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Neurophysiology And Functional Neuroanatomy Of Pain Perception

A. Schnitzler, M. Ploner
Published 2000 · Psychology, Medicine

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Summary The traditional view that the cerebral cortex is not involved in pain processing has been abandoned during the past decades based on anatomic and physiologic investigations in animals, and lesion, functional neuroimaging, and neurophysiologic studies in humans. These studies have revealed an extensive central network associated with nociception that consistently includes the thalamus, the primary (SI) and secondary (SII) somatosensory cortices, the insula, and the anterior cingulate cortex (ACC). Anatomic and electrophysiologic data show that these cortical regions receive direct nociceptive thalamic input. From the results of human studies there is growing evidence that these different cortical structures contribute to different dimensions of pain experience. The SI cortex appears to be mainly involved in sensory-discriminative aspects of pain. The SII cortex seems to have an important role in recognition, learning, and memory of painful events. The insula has been proposed to be involved in autonomic reactions to noxious stimuli and in affective aspects of pain-related learning and memory. The ACC is closely related to pain unpleasantness and may subserve the integration of general affect, cognition, and response selection. The authors review the evidence on which the proposed relationship between cortical areas, pain-related neural activations, and components of pain perception is based.
This paper references
Pain sensitivity alterations
J Comp Neurol (1991)
10.1016/S1082-3174(97)70002-3
The sensory-limbic model of pain memory: Connections from thalamus to the limbic system mediate the learned component of the affective dimension of pain
K. Casey (1997)
10.1523/JNEUROSCI.05-05-01103.1985
Attentional influences on noxious and innocuous cutaneous heat detection in humans and monkeys
M. Bushnell (1985)
10.1002/CNE.903080312
Anatomic evidence of nociceptive inputs to primary somatosensory cortex: Relationship between spinothalamic terminals and thalamocortical cells in squirrel monkeys
S. Gingold (1991)
10.3109/08990229309028839
Tactile-vibration-activated foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans.
H. Burton (1993)
10.1016/0013-4694(95)00032-T
Brain electrical source analysis of laser evoked potentials in response to painful trigeminal nerve stimulation.
B. Bromm (1995)
10.1016/0028-3932(79)90005-8
Analogous neural models for tactual and visual learning
M. Mishkin (1979)
10.1006/SMNS.1995.0031
Functional imaging of pain: new insights regarding the role of the cerebral cortex in human pain perception
V. Apkarian (1995)
10.1038/384258A0
Functional imaging of an illusion of pain
A. Craig (1996)
10.1152/JN.1998.79.5.2535
Responses of neurons in the insular cortex to gustatory, visceral, and nociceptive stimuli in rats.
T. Hanamori (1998)
10.1038/8065
Pain-related neurons in the human cingulate cortex
W. Hutchison (1999)
10.1002/CNE.902620207
Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents
B. Vogt (1987)
10.1016/0304-3940(96)13025-1
Laser-evoked potentials after painful hand and foot stimulation in humans: evidence for generation of the middle-latency component in the secondary somatosensory cortex
J. Spiegel (1996)
10.1046/j.1460-9568.1999.00429.x
Different cortical organization of visceral and somatic sensation in humans
A. Schnitzler (1999)
10.1038/373249A0
Blood flow changes in human somatosensory cortex during anticipated stimulation
W. Drevets (1995)
Righthemisphere preponderance of responses to painful CO2 stimulation of the human nasal mucosa
Lett (1983)
10.1007/978-1-4757-9619-3_5
The Insula of Reil in Man and Monkey
M. Mesulam (1985)
Parallel activation
Pain 1999a (1999)
10.1152/JN.1969.32.2.170
Symmetry and connectivity in the map of the body surface in somatosensory area II of primates.
