Temporal Filtering of Nociceptive Information by Dynamic Activation of Endogenous Pain Modulatory Systems

Yelle, Marc D.; Oshiro, Yasuo; Kraft, Robert A.; Coghill, Robert C.

doi:10.1523/jneurosci.4648-08.2009

Cited by 106 publications

(137 citation statements)

References 71 publications

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“…Functional magnetic resonance imaging studies have shown that several brain regions mediating pain relief are activated during induction of offset analgesia [74], and another study by Yelle et al [75] found increased activation of PAG, cerebellar regions, thalamus, dorsolateral prefrontal cortex, midcingulate cortex, and insular cortex.…”

Section: Offset Analgesiamentioning

confidence: 99%

Altered Central Sensitization and Pain Modulation in the CNS in Chronic Joint Pain

Arendt‐Nielsen

Skou

Nielsen

et al. 2015

Curr Osteoporos Rep

137

136

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Musculoskeletal pain disorders are the second largest contributor to global disability underlining the significance of effective treatments. However, treating chronic musculoskeletal pain, and chronic joint pain (osteoarthritis (OA)) in particular, is challenging as the underlying peripheral and central pain mechanisms are not fully understood, and safe and efficient analgesic drugs are not available. The pain associated with joint pain is highly individual, and features from radiological imaging have not demonstrated robust associations with the pain manifestations. In recent years, a variety of human quantitative pain assessment tools (quantitative sensory testing (QST)) have been developed providing new opportunities for profiling patients and reaching a greater understanding of the mechanisms involved in chronic joint pain. As joint pain is a complex interaction between many different pain mechanisms, available tools are important for patent profiling and providing the basic knowledge for development of new drugs and for developing pain management regimes.

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Section: Offset Analgesiamentioning

confidence: 99%

Altered Central Sensitization and Pain Modulation in the CNS in Chronic Joint Pain

Arendt‐Nielsen

Skou

Nielsen

et al. 2015

Curr Osteoporos Rep

137

136

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“…Functional imaging studies of CPM have identified reduced activity in several pain-processing areas including the thalamus, SI and SII as well as the anterior and middle cingulate cortex (ACC and MCC) and insula (INS) [28,30]. In contrast, OA reduces activity in SI, but produces greater activity in the periaqueductal gray (PAG), anterior INS, dorsalateral prefrontal cortex (DLPFC) and the MCC [7,42]. Since different noxious stimuli were applied across these different studies, it remains unclear if CPM and OA engage similar brain mechanisms of pain modulation.…”

Section: Introductionmentioning

confidence: 99%

Distinct brain mechanisms support spatial vs temporal filtering of nociceptive information

Nahman‐Averbuch

Martucci

Granovsky

et al. 2014

Pain

117

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The role of endogenous analgesic mechanisms has largely been viewed in the context of gain modulation during nociceptive processing. However, these analgesic mechanisms may play critical roles in the extraction and subsequent utilization of information related to spatial and temporal features of nociceptive input. To date, it remains unknown if spatial and temporal filtering of nociceptive information is supported by similar analgesic mechanisms. To address this question, human volunteers were recruited to assess brain activation with functional MRI during conditioned pain modulation (CPM) and offset analgesia (OA). CPM provides one paradigm for assessing spatial filtering of nociceptive information while OA provides a paradigm for assessing temporal filtering of nociceptive information. CPM and OA both produced statistically significant reductions in pain intensity. However, the magnitude of pain reduction elicited by CPM was not correlated with that elicited by OA across different individuals. Different patterns of brain activation were consistent with the psychophysical findings. CPM elicited widespread reductions in regions engaged in nociceptive processing such as the thalamus, insula and SII. OA produced reduced activity in SI, but was associated with greater activation in the anterior insula, dorso-lateral prefrontal cortex, intra-parietal sulcus, and inferior parietal lobule relative to CPM. In the brainstem, CPM consistently produced reductions in activity while OA produced increases in activity. Conjunction analysis confirmed that CPM related activity did not overlap with that of OA. Thus, dissociable mechanisms support inhibitory processes engaged during spatial vs. temporal filtering of nociceptive information.

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“…There are well-known dynamic effects in pain that occur during continuous or fast repetitive noxious stimulation, such as temporal summation 13, 17, 24, 29, 33, 40, 41, 53 and offset analgesia (the disproportionately large decrease in thermal pain following a slight decrease in stimulus temperature) 19, 63, 64 . Temporal pain adaptation also occurs during sequences of more widely spaced noxious stimuli (e.g., separated by 10–80 seconds).…”

Section: Introductionmentioning

confidence: 99%

The Dynamics of Pain: Evidence for Simultaneous Site-Specific Habituation and Site-Nonspecific Sensitization in Thermal Pain

Jepma

Jones

Wager

2014

The Journal of Pain

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Repeated exposure to noxious stimuli changes their painfulness, due to multiple adaptive processes in the peripheral and central nervous system. Somewhat paradoxically, repeated stimulation can produce an increase (sensitization) or a decrease (habituation) in pain. Adaptation processes may also be body-site-specific or operate across body sites, and considering this distinction may help explain the conditions under which habituation vs. sensitization occurs. To dissociate the effects of site-specific and site-nonspecific adaptation processes, we examined reported pain in 100 participants during counterbalanced sequences of noxious thermal stimulation on multiple skin sites. Analysis of pain ratings revealed two opposing sequential effects: repeated stimulations of the same skin site produced temperature-dependent habituation, whereas repeated stimulations across different sites produced sensitization. Stimulation trials were separated by ~20 seconds and sensitization was unrelated to the distance between successively stimulated sites, suggesting that neither temporal nor spatial summation occurred. To explain these effects, we propose a dynamic model with two adaptation processes, one site-specific and one site-nonspecific. The model explains 93% of the variance in the group-mean pain ratings after controlling for current stimulation temperature, with its estimated parameters showing evidence for habituation for the site-specific process and sensitization for the site-nonspecific process. The two pain-adaptation processes revealed in this study, and the ability to disentangle them, may hold keys to understanding multiple pain-regulatory mechanisms and their disturbance in chronic-pain syndromes. Perspective This article presents novel evidence for simultaneous site-specific habituation and site-nonspecific sensitization in thermal pain, which can be disentangled (and the direction and strength of each process estimated) by a dynamic model. The dissociation of site-specific and site-nonspecific adaptation processes may hold keys to understanding multiple pain-regulatory mechanisms in both healthy and patient populations.

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Temporal Filtering of Nociceptive Information by Dynamic Activation of Endogenous Pain Modulatory Systems

Cited by 106 publications

References 71 publications

Altered Central Sensitization and Pain Modulation in the CNS in Chronic Joint Pain

Altered Central Sensitization and Pain Modulation in the CNS in Chronic Joint Pain

Distinct brain mechanisms support spatial vs temporal filtering of nociceptive information

The Dynamics of Pain: Evidence for Simultaneous Site-Specific Habituation and Site-Nonspecific Sensitization in Thermal Pain

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