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Journal ArticleDOI

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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Citations
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Journal ArticleDOI
01 Dec 2013-Pain
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


Additional excerpts

  • ...—Claude Bernard...

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Journal ArticleDOI
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

Journal ArticleDOI
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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Journal ArticleDOI
01 Feb 2017-Medicine
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

Journal ArticleDOI
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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Journal ArticleDOI
01 Oct 1977-Pain
TL;DR: Long-term results suggest that a multidisciplinary approach can offer an effective means of treating chronic low-back pain.
Abstract: Thirty-six p tients with low-back pain who had been treated in our multidisciplinary pain center returned for 80-week follow-up evaluations by the staff psychologist, physiatrist and physical therapist. Statistically significant gains were maintained in the reduction of prescription analgesics and on 4 measures of physical functioning 1. (a) long-sitting-to-toe 2. (b) straight-legraise 3. (c) knee-to-chest 4. (d) overall exercise performance. Despite verbal reports of continuing pain, most patients claimed they were coping much better with it, and they displayed a marked reduction in their utilization of medical resources for further pain treatment. These long-term results suggest that a multidisciplinary approach can offer an effective means of treating chronic low-back pain.

96 citations

Journal ArticleDOI
01 Aug 2004-Pain
TL;DR: The data suggest that pain during sleep could trigger a sleep awaking response over all sleep stages and not only in light sleep.
Abstract: The literature on sensory perception during sleep suggests that light sleep (Stage 2) is more responsive to external sensory stimulation (e.g. sound, electrical shock) than deep sleep (Stages 3 and 4) and REM sleep. The main objective of this study was to characterize the specificity of nociceptive stimulation to trigger sleep arousal-awakening over all sleep stages. Thirteen healthy adults (e.g. without pain or sleep problems; six female and seven male of a mean age of 24.2+/-1.3 years) were included in the study. The responses to noxious intramuscular 5% hypertonic infusion were compared to innocuous vibrotactile and to respective control stimulations: isotonic infusion and auditory stimulations. These stimulations were applied during wakefulness and were repeated during sleep. Polygraphic signals (e.g. brain activity, heart rate) signals were recorded to score sleep arousal over all sleep stages. A subjective assessment of sleep quality was made on next morning. No overnight sensitization or habituation occurred with any of the experimental stimulations. The vibratory-auditory stimulations and the noxious hypertonic infusions triggered significantly (P < 0.05) more awakenings in sleep Stage 2 and in REM than their respective control stimulations. In sleep Stage 2, both vibratory + auditory stimulations and the noxious hypertonic infusions has the same awakening response frequency (approximately 30%), however, with the noxious infusions the response frequency were similar in sleep Stages 3 and 4 (P < 0.05) and in REM (trend). Compared to the baseline night, sleep quality was lower following the night with noxious stimulation (90.1+/-2.7 and 73.3+/-7.4 mm, respectively; P < 0.03. These data suggest that pain during sleep could trigger a sleep awaking response over all sleep stages and not only in light sleep.

93 citations


Additional excerpts

  • ...These pain threshold values were within the normal r 2640 r range of our laboratory and those reported by others using Nd:YAP lasers [Leandri et al., 2006; Perchet et al., 2008; Truini et al., 2007]....

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Journal ArticleDOI
TL;DR: Earlier latencies and larger amplitudes recorded when using Nd:YAP pulses suggest a more synchronized nociceptive afferent volley with this type of laser, which may favour the use of Nd?:YAP lasers in clinical settings.

77 citations


"Filtering the reality: Functional d..." refers result in this paper

  • ...Furthermore, the nociceptive thresholds obtained in our patients were strictly comparable to those previously reported in age-matched healthy subjects studied in our laboratory [Bastuji et al., 2008; Perchet et al., 2008]....

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  • ...Furthermore, no difference was observed between patients and normal controls as regards sleep organization and pain thresholds, the latter being similar in the sides ipsilateral and contralateral to the epileptic focus, and comparable to those of control subjects [Perchet et al., 2008]....

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  • ...These pain threshold values were within the normal r 2640 r range of our laboratory and those reported by others using Nd:YAP lasers [Leandri et al., 2006; Perchet et al., 2008; Truini et al., 2007]....

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  • ...range of our laboratory and those reported by others using Nd:YAP lasers [Leandri et al., 2006; Perchet et al., 2008; Truini et al., 2007]....

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Journal ArticleDOI
01 Jan 2005-Pain
TL;DR: The results show that the VP is definitely involved in thermo‐algesic transmission in man, and that its selective lesion can lead to central pain, but also suggest that much of the spino‐thalamo‐cortical volley elicited by painful heat stimuli does not transit through VP, supporting the hypothesis that a non‐VP locus lying more posteriorly in the human thalamus is important for thermo-algesics transmission.
Abstract: The respective roles of the ventral posterior complex (VP) and of the more recently described VMpo (posterior part of the ventral medial nucleus) as thalamic relays for pain and temperature pathways have recently been the subject of controversy. Data we obtained in one patient after a limited left thalamic infarct bring some new insights into this debate. This patient presented sudden right-sided hypesthesia for both lemniscal (touch, vibration, joint position) and spinothalamic (pain and temperature) modalities. He subsequently developed right-sided central pain with allodynia. Projection of 3D magnetic resonance images onto a human thalamic atlas revealed a lesion involving the anterior two thirds of the ventral posterior lateral nucleus (VPL) and, to a lesser extent, the ventral posterior medial (VPM) and inferior (VPI) nuclei. Conversely, the lesion did not extend posterior and ventral enough to concern the putative location of the spinothalamic-afferented nucleus VMpo. Neurophysiological studies showed a marked reduction (67%) of cortical responses depending on dorsal column-lemniscal transmission, while spinothalamic-specific, CO2-laser induced cortical responses were only moderately attenuated (33%). Our results show that the VP is definitely involved in thermo-algesic transmission in man, and that its selective lesion can lead to central pain. However, results also suggest that much of the spino-thalamo-cortical volley elicited by painful heat stimuli does not transit through VP, supporting the hypothesis that a non-VP locus lying more posteriorly in the human thalamus is important for thermo-algesic transmission.

69 citations


"Filtering the reality: Functional d..." refers background in this paper

  • ...…and posterior part of the ventral medial nucleus (VMpo) [Augustine, 1996; Craig et al., 1994; Freidman and Murray, 1986; Kobayashi et al., 2009; Montes et al., 2005; Stevens et al., 1993], whereas the cingulate cortex (Brodmann’ area 24) receives direct projections from midline and…...

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Journal ArticleDOI
TL;DR: Electrophysiological evidence is provided indicating that selective information processing corresponding to sensory discrimination of auditory stimuli is actively performed in stage 1 of NREM sleep and REM sleep.

69 citations


"Filtering the reality: Functional d..." refers background in this paper

  • ...This phenomenon has been reported in scalp responses to a variety of stimuli including auditory tones [Bastuji et al., 1995; Niiyama et al., 1994] and proper names [Perrin et al....

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  • ...This phenomenon has been reported in scalp responses to a variety of stimuli including auditory tones [Bastuji et al., 1995; Niiyama et al., 1994] and proper names [Perrin et al., 1999]....

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