Descending pain modulatory efficiency in healthy subjects is related to structure and resting connectivity of brain regions

Huynh, Vincent; Lütolf, Robin; Rösner, Jan; Luechinger, Roger; Curt, Armin; Kollias, Spyros; Michels, Lars; Hubli, Michéle

doi:10.1016/j.neuroimage.2021.118742

Cited by 10 publications

(15 citation statements)

References 82 publications

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“…Previous studies have confirmed that enhanced nociceptive sensitization in patients with chronic pain may be associated with overlapping pain activation in the insula (Ploghaus et al, 2001 ; Zhuo, 2016 ). In addition, reduced pain inhibition is associated with stronger resting-state FC in relation to the insula and other cortical brain regions (Huynh et al, 2022 ). Furthermore, impaired insula function can also produce or enhance emotions such as anxiety (Paulus and Stein, 2010 ; Avery et al, 2014 ; Zhuo, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Neuroplasticity of pain processing and motor control in CAI patients: A UK Biobank study with clinical validation

Li¹,

Xue²,

Xu³

et al. 2023

Front. Mol. Neurosci.

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BackgroundPain plays an important role in chronic ankle instability (CAI), and prolonged pain may be associated with ankle dysfunction and abnormal neuroplasticity.PurposeTo investigate the differences in resting-state functional connectivity among the pain-related brain regions and the ankle motor-related brain regions between healthy controls and patients with CAI, and explore the relationship between patients' motor function and pain.Study designA cross-database, cross-sectional study.MethodsThis study included a UK Biobank dataset of 28 patients with ankle pain and 109 healthy controls and a validation dataset of 15 patients with CAI and 15 healthy controls. All participants underwent resting-state functional magnetic resonance imaging scanning, and the functional connectivity (FC) among the pain-related brain regions and the ankle motor-related brain regions were calculated and compared between groups. The correlations between the potentially different functional connectivity and the clinical questionnaires were also explored in patients with CAI.ResultsThe functional connection between the cingulate motor area and insula significantly differed between groups in both the UK Biobank (p = 0.005) and clinical validation dataset (p = 0.049), which was also significantly correlated with Tegner scores (r = 0.532, p = 0.041) in patients with CAI.ConclusionA reduced functional connection between the cingulate motor area and the insula was present in patients with CAI, which was also directly correlated with reduction in the level of patient physical activity.

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Section: Discussionmentioning

confidence: 99%

Neuroplasticity of pain processing and motor control in CAI patients: A UK Biobank study with clinical validation

Li¹,

Xue²,

Xu³

et al. 2023

Front. Mol. Neurosci.

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“…This spectrum of CPM capacity is likely to represent the balance between anti‐ and pro‐nociceptive mechanisms. A recent study highlighted this spread of nociceptive phenotypes from inhibition to facilitation in HC by using an approach of contrasting noxious conditioning to innocuous conditioning, that is, sham‐controlled design, (Huynh et al, 2021 ). With around two thirds of their study cohort being classified as inhibitors and one third being facilitators, our data revealed similar proportions.…”

Section: Discussionmentioning

confidence: 99%

“…Such an observed spread might prevent to reveal overall differences in CPM between pain cohorts and HC and begs the question of how inhibitors and facilitators can be generally distinguished or further characterized. For example, a recent study reported that grey matter volume and resting state connectivity of particular brain regions partially explains the variability in CPM capacity in HC (Huynh et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Anti‐ and Pro‐Nociceptive mechanisms in neuropathic pain after human spinal cord injury