B. Whitsel (1969)
10.1002/(SICI)1096-9861(19981005)399:4<469::AID-CNE3>3.0.CO;2-#
Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex
C. J. Shi (1998)
10.1523/JNEUROSCI.14-11-06779.1994
Squirrel monkey lateral thalamus. I. Somatic nociresponsive neurons and their relation to spinothalamic terminals
A. Apkarian (1994)
10.1016/0304-3959(92)90109-O
Reversible pain and tactile deficits associated with a cerebral tumor compressing the posterior insula and parietal operculum
J. Greenspan (1992)
10.1152/JN.1994.72.2.542
Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys.
Willie K. Dong (1994)
10.1016/0006-8993(88)90841-4
SI nociceptive neurons participate in the encoding process by which monkeys perceive the intensity of noxious thermal stimulation
D. R. Kenshalo (1988)
10.1152/JN.1996.76.1.571
Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain.
K. Casey (1996)
10.1016/S0306-4522(99)00339-5
Monkey insular cortex neurons respond to baroreceptive and somatosensory convergent inputs
Z. Zhang (1999)
10.1111/j.1460-9568.1993.tb00536.x
Functional Organization of the Human First and Second Somatosensory Cortices: a Neuromagnetic Study
R. Hari (1993)
10.1001/ARCHNEURPSYC.1956.02330210011001
The conduction of pain above the level of the thalamus opticus.
A. Biemond (1956)
10.1126/SCIENCE.107587
Thalamic and cortical afferents differentiate anterior from posterior cingulate cortex in the monkey.
B. Vogt (1979)
10.1038/372770A0
A thalamic nucleus specific for pain and temperature sensation
A. Craig (1994)
10.1002/(SICI)1096-9861(19981005)399:4<440::AID-CNE2>3.0.CO;2-1
Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices
C. J. Shi (1998)
Medulla to thalamus
AD Craig
10.1006/nimg.1999.0482
A Comparative fMRI Study of Cortical Representations for Thermal Painful, Vibrotactile, and Motor Performance Tasks
P. A. Gelnar (1999)
10.1016/0028-3932(93)90147-R
Investigations of the functional anatomy of attention using the stroop test
C. Bench (1993)
10.1098/rspb.1991.0048
Cortical and subcortical localization of response to pain in man using positron emission tomography
A. K. Jones (1991)
10.1152/JN.1999.82.4.1934
Pain intensity processing within the human brain: a bilateral, distributed mechanism.
R. Coghill (1999)
Reversible
JD Greenspan
relief” by frontal cingulotomy
Nature (1995)
10.1152/JN.2000.83.3.1770
Differential organization of touch and pain in human primary somatosensory cortex.
M. Ploner (2000)
10.1016/0304-3959(89)90008-0
Analgesia produced by injection of lidocaine into the anterior cingulum bundle of the rat
A. Vaccarino (1989)
Nociceptive neurons in primate insular cortex
J O Dostrovsky
10.1093/BRAIN/121.5.931
Neural activation during acute capsaicin-evoked pain and allodynia assessed with PET.
M. Iadarola (1998)
10.1016/0006-8993(96)00561-6
Morphological and electrophysiological properties of ACCx nociceptive neurons in rats
H. Yamamura (1996)
Neural mechanisms subserving cutaneous sensibility, with special reference to the role of afferent inhibition in sensory perception and discrimination.
V. Mountcastle (1959)
studied by positron emission tomography
RW Hurt (1995)
10.1093/BRAIN/60.4.389
SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION
W. Penfield (1937)
10.1016/0304-3940(91)90362-W
In vivo distribution of opioid receptors in man in relation to the cortical projections of the medial and lateral pain systems measured with positron emission tomography
A. Jones (1991)
10.1002/1531-8249(199901)45:1<40::AID-ART8>3.0.CO;2-L
Region‐specific encoding of sensory and affective components of pain in the human brain: A positron emission tomography correlation analysis
T. Toelle (1999)
10.1111/j.1460-9568.1995.tb00716.x
Somatosensory Activations of the Parietal Operculum of Man. A PET Study
A. Ledberg (1995)
10.1016/S0016-5085(97)70220-8
Regional cerebral activity in normal and pathological perception of visceral pain.
