Neuroimaging of cold allodynia reveals a central disinhibition mechanism of pain

Julia Forstenpointner; Andreas Binder; Rainer Maag; Oliver Granert; Philipp Hüllemann; Martin Peller; Gunnar Wasner; Stefan Wolff; Olav Jansen; Hartwig Roman Siebner; Ralf Baron

doi:10.2147/JPR.S216508

Neuroimaging of cold allodynia reveals a central disinhibition mechanism of pain

Julia Forstenpointner^*, Andreas Binder, Rainer Maag, Oliver Granert, Philipp Hüllemann, Martin Peller, Gunnar Wasner, Stefan Wolff, Olav Jansen, Hartwig Roman Siebner, Ralf Baron

^*Corresponding author af dette arbejde

Institut for Klinisk Medicin

1 Citationer (Scopus)

2 Downloads (Pure)

Abstract

Purpose: Allodynia refers to pain evoked by physiologically innocuous stimuli. It is a disabling symptom of neuropathic pain following a lesion within the peripheral or central nervous system. In fact, two different pathophysiological mechanisms of cold allodynia (ie, hypersensitivity to innocuous cold) have been proposed. The peripheral sensitization of nociceptive neurons can produce cold allodynia, which can be induced experimentally by a topical application of menthol. An alternative mechanism involves reduced inhibition of central pain processing by innocuous cold stimuli. A model to induce the latter type of allodynia is the conduction block of peripheral A-fiber input. Patients and methods: In the presented study, functional MRI was used to analyze these two different experimental models of cold allodynia. In order to identify the underlying cerebral activation patterns of both mechanisms, the application of menthol and the induction of a mechanical A-fiber blockade were studied in healthy volunteers. Results: The block-induced cold allodynia caused significantly stronger activation of the medial polymodal pain processing pathway, including left medial thalamus, anterior cingulate cortex, and medial prefrontal cortex. In contrast, menthol-induced cold allodynia caused significantly stronger activity of the left lateral thalamus as well as the primary and secondary somatosensory cortices, key structures of the lateral discriminative pathway of pain processing. Mean pain intensity did not differ between both forms of cold allodynia. Conclusion: Experimental cold allodynia is mediated in different cerebral areas depending on the underlying pathophysiology. The activity pattern associated with block-induced allodynia confirms a fundamental integration between painful and non-painful temperature sensation, ie, the cold-induced inhibition of cold pain.

Originalsprog	Engelsk
Tidsskrift	Journal of Pain Research
Vol/bind	12
Sider (fra-til)	3055-3066
ISSN	1178-7090
DOI	https://doi.org/10.2147/JPR.S216508
Status	Udgivet - 2019

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10.2147/JPR.S216508Licens: CC BY-NC

jpr-216508-neuroimaging-of-cold-allodynia-reveals-a-central-disinhibitiForlagets udgivne version, 2,84 MBLicens: CC BY-NC

Citationsformater

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title = "Neuroimaging of cold allodynia reveals a central disinhibition mechanism of pain",

abstract = "Purpose: Allodynia refers to pain evoked by physiologically innocuous stimuli. It is a disabling symptom of neuropathic pain following a lesion within the peripheral or central nervous system. In fact, two different pathophysiological mechanisms of cold allodynia (ie, hypersensitivity to innocuous cold) have been proposed. The peripheral sensitization of nociceptive neurons can produce cold allodynia, which can be induced experimentally by a topical application of menthol. An alternative mechanism involves reduced inhibition of central pain processing by innocuous cold stimuli. A model to induce the latter type of allodynia is the conduction block of peripheral A-fiber input. Patients and methods: In the presented study, functional MRI was used to analyze these two different experimental models of cold allodynia. In order to identify the underlying cerebral activation patterns of both mechanisms, the application of menthol and the induction of a mechanical A-fiber blockade were studied in healthy volunteers. Results: The block-induced cold allodynia caused significantly stronger activation of the medial polymodal pain processing pathway, including left medial thalamus, anterior cingulate cortex, and medial prefrontal cortex. In contrast, menthol-induced cold allodynia caused significantly stronger activity of the left lateral thalamus as well as the primary and secondary somatosensory cortices, key structures of the lateral discriminative pathway of pain processing. Mean pain intensity did not differ between both forms of cold allodynia. Conclusion: Experimental cold allodynia is mediated in different cerebral areas depending on the underlying pathophysiology. The activity pattern associated with block-induced allodynia confirms a fundamental integration between painful and non-painful temperature sensation, ie, the cold-induced inhibition of cold pain.",

keywords = "A-fiber block, Cold allodynia, FMRI, Menthol",

author = "Julia Forstenpointner and Andreas Binder and Rainer Maag and Oliver Granert and Philipp H{\"u}llemann and Martin Peller and Gunnar Wasner and Stefan Wolff and Olav Jansen and Siebner, {Hartwig Roman} and Ralf Baron",

year = "2019",

doi = "10.2147/JPR.S216508",

language = "English",

volume = "12",

pages = "3055--3066",

journal = "Journal of Pain Research",

issn = "1178-7090",

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TY - JOUR

T1 - Neuroimaging of cold allodynia reveals a central disinhibition mechanism of pain

