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Journal ArticleDOI

Filtering the reality: Functional dissociation of lateral and medial pain systems during sleep in humans

01 Nov 2012-Human Brain Mapping (Hum Brain Mapp)-Vol. 33, Iss: 11, pp 2638-2649

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.

AbstractBehavioral 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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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.

300 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.

56 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.
Abstract: Wakefulness, non-rapid eye movement (NREM), and rapid eye movement (REM) sleep are characterized by specific brain activities. However, recent experimental findings as well as various clinical conditions (parasomnia, sleep inertia) have revealed the presence of transitional states. Brief intrusions of wakefulness into sleep, namely, arousals, appear as relevant phenomena to characterize how brain commutes from sleep to wakefulness. Using intra-cerebral recordings in 8 drug-resistant epileptic patients, we analyzed electroencephalographic (EEG) activity during spontaneous or nociceptive-induced arousals in NREM and REM sleep. Wavelet spectral analyses were performed to compare EEG signals during arousals, sleep, and wakefulness, simultaneously in the thalamus, and primary, associative, or high-order cortical areas. We observed that 1) thalamic activity during arousals is stereotyped and its spectral composition corresponds to a state in-between wakefulness and sleep; 2) patterns of cortical activity during arousals are heterogeneous, their manifold spectral composition being related to several factors such as sleep stages, cortical areas, arousal modality (“spontaneous” vs nociceptive-induced), and homeostasis; 3) spectral compositions of EEG signals during arousal and wakefulness differ from each other. Thus, stereotyped arousals at the thalamic level seem to be associated with different patterns of cortical arousals due to various regulation factors. These results suggest that the human cortex does not shift from sleep to wake in an abrupt binary way. Arousals may be considered more as different states of the brain than as “short awakenings.” This phenomenon may reflect the mechanisms involved in the negotiation between two main contradictory functional necessities, preserving the continuity of sleep, and maintaining the possibility to react.

42 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.
Abstract: Pain is an unpleasant, complex, and perceived experience that places a significant burden on patients and clinicians. Its severity may be mediated by emotion, attitude, and environmental influences, and pain may be expressed differently in males and females. Traumatic brain injury (TBI) is f

29 citations


Journal ArticleDOI
Wang Yuan1, Li Dan1, Rana Netra1, Ma Shaohui1, Jin Chen-wang1, Zhang Ming1 
Abstract: Sumatriptan, a drug widely used to alleviate migraine headaches, has several somatosensory adverse effects, including tactile allodynia. To understand whether sumatriptan affects sensory and affective circuitries simultaneously, we investigated the responses of 12 healthy volunteers to electrical stimuli after infusion with either sumatriptan or saline. Using a double-blind crossover study design, we used functional magnetic resonance imaging (fMRI) to measure brain activation in different areas during electrical stimulation. The visual analog scale (VAS) and short-form McGill pain questionnaire (SF-MPQ) were used to rate stimulation-evoked sensations and affections after drug administration. VAS rating, SF-MPQ, and block fMRI were all performed in each subject during sumatriptan and saline injection. Echo-planar imaging sequences were used to determine the whole-brain blood oxygenation level-dependent signal of the entire brain. Our results showed that sumatriptan predominantly activated regions in the medial pain system and smaller regions in the lateral pain system. These regions included the secondary somatosensory cortex (SII), anterior insular cortex, orbitofrontal cortex, medial thalamus, cerebellar supravermis, dentate nucleus, and the majority of the anterior cingulate cortex (ACC). In contrast, activation following saline administration was observed primarily in the lateral pain system, including the primary sensory cortex, lateral SII, posterior insular cortex, anterior ACC, and lateral thalamus. Importantly, we found that VAS ratings and MPQ scores were increased after sumatriptan infusion, but not after saline administration. Our fMRI, VAS, and SF-MPQ findings suggest that sumatriptan plays a significant role in the affective dimension of pain and a minor role related to sensory discrimination.

