRL 0.3

100 0.2

0.1

V) 80 µ

HEP Amplitude HEP ( 60 -0.1 Mean Microstate Duration (ms)

-0.2 40

-0.3

-300 -200 -100 0 100 200 300 400 500 600 A B C D E Time (ms) Microstate Class

Current Opinion in Behavioral Sciences

(a) Frontal heartbeat-evoked potential (HEP) waveforms in 32 people with insomnia disorder (ID) and 32 healthy controls (CTRL) during wakeful

rest in the evening with eyes closed. The average time courses over the frontal and prefrontal electrodes (large black dots) time-locked to the R-

wave peak (0 ms) are depicted. Shaded areas indicate one standard error of the mean (SEM). Adapted from Ref. [56]. (b) Boxplots of mean EEG

microstate duration for each microstate class in the same groups of people with ID and CTRL during wakeful rest in the evening with eyes closed.

Data are obtained from Ref. [57]. Asterisks indicate significant group differences ( p < 0.05).

In sum, it is important to note an unfortunate disbalance. perception speciﬁcally of large ﬁber-mediated afferents at

While people with ID show increased interoceptive the soft palate [66]. In comparison, others applying the

awareness across modalities, they are actually less likely same method to the toes showed reduced current per-

to either sense comfort or to label experiences as com- ception thresholds in people with RLS for both large

fortable or pleasant [51,53–55]. Neuroimaging studies ﬁber-mediated and small ﬁber-mediated afferents during

have commenced to ﬁnd neural correlates of this disba- the symptomatic period [67]. Because participants with

lance and suggested that increased reactivity may relate abnormal test results indicative of peripheral neuropathy

to hyperconnectivity of the angular gyrus while deﬁcient were excluded, the authors concluded that CNS mecha-

comfort sensing likely involves suboptimal orbitofrontal nisms are likely to underlie hyperesthesia in RLS, a

processing [58,59]. The disbalance toward negative conclusion also corroborated by earlier studies using other

experiences may have long-standing consequences, as methodologies [68].

recent studies have found that the affective signatures

of negative emotional experiences could persist through Conclusion

extinction learning, across the night, and over the long To our knowledge, this is the ﬁrst review that attempts to

term in people with ID [60–63]. synthesize the vast literature on the links between sleep

and sensory processing across a wide range of interocep-

With respect to sleep disorders other than ID, accumu- tive modalities. The state of science has really only

lating evidence suggests that OSA is associated with scratched the surface of their complex, dynamic interac-

impaired mechano- and thermosensitivity of the upper tions. We hope that our synopsis has presented a coherent

airway resulting from local neuropathy [64,65]. A recent account of their intricate relationship and will inspire

study systematically examined the functional integrity of innovative future research on this important topic.

afferent neural pathways from the palate by means of

electrical stimulation with alternating currents at differ- Conﬂict of interest statement

ent frequencies and found in patients with OSA impaired Nothing declared.

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6 Cognition and perception - *sleep and cognition*

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