Filtering the reality: Functional dissociation of lateral and medial pain systems during sleep in humans
TL;DR: While the lateral operculo‐insular system subserving sensory analysis of somatic stimuli remained active during paradoxical‐REM sleep, mid‐anterior cingulate processes related to orienting and avoidance behavior were suppressed, explaining why nociceptive stimuli can be either neglected or incorporated into dreams without awakening the subject.
Abstract: Behavioral reactions to sensory stimuli during sleep are scarce despite preservation of sizeable cortical responses. To further understand such dissociation, we recorded intracortical field potentials to painful laser pulses in humans during waking and all-night sleep. Recordings were obtained from the three cortical structures receiving 95% of the spinothalamic cortical input in primates, namely the parietal operculum, posterior insula, and mid-anterior cingulate cortex. The dynamics of responses during sleep differed among cortical sites. In sleep Stage 2, evoked potential amplitudes were similarly attenuated relative to waking in all three cortical regions. During paradoxical, or rapid eye movements (REM), sleep, opercular and insular potentials remained stable in comparison with Stage 2, whereas the responses from mid-anterior cingulate abated drastically, and decreasing below background noise in half of the subjects. Thus, while the lateral operculo-insular system subserving sensory analysis of somatic stimuli remained active during paradoxical-REM sleep, mid-anterior cingulate processes related to orienting and avoidance behavior were suppressed. Dissociation between sensory and orienting-motor networks might explain why nociceptive stimuli can be either neglected or incorporated into dreams without awakening the subject.
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TL;DR: The pain matrix is conceptualised here as a fluid system composed of several interacting networks, including posterior parietal, prefrontal and anterior insular areas, which ensures the bodily specificity of pain and is the only one whose destruction entails selective pain deficits.
Abstract: The pain matrix is conceptualised here as a fluid system composed of several interacting networks. A nociceptive matrix receiving spinothalamic projections (mainly posterior operculoinsular areas) ensures the bodily specificity of pain and is the only one whose destruction entails selective pain deficits. Transition from cortical nociception to conscious pain relies on a second-order network, including posterior parietal, prefrontal and anterior insular areas. Second-order regions are not nociceptive-specific; focal stimulation does not evoke pain, and focal destruction does not produce analgesia, but their joint activation is necessary for conscious perception, attentional modulation and control of vegetative reactions. The ensuing pain experience can still be modified as a function of beliefs, emotions and expectations through activity of third-order areas, including the orbitofrontal and perigenual/limbic networks. The pain we remember results from continuous interaction of these subsystems, and substantial changes in the pain experience can be achieved by acting on each of them. Neuropathic pain (NP) is associated with changes in each of these levels of integration. The most robust abnormality in NP is a functional depression of thalamic activity, reversible with therapeutic manoeuvres and associated with rhythmic neural bursting. Neuropathic allodynia has been associated with enhancement of ipsilateral over contralateral insular activation and lack of reactivity in orbitofrontal/perigenual areas. Although lack of response of perigenual cortices may be an epiphenomenon of chronic pain, the enhancement of ipsilateral activity may reflect disinhibition of ipsilateral spinothalamic pathways due to depression of their contralateral counterpart. This in turn may bias perceptual networks and contribute to the subjective painful experience.
370 citations
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...—Claude Bernard...
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TL;DR: It is contended that even in unconscious subjects, repeated limbic and vegetative activation by painful stimuli via spino‐amygdalar pathways can generate implicit memory traces and stimulus‐response abnormal sequences, possibly contributing to long‐standing anxiety or hyperalgesic syndromes in patients surviving coma.