D. Silverman (1997)
10.1002/HBM.460030102
Topography of diprenorphine binding in human cingulate gyrus and adjacent cortex derived from coregistered PET and MR images
B. Vogt (1995)
10.1093/BRAIN/118.1.279
Contributions of anterior cingulate cortex to behaviour.
O. Devinsky (1995)
CO 2 stimulation of the human nasal mucosa
H Head (1997)
10.1097/00001756-199808030-00044
Nociceptive neurons in the macaque anterior cingulate activate during anticipation of pain
T. Koyama (1998)
10.1016/0304-3940(83)90425-1
Neuromagnetic localization of cortical activity evoked by painful dental stimulation in man
R. Hari (1983)
10.1016/0006-8993(89)90375-2
Nociceptive responses of trigeminal neurons in SII-7b cortex of awake monkeys
Willie K. Dong (1989)
10.1126/SCIENCE.2003220
Multiple representations of pain in human cerebral cortex.
J. Talbot (1991)
10.1073/PNAS.96.14.7705
Pain perception: is there a role for primary somatosensory cortex?
M. Bushnell (1999)
Cerebral localization of pain
WH Sweet
Atten - tional influences on noxious and innocuous cutaneous heat detection in humans and monkeys
MC Bushnell (1985)
10.1016/S0304-3959(97)00023-7
Right-hemisphere preponderance of responses to painful CO2 stimulation of the human nasal mucosa
R. Hari (1997)
10.1002/ANA.410440516
Somatic and limbic cortex activation in esophageal distention: A functional imaging study
F. Binkofski (1998)
10.1002/CNE.901920106
Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis
C. Robinson (1980)
10.1152/JN.1990.63.3.559
Responses of nociceptive SI neurons in monkeys and pain sensation in humans elicited by noxious thermal stimulation: effect of interstimulus interval.
E. Chudler (1990)
10.1016/S0168-5597(98)00054-9
Intracortical recordings of early pain-related CO2-laser evoked potentials in the human second somatosensory (SII) area
Maud Frot (1999)
10.1016/S0165-0173(96)00011-2
Circuitry and functional aspects of the insular lobe in primates including humans
J. Augustine (1996)
The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm.Proc
Bull Johns Hopkins Hosp (1959)
10.1016/S0959-4388(98)80041-X
Hierarchical somatosensory processing
Y. Iwamura (1998)
10.1002/CNE.903110209
Parallel thalamic activation of the first and second somatosensory areas in prosimian primates and tree shrews
P. Garraghty (1991)
10.1093/BRAIN/34.2-3.102
Sensory disturbances from cerebral lesions
H. Head (1911)
10.1152/JN.1999.81.6.3100
Parallel activation of primary and secondary somatosensory cortices in human pain processing.
M. Ploner (1999)
10.1016/0013-4694(86)90159-8
Cortical responses to painful CO2 stimulation of nasal mucosa; a magnetoencephalographic study in man.
J. Huttunen (1986)
10.1016/0165-0173(85)90013-X
Diencephalic mechanisms of pain sensation
D. Albe-Fessar (1985)
10.1016/S1388-2457(00)00273-X
Sources of cortical responses to painful CO2 laser skin stimulation of the hand and foot in the human brain
Massimiliano Valeriani (2000)
10.1016/0013-4694(91)90137-S
Tonic changes in alpha power during immersion of the hand in cold water.
M. Backonja (1991)
10.1212/WNL.43.4.762
Ventrolateral and dorsomedial somatosensory association cortex damage produces distinct somesthetic syndromes in humans
R. Caselli (1993)
10.1152/JN.1983.50.6.1479
Responses of primate SI cortical neurons to noxious stimuli.
D. Kenshalo (1983)
10.1152/JN.1980.43.6.1594
Responses of neurons in primate ventral posterior lateral nucleus to noxious stimuli.
D. Kenshalo (1980)
10.1126/SCIENCE.277.5328.968
Pain affect encoded in human anterior cingulate but not somatosensory cortex.
