Altered neural activity to monetary reward/loss processing in episodic migraine

Kocsel, Natália; Galambos, Attila; Szabó, Emese; Édes, Andrea Edit; Magyar, Máté; Zsombók, Terézia; Pap, Dorottya; Kozák, Lajos R.; Bagdy, György; Kökönyei, Gyöngyi; Juhász, Gabriella

doi:10.1038/s41598-019-41867-x

Cited by 9 publications

(11 citation statements)

References 74 publications

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“… 4 Alongside these changes, studies point to abnormal reward processing in episodic migraine (EM) patients even during the interictal period, such as altered neural response to secondary (eg, monetary) reward/loss consumption. 5 Seemingly unrelated, it is evident that reward strongly interacts with pain through their overlapping neuroanatomical structures such as the amygdala and nucleus accumbens (NAc). 6 , 7 Chronic pain impairs the mesolimbic reward system, which leads to reduced motivated behaviors, negative affect, and further debilitating pain-related suffering.…”

Section: Introductionmentioning

confidence: 99%

Dopaminergic Regulation of Reward System Connectivity Underpins Pain and Emotional Suffering in Migraine

Kim¹,

Jassar²,

Lim³

et al. 2021

JPR

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Purpose It has been suggested that reward system dysfunction may account for emotion and pain suffering in migraine. However, there is a lack of evidence whether the altered reward system connectivity is directly associated with clinical manifestations, including negative affect and ictal pain severity and, at the molecular level, the dopamine (DA) D2/D3 receptors (D2/3Rs) signaling implicated in encoding motivational and emotional cues. Patients and Methods We acquired resting-state functional MRI from interictal episodic migraine (EM) patients and age-matched healthy controls, as well as positron emission tomography (PET) with [ 11 C]raclopride, a selective radiotracer for DA D2/3Rs, from a subset of these participants. The nucleus accumbens (NAc) was seeded to measure functional connectivity (FC) and DA D2/3Rs availability based on its essential involvement in pain-related aversive/reward functions. Associations of the brain measures with positive/negative affect and ictal pain severity were also assessed. Results Compared with controls, the EM group showed weaker right NAc connectivity with areas implicated in pain and emotional regulation, such as the amygdala, rostral anterior cingulate cortex, hippocampus, and thalamus; but showed stronger left NAc connectivity with the dorsolateral prefrontal cortex and lingual gyrus. Moreover, among the altered NAc connectivities, only right NAc-amygdala connectivity was inversely correlated with DA D2/3Rs availability in migraine patients (diagnostic group-by-D2/3Rs interaction p < 0.007). At a clinical level, such weaker NAc-amygdala connectivity was associated with lower interictal positive affect and greater ictal pain severity over the head and facial extension area (pain area and intensity number summation, PAINS). Conclusion Together, our findings suggest that altered reward system connectivity, specifically between the NAc and amygdala, might be affected by endogenous DA D2/3Rs signaling, and such process might be a neural mechanism that underlies emotional and pain suffering in episodic migraineurs.

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Section: Introductionmentioning

confidence: 99%

Dopaminergic Regulation of Reward System Connectivity Underpins Pain and Emotional Suffering in Migraine

Kim¹,

Jassar²,

Lim³

et al. 2021

JPR

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“…On average, 62 ± 36 participants (median 52 participants) were included per study. Of the identified studies, 68 studied groups with migraine without aura (23–90), 15 migraine with aura (30,31,35,36,…”

Section: Resultsmentioning

confidence: 99%

Functional magnetic resonance imaging in migraine: A systematic review

et al. 2023

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Background Migraine is a highly prevalent primary headache disorder. Despite a high burden of disease, key disease mechanisms are not entirely understood. Functional magnetic resonance imaging is an imaging method using the blood-oxygen-level-dependent signal, which has been increasingly used in migraine research over recent years. This systematic review summarizes recent findings employing functional magnetic resonance imaging for the investigation of migraine. Methods We conducted a systematic search and selection of functional magnetic resonance imaging applications in migraine from April 2014 to December 2021 (PubMed and references of identified articles according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines). Methodological details and main findings were extracted and synthesized. Results Out of 224 articles identified, 114 were included after selection. Repeatedly emerging structures of interest included the insula, brainstem, limbic system, hypothalamus, thalamus, and functional networks. Assessment of functional brain changes in response to treatment is emerging, and machine learning has been used to investigate potential functional magnetic resonance imaging-based markers of migraine. Conclusions A wide variety of functional magnetic resonance imaging-based metrics were found altered across the brain for heterogeneous migraine cohorts, partially correlating with clinical parameters and supporting the concept to conceive migraine as a brain state. However, a majority of findings from previous studies have not been replicated, and studies varied considerably regarding image acquisition and analyses techniques. Thus, while functional magnetic resonance imaging appears to have the potential to advance our understanding of migraine pathophysiology, replication of findings in large representative datasets and precise, standardized reporting of clinical data would likely benefit the field and further increase the value of observations.

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“…However, we cannot exclude the possibility that migraine-related variables other than migraine frequency had an association with anticipatory processes. For instance, previous findings showed that monetary loss anticipation was associated with the time of the last attack [ 91 ]. In addition, migraine cycle can also alter pain processing.…”

Section: Discussionmentioning

confidence: 99%

Inter-individual differences in pain anticipation and pain perception in migraine: Neural correlates of migraine frequency and cortisol-to-dehydroepiandrosterone sulfate (DHEA-S) ratio

et al. 2021

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Previous studies targeting inter-individual differences in pain processing in migraine mainly focused on the perception of pain. Our main aim was to disentangle pain anticipation and perception using a classical fear conditioning task, and investigate how migraine frequency and pre-scan cortisol-to-dehydroepiandrosterone sulfate (DHEA-S) ratio as an index of neurobiological stress response would relate to neural activation in these two phases. Functional Magnetic Resonance Imaging (fMRI) data of 23 participants (18 females; mean age: 27.61± 5.36) with episodic migraine without aura were analysed. We found that migraine frequency was significantly associated with pain anticipation in brain regions comprising the midcingulate and caudate, whereas pre-scan cortisol-to DHEA-S ratio was related to pain perception in the pre-supplementary motor area (pre-SMA). Both results suggest exaggerated preparatory responses to pain or more general to stressors, which may contribute to the allostatic load caused by stressors and migraine attacks on the brain.

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Altered neural activity to monetary reward/loss processing in episodic migraine

Cited by 9 publications

References 74 publications

Dopaminergic Regulation of Reward System Connectivity Underpins Pain and Emotional Suffering in Migraine

Dopaminergic Regulation of Reward System Connectivity Underpins Pain and Emotional Suffering in Migraine

Functional magnetic resonance imaging in migraine: A systematic review

Inter-individual differences in pain anticipation and pain perception in migraine: Neural correlates of migraine frequency and cortisol-to-dehydroepiandrosterone sulfate (DHEA-S) ratio

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