17 citations


Cites background from "Filtering the reality: Functional d..."

  • ...The medial system includes polysynaptic and poorly lateralized non-somatotopic projections to the lentiform nuclei, insular cortex (IC), and anterior cingulate cortex (ACC) (Bastuji et al. 2011)....

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References
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Journal ArticleDOI
TL;DR: Techniques of recording, scoring, and doubtful records are carefully considered, and Recommendations for abbreviations, types of pictorial representation, order of polygraphic tracings are suggested.
Abstract: With the vast research interest in sleep and dreams that has developed in the past 15 years, there is increasing evidence of noncomparibility of scoring of nocturnal electroencephalograph-electroculograph records from different laboratories. In 1967 a special session on scoring criteria was held at the seventh annual meeting of the Association for the Psychophysiological Study of Sleep. Under the auspices of the UCLA Brain Information, an ad hoc committee composed of some of the most active current researchers was formed in 1967 to develop a terminology and scoring system for universal use. It is the results of the labors of this group that is now published under the imprimatur of the National Institutes of Health. The presentation is beautifully clear. Techniques of recording, scoring, and doubtful records are carefully considered. Recommendations for abbreviations, types of pictorial representation, order of polygraphic tracings are suggested.

7,774 citations



Journal ArticleDOI
Abstract: Context: The perception of pain due to an acute injury or in clinical pain states undergoes substantial processing at supraspinal levels. Supraspinal, brain mechanisms are increasingly recognized as playing a major role in the representation and modulation of pain experience. These neural mechanisms may then contribute to interindividual variations and disabilities associated with chronic pain conditions. Objective: To systematically review the literature regarding how activity in diverse brain regions creates and modulates the experience of acute and chronic pain states, emphasizing the contribution of various imaging techniques to emerging concepts. Data Sources: MEDLINE and PRE-MEDLINE searches were performed to identify all English-language articles that examine human brain activity during pain, using hemodynamic (PET, fMRI), neuroelectrical (EEG, MEG) and neurochemical methods (MRS, receptor binding and neurotransmitter modulation), from January 1, 1988 to March 1, 2003. Additional studies were identified through bibliographies. Study Selection: Studies were selected based on consensus across all four authors. The criteria included well-designed experimental procedures, as well as landmark studies that have significantly advanced the field. Data Synthesis: Sixty-eight hemodynamic studies of experimental pain in normal subjects, 30 in clinical pain conditions, and 30 using neuroelectrical methods met selection criteria and were used in a meta-analysis. Another 24 articles were identified where brain neurochemistry of pain was examined. Technical issues that may explain differences between studies across laboratories are expounded. The evidence for and the respective incidences of brain areas constituting the brain network for acute pain are presented. The main components of this network are: primary and secondary somatosensory, insular, anterior cingulate, and prefrontal cortices (S1, S2, IC, ACC, PFC) and thalamus (Th). Evidence for somatotopic organization, based on 10 studies, and psychological modulation, based on 20 studies, is discussed, as well as the temporal sequence of the afferent volley to the cortex, based on neuroelectrical studies. A meta-analysis highlights important methodological differences in identifying the brain network underlying acute pain perception. It also shows that the brain network for acute pain perception in normal subjects is at least partially distinct from that seen in chronic clinical pain conditions and that chronic pain engages brain regions critical for cognitive/emotional assessments, implying that this component of pain may be a distinctive feature between chronic and acute pain. The neurochemical studies highlight the role of opiate and catecholamine transmitters and receptors in pain states, and in the modulation of pain with environmental and genetic influences. Conclusions: The nociceptive system is now recognized as a sensory system in its own right, from primary afferents to multiple brain areas. Pain experience is strongly modulated by interactions of ascending and descending pathways. Understanding these 1090-3801/$30 2004 Published by Elsevier Ltd on behalf of European Federation of Chapters of the International Association for the Study of

2,504 citations