P. Rainville (1997)
10.1152/JN.1997.77.6.3370
Functional MRI of pain- and attention-related activations in the human cingulate cortex.
K. Davis (1997)
10.1007/978-1-4615-6622-9_5
The Role of the Cerebral Cortex in Pain Sensation
D. R. Kenshalo (1991)
Supraspinal projections of lamina I neurons
AD Craig
10.1152/JN.1993.70.1.331
Neuronal activity in the second somatosensory cortex of monkeys (Macaca mulatta) during active touch of gratings.
R. Sinclair (1993)
10.1002/CNE.902520304
Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch
D. Friedman (1986)
10.1038/331585A0
Positron emission tomographic studies of the cortical anatomy of single-word processing
S. E. Petersen (1988)
10.1016/S0304-3959(97)00138-3
Pain processing during three levels of noxious stimulation produces differential patterns of central activity
S. Derbyshire (1997)
10.1523/JNEUROSCI.11-08-02383.1991
Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography
M. Corbetta (1991)
10.1097/00004691-199310000-00009
Equivalent electrical source analysis of pain-related somatosensory evoked potentials elicited by a CO2 laser.
I. Tarkka (1993)
Textbook of pain.New York: Churchill Livingstone
CJ Robinson (1999)
10.1007/978-3-0348-9016-8_3
Pain, temperature, and the sense of the body
A. Craig (1996)
10.1152/JN.1998.80.6.3312
Temporal and intensity coding of pain in human cortex.
C. Porro (1998)
10.1093/NEUROSURGERY/21.CN_SUPPL_1.334
Stereotactic anterior cingulate lesions for persistent pain: a report on 68 cases.
Hurt Rw (1974)
Two cortical visual systems
Leslie G. Ungerleider (1982)
Peripheral neural mechanisms of nociception
SN Raja
10.1212/WNL.4.6.483
Epilepsy and the Functional Anatomy of the Human Brain
R.N.Dej. (1954)
10.1093/neurosurgery/21.cn_suppl_1.334
Stereotactic anterior cingulate lesions for persistent pain: a report on 68 cases.
R. W. Hurt (1974)
10.3109/08990229409051393
Heat-induced pain diminishes vibrotactile perception: a touch gate.
A. Apkarian (1994)
10.1002/ANA.410240109
Asymbolia for pain: A sensory‐limbic disconnection syndrome
M. Berthier (1988)
10.1002/CNE.902520305
Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the macaque
D. Friedman (1986)
10.1111/j.1460-9568.1996.tb01608.x
Pain Processing in Four Regions of Human Cingulate Cortex Localized with Co‐registered PET and MR Imaging
B. Vogt (1996)
10.1523/JNEUROSCI.14-07-04095.1994
Distributed processing of pain and vibration by the human brain
R. Coghill (1994)
10.3171/JNS.1962.19.2.0089
Pain "relief" by frontal cingulumotomy.
E. Foltz (1962)
10.1016/0006-8993(93)91541-Y
Spinothalamocortical projections to the secondary somatosensory cortex (SII) in squirrel monkey
R. Stevens (1993)
10.1152/JN.1992.67.2.411
Parallel processing of tactile information in the cerebral cortex of the cat: effect of reversible inactivation of SI on responsiveness of SII neurons.
A. Turman (1992)
Somatic and limbic cortex activation in esophageal distention: a functional magnetic resonance imaging study.
F. Binkofski (1998)
10.1016/S0304-3959(99)00012-3
Pain affect without pain sensation in a patient with a postcentral lesion
M. Ploner (1999)
10.1152/JN.1992.68.5.1720
Nociceptive neurons in area 24 of rabbit cingulate cortex.
R. Sikes (1992)
10.1093/BRAIN/103.3.525
The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis.