AU - Forstenpointner, Julia

AU - Binder, Andreas

AU - Maag, Rainer

AU - Granert, Oliver

AU - Hüllemann, Philipp

AU - Peller, Martin

AU - Wasner, Gunnar

AU - Wolff, Stefan

AU - Jansen, Olav

AU - Siebner, Hartwig Roman

AU - Baron, Ralf

PY - 2019

Y1 - 2019

N2 - Purpose: Allodynia refers to pain evoked by physiologically innocuous stimuli. It is a disabling symptom of neuropathic pain following a lesion within the peripheral or central nervous system. In fact, two different pathophysiological mechanisms of cold allodynia (ie, hypersensitivity to innocuous cold) have been proposed. The peripheral sensitization of nociceptive neurons can produce cold allodynia, which can be induced experimentally by a topical application of menthol. An alternative mechanism involves reduced inhibition of central pain processing by innocuous cold stimuli. A model to induce the latter type of allodynia is the conduction block of peripheral A-fiber input. Patients and methods: In the presented study, functional MRI was used to analyze these two different experimental models of cold allodynia. In order to identify the underlying cerebral activation patterns of both mechanisms, the application of menthol and the induction of a mechanical A-fiber blockade were studied in healthy volunteers. Results: The block-induced cold allodynia caused significantly stronger activation of the medial polymodal pain processing pathway, including left medial thalamus, anterior cingulate cortex, and medial prefrontal cortex. In contrast, menthol-induced cold allodynia caused significantly stronger activity of the left lateral thalamus as well as the primary and secondary somatosensory cortices, key structures of the lateral discriminative pathway of pain processing. Mean pain intensity did not differ between both forms of cold allodynia. Conclusion: Experimental cold allodynia is mediated in different cerebral areas depending on the underlying pathophysiology. The activity pattern associated with block-induced allodynia confirms a fundamental integration between painful and non-painful temperature sensation, ie, the cold-induced inhibition of cold pain.

AB - Purpose: Allodynia refers to pain evoked by physiologically innocuous stimuli. It is a disabling symptom of neuropathic pain following a lesion within the peripheral or central nervous system. In fact, two different pathophysiological mechanisms of cold allodynia (ie, hypersensitivity to innocuous cold) have been proposed. The peripheral sensitization of nociceptive neurons can produce cold allodynia, which can be induced experimentally by a topical application of menthol. An alternative mechanism involves reduced inhibition of central pain processing by innocuous cold stimuli. A model to induce the latter type of allodynia is the conduction block of peripheral A-fiber input. Patients and methods: In the presented study, functional MRI was used to analyze these two different experimental models of cold allodynia. In order to identify the underlying cerebral activation patterns of both mechanisms, the application of menthol and the induction of a mechanical A-fiber blockade were studied in healthy volunteers. Results: The block-induced cold allodynia caused significantly stronger activation of the medial polymodal pain processing pathway, including left medial thalamus, anterior cingulate cortex, and medial prefrontal cortex. In contrast, menthol-induced cold allodynia caused significantly stronger activity of the left lateral thalamus as well as the primary and secondary somatosensory cortices, key structures of the lateral discriminative pathway of pain processing. Mean pain intensity did not differ between both forms of cold allodynia. Conclusion: Experimental cold allodynia is mediated in different cerebral areas depending on the underlying pathophysiology. The activity pattern associated with block-induced allodynia confirms a fundamental integration between painful and non-painful temperature sensation, ie, the cold-induced inhibition of cold pain.

KW - A-fiber block

KW - Cold allodynia

KW - FMRI

KW - Menthol

U2 - 10.2147/JPR.S216508

DO - 10.2147/JPR.S216508

M3 - Journal article

C2 - 31807061

AN - SCOPUS:85074793807

SN - 1178-7090

VL - 12

SP - 3055

EP - 3066

JO - Journal of Pain Research

JF - Journal of Pain Research

ER -

Neuroimaging of cold allodynia reveals a central disinhibition mechanism of pain

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