Abstract: The aversive experience we call "pain" results from the coordinated activation of multiple brain areas, commonly described as a "pain matrix". This is not a fixed arrangement of structures but rather a fluid system composed of several interacting networks: A 'nociceptive matrix' includes regions receiving input from ascending nociceptive systems, and ensures the bodily characteristics of physical pain. A further set of structures receiving secondary input supports the 'salience' attributes of noxious stimuli, triggers top-down cognitive controls, and -most importantly- ensures the passage from pre-conscious nociception to conscious pain. Expectations and beliefs can still modulate the conscious experience via activity in supramodal regions with widespread cortical projections such as the ventral tegmental area. Intracortical EEG responses in humans show that nociceptive cortical processing is initiated in parallel in sensory, motor and limbic areas; it progresses rapidly to the recruitment of anterior insular and fronto-parietal networks, and finally to the activation of perigenual, posterior cingulate and hippocampal structures. Functional connectivity between sensory and high-level networks increases during the first second post-stimulus, which may be determinant for access to consciousness. A model is described, progressing from unconscious sensori-motor and limbic processing of spinothalamic and spino-parabrachial input, to an immediate sense of awareness supported by coordinated activity in sensorimotor and fronto-parieto-insular networks, and leading to full declarative consciousness through integration with autobiographical memories and self-awareness, involving posterior cingulate and medial temporal areas. This complete sequence is only present during full vigilance states. We contend, however, that even in unconscious subjects, repeated limbic and vegetative activation by painful stimuli via spino-amygdalar pathways can generate implicit memory traces and stimulus-response abnormal sequences, possibly contributing to long-standing anxiety or hyperalgesic syndromes in patients surviving coma.
82 citations
TL;DR: The results suggest that the human cortex does not shift from sleep to wake in an abrupt binary way, and stereotyped arousals at the thalamic level seem to be associated with different patterns of cortical arousals due to various regulation factors.
65 citations
Cites background from "Filtering the reality: Functional d..."
...Laser stimulation protocol is detailed in Bastuji et al. (2012)....
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...…impossible to explore with scalp EEG, intra-cerebral recordings performed in epileptic patients have proved to be useful in many electrophysiological sleep studies (Nobili et al., 2011; Sarasso et al., 2014; Bastuji et al., 2012; Magnin et al., 2004; Nir et al., 2011; Peter-Derex et al., 2012)....
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TL;DR: Examining the multidimensional construct of pain in concussion/mTBI through a sex lens garners new directions for future longitudinal research on the pain mechanisms involved in postconcussion syndrome.
35 citations
TL;DR: This patient exhibited finger lifts in response to stimulations delivered during paradoxical (REM) sleep, suggesting that during PS, not only the processing of sensory inputs but also the capacity for the sleeper to intentionally indicate his perception could be preserved under particular circumstances is suggested.
Abstract: Sleep disruption by painful stimuli is frequently observed both in clinical and experimental conditions. Nociceptive stimuli produce significantly more arousals (30% of stimuli) than non-nociceptive ones. However, even if they do not interrupt sleep, they can trigger a variety of other reactions. Reflex behaviours in response to nociceptive stimuli can be observed during all sleep stages, and are more likely to occur in association with an arousal than alone. Cardiac activation represents a robust sympathetically driven effect preserved whatever the state of vigilance, even if its magnitude can be modulated by a concomitant cortical arousal. Not withstanding these reactions, incorporation of nociceptive stimuli into dream content remains limited. At cortical level, laser-evoked potential studies demonstrate that the processing of nociceptive stimulations is partly conserved during all sleep stages. Furthermore, when nociceptive stimulations interrupt sleep, the cortical response presents a late component suggesting that the stimulation has to be cognitively processed in order to produce a subsequent arousal. More complex reactions to nociceptive stimulations were occasionally reported. In this context, an epileptic patient with intracerebral electrodes implanted for therapeutic purposes allowed us extending these observations. This patient exhibited finger lifts in response to stimulations delivered during paradoxical (REM) sleep. This motor reaction was previously used during wakefulness to indicate that the stimulation had been perceived. When these finger lifts occurred a systematic re-activation of the anterior cingulate preceded each movement. This observation suggests that during PS, not only the processing of sensory inputs but also the capacity for the sleeper to intentionally indicate his perception could be preserved under particular circumstances.