C. Baleydier (1980)
10.1007/BF00235539
Rat somatosensory (SmI) cortex: I. Characteristics of neuronal responses to noxious stimulation and comparison with responses to non-noxious stimulation
Y. Lamour (2004)
10.1016/0304-3959(95)00048-W
Central representation of chronic ongoing neuropathic pain studied by positron emission tomography
J. Hsieh (1995)
Nociceptive neurons in primate insular cortex [ abstract ]
JO Dostrovsky
10.1016/S0304-3959(99)00021-4
Pain sensitivity alterations as a function of lesion location in the parasylvian cortex
J. Greenspan (1999)
10.1152/JN.1998.79.4.2231
Painful stimuli evoke potentials recorded over the human anterior cingulate gyrus.
F. Lenz (1998)
10.1007/s002210050215
Somatotopic organization along the central sulcus, for pain localization in humans, as revealed by positron emission tomography
J. Andersson (1997)
10.1152/JN.1978.41.6.1592
Nociceptive responses of neurons in medial thalamus and their relationship to spinothalamic pathways.
Willie K. Dong (1978)
10.1152/JN.1998.80.3.1533
Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli.
K. Davis (1998)
10.1016/S0304-3940(98)00007-X
Possible representation of somatic pain in the rat insular visceral sensory cortex: a field potential study
S. Ito (1998)
10.1016/0924-980X(95)92867-L
Pain-related magnetic fields following painful CO2 laser stimulation in man.
R. Kakigi (1995)
Stereotactic anterior cingulate lesions
Pain (1995)
10.1097/00007611-195402000-00035
Book Reviews: Epilepsy and the Functional Anatomy of the Human Brain
W. Penfield (1954)
10.1016/S1082-3174(98)70004-2
A new version of the thalamic disinhibition hypothesis of central pain
A. Craig (1998)
10.1152/JN.1998.80.6.3272
Response of anterior parietal cortex to different modes of same-site skin stimulation.
M. Tommerdahl (1998)
10.1016/0304-3940(92)90088-O
Persistent pain inhibits contralateral somatosensory cortical activity in humans
A. Apkarian (1992)
10.1152/JN.1996.75.6.2662
Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site.
M. Tommerdahl (1996)
10.1097/00005053-191012000-00013
Vergleichende Lokalisationslehre der Grosshirnrinde
Jelliffe. (1910)
10.1136/jnnp.57.10.1166
Cerebral responses to pain in patients with atypical facial pain measured by positron emission tomography.
S. Derbyshire (1994)
10.1007/s002210050254
Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex
S. Derbyshire (1998)
10.1016/0304-3940(95)11604-U
Pain-related magnetic fields following painful CO2 laser stimulation in man
R. Kakigi (1995)
10.1152/JN.1994.71.2.802
Positron emission tomographic analysis of cerebral structures activated specifically by repetitive noxious heat stimuli.
K. Casey (1994)
10.1093/CERCOR/2.6.435-A
Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions.
B. Vogt (1992)
10.1073/PNAS.87.1.256
The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm.
J. V. Pardo (1990)
10.1002/CNE.902880308
Primate spinothalamic pathways: II. The cells of origin of the dorsolateral and ventral spinothalamic pathways
A. Apkarian (1989)



This paper is referenced by
10.1037/0735-7044.119.2.491
Contingent negative variation in the parasylvian cortex increases during expectancy of painful sensorimotor events: a magnetoencephalographic study.
C. Babiloni (2005)
10.1016/S0889-8553(03)00132-8
Brain processing of esophageal sensation in health and disease.
A. Hobson (2004)
10.1523/JNEUROSCI.5061-05.2006
Receptive Field (RF) Properties of the Macaque Second Somatosensory Cortex: RF Size, Shape, and Somatotopic Organization
P. Fitzgerald (2006)
10.1111/pme.12133
Heart rate variability parameters do not correlate with pain intensity in healthy volunteers.
