The altered right frontoparietal network functional connectivity in migraine and the modulation effect of treatment

Aims This study aims to investigate the resting-state functional connectivity (rs-fc) of the right frontoparietal network (rFPN) between migraineurs and healthy controls (HCs) in order to determine how the rFPN rs-fc can be modulated by effective treatment. Methods One hundred patients and 46 matched HCs were recruited. Migraineurs were randomized to verum acupuncture, sham acupuncture, and waiting list groups. Resting-state functional magnetic resonance imaging data were collected before and after longitudinal treatments. Independent component analysis was applied in the data analysis. Results We found that migraineurs showed decreased rs-fc between the rFPN and bilateral precuneus compared with HCs. After treatments (real and sham), rFPN rs-fc with the precuneus was significantly reduced. This reduction was associated with headache intensity relief. In order to explore the role of the precuneus in acupuncture modulation, we performed a seed-based rs-fc analysis using the precuneus as a seed and found that the precuneus rs-fc with the bilateral rostral anterior cingulate cortex/medial prefrontal cortex, ventral striatum, and dorsolateral prefrontal cortex was significantly enhanced after treatment. Conclusion Our results suggest that migraineurs are associated with abnormal rFPN rs-fc. An effective treatment, such as acupuncture, may relieve symptoms by strengthening the cognitive adaptation/coping process. Elucidation of the adaptation/coping mechanisms may open up a new window for migraine management.

[1]  Ying Li,et al.  Altered periaqueductal gray resting state functional connectivity in migraine and the modulation effect of treatment , 2016, Scientific Reports.

[2]  Randy L. Gollub,et al.  Repeated verum but not placebo acupuncture normalizes connectivity in brain regions dysregulated in chronic pain , 2015, NeuroImage: Clinical.

[3]  Ted J. Kaptchuk,et al.  Distinct neural representations of placebo and nocebo effects , 2015, NeuroImage.

[4]  C. Wallraven,et al.  When pain is not only pain: Inserting needles into the body evokes distinct reward-related brain responses in the context of a treatment , 2015, Physiology & Behavior.

[5]  Catherine D. Chong,et al.  Functional MRI of migraine , 2015, The Lancet Neurology.

[6]  Randy L. Gollub,et al.  Simultaneous fMRI–PET of the opioidergic pain system in human brain , 2014, NeuroImage.

[7]  X. Zuo,et al.  Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: A systems neuroscience perspective , 2014, Neuroscience & Biobehavioral Reviews.

[8]  V. Napadow,et al.  Disrupted functional connectivity of the periaqueductal gray in chronic low back pain , 2014, NeuroImage: Clinical.

[9]  S. Rombouts,et al.  Resting-state functional MR imaging: a new window to the brain. , 2014, Radiology.

[10]  D. Finn,et al.  Cognition and pain , 2014, Current opinion in supportive and palliative care.

[11]  Amanda V. Utevsky,et al.  Precuneus Is a Functional Core of the Default-Mode Network , 2014, The Journal of Neuroscience.

[12]  M. Baliki,et al.  Chronic pain: the role of learning and brain plasticity. , 2014, Restorative neurology and neuroscience.

[13]  B. Schlaggar,et al.  Allodynia and descending pain modulation in migraine: a resting state functional connectivity analysis. , 2014, Pain medicine.

[14]  R. Burstein,et al.  Migraine pathophysiology: Anatomy of the trigeminovascular pathway and associated neurological symptoms, cortical spreading depression, sensitization, and modulation of pain , 2013, PAIN®.

[15]  M. Bushnell,et al.  Cognitive and emotional control of pain and its disruption in chronic pain , 2013, Nature Reviews Neuroscience.

[16]  V. Napadow,et al.  The missing link: Enhanced functional connectivity between amygdala and visceroceptive cortex in migraine , 2013, Cephalalgia : an international journal of headache.

[17]  Yufeng Zang,et al.  Toward reliable characterization of functional homogeneity in the human brain: Preprocessing, scan duration, imaging resolution and computational space , 2013, NeuroImage.

[18]  David Borsook,et al.  Common hippocampal structural and functional changes in migraine , 2012, Brain Structure and Function.

[19]  Jie Tian,et al.  Intrinsic Brain Network Abnormalities in Migraines without Aura Revealed in Resting-State fMRI , 2012, PloS one.

[20]  H. Fields,et al.  Pain relief produces negative reinforcement through activation of mesolimbic reward–valuation circuitry , 2012, Proceedings of the National Academy of Sciences.

[21]  George Lewith,et al.  Acupuncture for chronic pain: individual patient data meta-analysis. , 2012, Archives of internal medicine.

[22]  F. Esposito,et al.  Executive resting-state network connectivity in migraine without aura , 2012, Cephalalgia : an international journal of headache.