Lütolf

Schoenmacker

Rösner

et al. 2022

European Journal of Pain

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BACKGROUND Deficient endogenous pain modulation and increased nociceptive excitability are key features of central sensitization and can be assessed in humans by conditioned pain modulation (CPM, anti-nociceptive) and temporal summation of pain (TSP, pro-nociceptive), respectively. This study aimed to investigate these measures as proxies for central sensitization in subjects with chronic neuropathic pain (NP) after spinal cord injury (SCI). METHODS In paraplegic subjects with NP (SCI-NP; n = 17) and healthy controls (HC; n = 17), parallel and sequential sham-controlled CPM paradigms were performed using pressure pain threshold at the hand, that is, above lesion level, as test stimulus. The conditioning stimulus was a noxious cold (verum) or lukewarm water bath (sham) applied contralaterally. Regarding pro-nociceptive mechanisms, a TSP protocol with individually-adjusted pressure pain stimuli at the thenar eminence was used. CPM and TSP magnitudes were related to intensity and spatial extent of spontaneous NP. RESULTS Neither the parallel nor sequential sham-controlled CPM paradigm showed any significant inhibition of above-level pressure pain thresholds for SCI-NP or HC. Accordingly, no group difference in CPM capacity was found, however, subjects with more intense spontaneous NP showed lower inhibitory CPM capacity. TSP was observed for both groups but was not enhanced in SCI-NP. CONCLUSIONS Our results do not support altered above-level anti-or pro-nociceptive mechanisms in SCI-NP compared with HC; however, they also highlight the relevance of spontaneous NP intensity with regards to the capacity of endogenous pain modulation in SCI subjects. SIGNIFICANCE Central sensitization encompasses deficient endogenous pain modulation and increased nociceptive excitability. These two mechanisms can be assessed in humans by conditioned pain modulation and temporal summation of pain, respectively. Our data demonstrates a lack of descending pain inhibition only in subjects with severe neuropathic pain which may hint towards central sensitization at spinal and/or supra-spinal levels. Disentangling the mechanisms of endogenous pain modulation and neuronal hyperexcitability might improve mechanism-based treatment of neuropathic pain in subjects with spinal cord injury.

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“…Many attempts to tackle the heterogeneity and non-specificity of FM manifestations have been made by describing this complex disease in terms of its subgroups, which vary in type and degree of physical and cognitive-affective symptoms 6 . The descending pain modulatory system (DPMS) facilitates or inhibits pain, comprising cortical and subcortical CNS regions such as the ventrolateral periaqueductal grey, rostroventral medulla, and anterior cingulate cortex, among other regions, with significant involvement of the prefrontal cortex (PFC) and motor cortex (MC) 7 , 8 . We previously reported that the dysfunction of the DPMS in women with FM was associated with higher functional connectivity (FC) between the left MC and bilateral PFC assessed by functional near-infrared spectroscopy (fNIRS) 9 .…”

Section: Introductionmentioning

confidence: 99%

“…We previously reported that the dysfunction of the DPMS in women with FM was associated with higher functional connectivity (FC) between the left MC and bilateral PFC assessed by functional near-infrared spectroscopy (fNIRS) 9 . Higher severity of FM symptoms has been associated with dysfunction of the DPMS 10 , the latter assessed by a standardized quantitative psychophysical protocol known as the conditioned pain modulation (CPM) test 7 , 10 .…”

Section: Introductionmentioning

confidence: 99%

Functional connectivity response to acute pain assessed by fNIRS is associated with BDNF genotype in fibromyalgia: an exploratory study

Franco

Venturini

Alves

et al. 2022

Sci Rep

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Fibromyalgia is a heterogenous primary pain syndrome whose severity has been associated with descending pain modulatory system (DPMS) function and functional connectivity (FC) between pain processing areas. The brain-derived neurotrophic factor (BDNF) Val66Met single nucleotide polymorphism has been linked to vulnerability to chronic pain. In this cross-sectional imaging genetics study, we investigated fibromyalgia, the relationship between BDNF Val66Met heterozygous genotypes (Val/Met), and the functional connectivity (FC) response pattern to acute pain stimulus in the motor (MC) and prefrontal (PFC) cortex assessed by near-infrared spectroscopy (fNIRS) before and after a cold pressor test utilizing water (0–1 °C). Also, we assessed the relationship between this genotype with the DPMS function and quality of life. We included 42 women (Val/Val = 30; Val/Met = 12) with fibromyalgia, ages 18–65. The MANCOVA comparing Val/Met to Val/Val genotypes showed higher ΔFC between left(l)-PFC—l-MC (β = 0.357, p = 0.048), l-PFC—right(r)-PFC (β = 0.249, p = 0.012), l-PFC—r-MC (β = 0.226, p = 0.022), and l-MC—r-PFC (β = 0.260, p = 0.016). Val/Met genotypes showed higher efficiency of the DPMS and lower disability due to pain. Here we show that fibromyalgia patients carrying the Val/Met BDNF genotype presented an increased ΔFC across MC and PFC in response to acute pain associated with differences in acute pain perception and fibromyalgia symptoms.

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Descending pain modulatory efficiency in healthy subjects is related to structure and resting connectivity of brain regions

Cited by 10 publications

References 82 publications

Neuroplasticity of pain processing and motor control in CAI patients: A UK Biobank study with clinical validation

Neuroplasticity of pain processing and motor control in CAI patients: A UK Biobank study with clinical validation

Anti‐ and Pro‐Nociceptive mechanisms in neuropathic pain after human spinal cord injury

Functional connectivity response to acute pain assessed by fNIRS is associated with BDNF genotype in fibromyalgia: an exploratory study

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