J. Meeuse (2013)
10.3389/fnins.2012.00136
Organization of Neural Systems for Aversive Information Processing: Pain, Error, and Punishment
Shunsuke Kobayashi (2012)
10.1016/j.clinph.2011.07.047
Brain activity in rectosigmoid pain: Unravelling conditioning pain modulatory pathways
C. Brock (2012)
10.1046/j.1460-9568.2003.02851.x
Anticipatory cortical responses during the expectancy of a predictable painful stimulation. A high‐resolution electroencephalography study
C. Babiloni (2003)
Spotting pain in the brain. Towards a useful animal model of pain
Tanja L Jensen (2011)
10.1023/A:1022911411903
Dissolving the Explanatory Gap: Neurobiological Differences Between Phenomenal and Propositional Knowledge
J. Musacchio (2002)
10.1007/s00415-003-0237-7
Neurophysiological studies of pain pathways in peripheral and central nervous system disorders
R.-D. Treede (2003)
10.1016/S0306-4522(03)00261-6
A comparative magnetoencephalographic study of cortical activations evoked by noxious and innocuous somatosensory stimulations
K. Inui (2003)
10.1523/JNEUROSCI.2197-10.2010
Insular Cortex Activity Is Associated with Effects of Negative Expectation on Nociceptive Long-Term Habituation
R. Rodriguez-Raecke (2010)
10.1093/CERCOR/BHJ071
Brain processing of the signals ascending through unmyelinated C fibers in humans: an event-related functional magnetic resonance imaging study.
Y. Qiu (2006)
10.1007/s00132-002-0354-5
“Repetitive strain injuries”
H. Sorgatz (2002)
AINS ET DOULEUR : ACTUALITES CHEZ LES CARNIVORES DOMESTIQUES
M. Senard (2003)
10.1016/j.npep.2020.102046
Differential role of specific cardiovascular neuropeptides in pain regulation: Relevance to cardiovascular diseases
Ewa Szczepanska-sadowska (2020)
10.1007/S12152-012-9163-7
Ethical Aspects of Computational Neuroscience
Tyler D. Bancroft (2013)
10.1016/B978-0-12-418677-4.00018-X
Imaging Pain in the Human Brain
M. Loggia (2014)
10.1002/ddrr.15
The nervous system and gastrointestinal function.
M. A. Altaf (2008)
10.1002/j.1532-2149.2012.00254.x
Peripheral and central nervous contribution to gastrointestinal symptoms in diabetic patients with autonomic neuropathy
C. Brock (2013)
10.1007/s11682-012-9179-y
Brain regions associated with psychological pain: implications for a neural network and its relationship to physical pain
E. Meerwijk (2012)
10.1016/j.neuroimage.2010.09.084
A multisensory investigation of the functional significance of the “pain matrix”
A. Mouraux (2011)
10.1186/1757-7241-20-22
Pain-related somatosensory evoked potentials and functional brain magnetic resonance in the evaluation of neurologic recovery after cardiac arrest: a case study of three patients
P. Zanatta (2012)
Brain imaging of chronic pain
N. Vartiainen (2009)
10.1016/j.pain.2008.05.007
Trigeminal activation using chemical, electrical, and mechanical stimuli
E. Iannilli (2008)
10.11606/D.42.2012.TDE-09112012-093200
Mecanismos centrais da dor músculo-esquelética induzida por carregenina em ratos.
M. Freitas (2012)
10.1152/jn.00097.2008
Determinants of laser-evoked EEG responses: pain perception or stimulus saliency?
G. Iannetti (2008)
10.1007/978-1-4419-0345-7_37
White Matter: Functional Anatomy of Key Tracts
Mohit Maheshwari (2011)
10.1007/s12264-011-1035-3
Behavioral assessments of the aversive quality of pain in animals
Xu-Jie Zhang 张许杰 (2011)
10.1097/00001756-200401190-00014
Pain-related aversion and Fos expression in the central nervous system in rats
L. Lei (2004)
10.1007/s10548-004-1006-3
Scalp Field Potentials of Human Pain: Spatial Effects and Temporal Relation in Finger Stimulation
L. Wang (2004)
10.1055/S-2004-830010
Anatomy and Physiology of Pain
M. Heinricher (2004)
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