[23]  Dania Vecchia,et al.  Migraine: a disorder of brain excitatory–inhibitory balance? , 2012, Trends in Neurosciences.

[24]  P. Goadsby,et al.  Pathophysiology of migraine , 2012, Annals of Indian Academy of Neurology.

[25]  M. Ingvar,et al.  Cognitive Behavioral Therapy increases pain-evoked activation of the prefrontal cortex in patients with fibromyalgeia , 2012, PAIN.

[26]  Hang Joon Jo,et al.  Trouble at Rest: How Correlation Patterns and Group Differences Become Distorted After Global Signal Regression , 2012, Brain Connect..

[27]  Acupuncture for migraine prophylaxis: a randomized controlled trial , 2012, Canadian Medical Association Journal.

[28]  Peter J. Goadsby,et al.  Chronic migraine—classification, characteristics and treatment , 2012, Nature Reviews Neurology.

[29]  L. Becerra,et al.  Understanding Migraine through the Lens of Maladaptive Stress Responses: A Model Disease of Allostatic Load , 2012, Neuron.

[30]  Jisheng Han.  Acupuncture analgesia: Areas of consensus and controversy , 2011, PAIN.

[31]  D. Finn,et al.  The effect of pain on cognitive function: A review of clinical and preclinical research , 2011, Progress in Neurobiology.

[32]  A. May,et al.  Trigeminal Nociceptive Transmission in Migraineurs Predicts Migraine Attacks , 2011, The Journal of Neuroscience.

[33]  Jian Kong,et al.  Intrinsic functional connectivity of the periaqueductal gray, a resting fMRI study , 2010, Behavioural Brain Research.

[34]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[35]  Justin L. Vincent,et al.  Precuneus shares intrinsic functional architecture in humans and monkeys , 2009, Proceedings of the National Academy of Sciences.

[36]  Ted J. Kaptchuk,et al.  An fMRI study on the interaction and dissociation between expectation of pain relief and acupuncture treatment , 2009, NeuroImage.

[37]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[38]  Yi Zhang,et al.  Combining spatial and temporal information to explore function‐guide action of acupuncture using fMRI , 2009, Journal of magnetic resonance imaging : JMRI.

[39]  F. Riederer,et al.  Quality of Sleep, Fatigue and Daytime Sleepiness in Migraine—A Controlled Study , 2009, Cephalalgia : an international journal of headache.

[40]  F. Andrasik,et al.  Psychological variables in chronic migraine with medication overuse before and after inpatient withdrawal: results at 1-year follow-up , 2009, Neurological Sciences.

[41]  P. Matthews,et al.  Distinct patterns of brain activity in young carriers of the APOE e4 allele , 2009, NeuroImage.

[42]  A. Vickers,et al.  Acupuncture for migraine prophylaxis , 2015, Sao Paulo medical journal = Revista paulista de medicina.

[43]  Ted J. Kaptchuk,et al.  Expectancy and treatment interactions: A dissociation between acupuncture analgesia and expectancy evoked placebo analgesia , 2008, NeuroImage.

[44]  G. Crombez,et al.  Coping with pain: A motivational perspective , 2008, PAIN.

[45]  K. Wiech,et al.  Neurocognitive aspects of pain perception , 2008, Trends in Cognitive Sciences.

[46]  I. Tracey,et al.  A common neurobiology for pain and pleasure , 2008, Nature Reviews Neuroscience.

[47]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[48]  Jian Kong,et al.  Acupuncture de qi, from qualitative history to quantitative measurement. , 2007, Journal of alternative and complementary medicine.

[49]  Robert C. Coghill,et al.  Attentional Modulation of Spatial Integration of Pain: Evidence for Dynamic Spatial Tuning , 2007, The Journal of Neuroscience.

[50]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[51]  Daniel S. Margulies,et al.  Mapping the functional connectivity of anterior cingulate cortex , 2007, NeuroImage.

[52]  Scott T. Grafton,et al.  Response to Comment on "Wandering Minds: The Default Network and Stimulus-Independent Thought" , 2007, Science.

[53]  L. Stovner,et al.  Prevalence, burden, and cost of headache disorders , 2006, Current opinion in neurology.

[54]  R. Lipton,et al.  The global burden of migraine: measuring disability in headache disorders with WHO's Classification of Functioning, Disability and Health (ICF) , 2005, The Journal of Headache and Pain.

[55]  P. Westerhuis,et al.  The International Classification of Headache Disorders (2nd ed.) , 2004 .

[56]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[57]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[58]  J. Pascual,et al.  Quality of life in chronic daily headache: A study in a general population , 2002, Neurology.

[59]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[60]  M. Catherine Bushnell,et al.  Cognitive modulation of pain: how do attention and emotion influence pain processing? , 2002, Pain.

[61]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[62]  W. Spoerel,et al.  Acupuncture in chronic pain. , 1976, The American journal of Chinese medicine.