22 citations
References
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TL;DR: The results suggest that the sympathetic‐dependent cardiac activation induced by nociceptive stimuli is modulated by a sleep dependent phenomenon related to cortical activation and not by sleep itself, since it reaches a same intensity whatever the state of vigilance.
39 citations
TL;DR: It is suggested that pain dreams do occur at a greater frequency in suffering populations than in normal volunteers and dreaming about pain may be an added stress for burn patents and may contribute to both poor sleep and higher pain intensity, which could evolve into a cycle of pain-anxiety-sleeplessness.
Abstract: It has been shown that realistic, localized painful sensations can be experienced in dreams either through direct incorporation or from past memories of pain. Nevertheless, the frequency of pain dreams in healthy subjects is low. This prospective study was designed to evaluate the occurrence and frequency of pain in the dreams of patients suffering from burn pain. Twenty-eight nonventilated burn victims were interviewed for 5 consecutive mornings during the first week of hospitalization. A structured-interview protocol was used to collect information on dream content, quality of sleep, and pain intensity and location. Patients were also administered the Impact of Event Scale to assess posttraumatic symptoms. Thirty-nine percent of patients reported 19 pain dreams on a total of 63 dreams (30%). Patients with pain dreams showed evidence of worse sleep, more nightmares, higher intake of anxiolytic medication, and higher scores on the Impact of Event Scale than did patents reporting dreams with no pain content. Moreover, patients with pain dreams also had a tendency to report more intense pain during therapeutic procedures. Although more than half of our sample did not report pain dreams, these results suggest that pain dreams do occur at a greater frequency in suffering populations than in normal volunteers. More importantly, dreaming about pain may be an added stress for burn patents and may contribute to both poor sleep and higher pain intensity, which could evolve into a cycle of pain-anxiety-sleeplessness.
38 citations
Journal Article•
TL;DR: The increasing recognition of the coexistence of fibromyalgia, myofascial pain in the head and neck region, and the presence of temporomandibular disorders further increases the need for the dentist to be aware of sleep as a contributory factor from the diagnostic and the therapeutic aspects.
34 citations
TL;DR: PGB has efficacy of pre-emptive analgesia on pathological pain associated with central sensitization in isoflurane-anesthetized intact and spinalized rats, suggesting that PGB-induced selective antinociceptive effect on C-fiber mediated nociception is mainly central effects involving supraspinal centers via descending inhibitory controls.
28 citations
"Filtering the reality: Functional d..." refers background in this paper
...…including pregabalin and oxcarbazepine, may attenuate acute nociceptive neuronal and behavioral responses in animal pain models [Tomic et al., 2010; You et al., 2009], and have analgesic effects on chronic neuropathic pain, but there is no clinical evidence of their effectiveness in clinical acute…...
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...Some antiepileptic drugs, including pregabalin and oxcarbazepine, may attenuate acute nociceptive neuronal and behavioral responses in animal pain models [Tomic et al., 2010; You et al., 2009], and have analgesic effects on chronic neuropathic pain, but there is no clinical evidence of their effectiveness in clinical acute pain [e....
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TL;DR: The data indicate that central mechanisms of alerting function in sleep states as well as in W and suggest that CLE and PGOE reflect activity in mechanisms underlying cortical desynchronization and visual processes which may act in concert during alerting.
27 citations
"Filtering the reality: Functional d..." refers background in this paper
...consistent with their role in motor withdrawal, as motor reactions to external sensory input are scarce during this vigilance stage [Morrison et al., 1995; Rechtschaffen et al., 1966; Sanford et al., 1992]....
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...W: waking; S2: Stage 2; PS: paradoxical sleep. r 2643 r consistent with their role in motor withdrawal, as motor reactions to external sensory input are scarce during this vigilance stage [Morrison et al., 1995; Rechtschaffen et al., 1966; Sanford et al., 1992]....
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