Aberrant Salience? Brain Hyperactivation in Response to Pain Onset and Offset in Fibromyalgia
Objective While much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased pain‐related brain activity often reported in FM studies may be partially explained by stronger responses to salient aspects of the stimula...
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| Published in | Arthritis & rheumatology (Hoboken, N.J.) Vol. 72; no. 7; pp. 1203 - 1213 |
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| Main Authors | , , , , , , |
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| Language | English |
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01.07.2020
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| Abstract | Objective
While much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased pain‐related brain activity often reported in FM studies may be partially explained by stronger responses to salient aspects of the stimulation rather than, or in addition to, the stimulation's painfulness. Therefore, this study was undertaken to test our hypothesis that FM patients would demonstrate elevated brain responses to both pain onset and offset—2 salient sensory events of opposing valences.
Methods
Thirty‐eight FM patients (mean ± SD age 46.1 ± 13.4 years; 33 women) and 15 healthy controls (mean ± SD age 45.5 ± 12.4; 10 women) received a moderately painful pressure stimulus to the leg during blood oxygen level–dependent (BOLD) functional magnetic resonance imaging. Stimulus onset and offset transients were analyzed using a general linear model as stick functions.
Results
During pain onset, higher BOLD signal response was observed in FM patients compared to healthy controls in dorsolateral and ventrolateral prefrontal cortices (DLPFC and VLPFC, respectively), orbitofrontal cortex (OFC), frontal pole, and precentral gyrus (PrCG). During pain offset, higher and more widespread BOLD signal response was demonstrated in FM patients compared to controls in frontal regions significantly hyperactivated in response to onset. In FM patients, some of these responses were positively correlated with pain unpleasantness ratings (VLPFC, onset; r = 0.35, P = 0.03), pain catastrophizing scores (DLPFC, offset; r = 0.33, P = 0.04), or negatively correlated with stimulus intensity (OFC, offset; r = −0.35, P = 0.03) (PrCG, offset; r = −0.39, P = 0.02).
Conclusion
Our results suggest that the increased sensitivity exhibited by FM patients in response to the onset and offset of painful stimuli may reflect a more generalized hypersensitivity to salient sensory events, and that brain hyperactivation may be a mechanism potentially involved in the generalized hypervigilance to salient stimuli in FM. |
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| AbstractList | OBJECTIVEWhile much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased pain-related brain activity often reported in FM studies may be partially explained by stronger responses to salient aspects of the stimulation rather than, or in addition to, the stimulation's painfulness. Therefore, this study was undertaken to test our hypothesis that FM patients would demonstrate elevated brain responses to both pain onset and offset-2 salient sensory events of opposing valences. METHODSThirty-eight FM patients (mean ± SD age 46.1 ± 13.4 years; 33 women) and 15 healthy controls (mean ± SD age 45.5 ± 12.4; 10 women) received a moderately painful pressure stimulus to the leg during blood oxygen level-dependent (BOLD) functional magnetic resonance imaging. Stimulus onset and offset transients were analyzed using a general linear model as stick functions. RESULTSDuring pain onset, higher BOLD signal response was observed in FM patients compared to healthy controls in dorsolateral and ventrolateral prefrontal cortices (DLPFC and VLPFC, respectively), orbitofrontal cortex (OFC), frontal pole, and precentral gyrus (PrCG). During pain offset, higher and more widespread BOLD signal response was demonstrated in FM patients compared to controls in frontal regions significantly hyperactivated in response to onset. In FM patients, some of these responses were positively correlated with pain unpleasantness ratings (VLPFC, onset; r = 0.35, P = 0.03), pain catastrophizing scores (DLPFC, offset; r = 0.33, P = 0.04), or negatively correlated with stimulus intensity (OFC, offset; r = -0.35, P = 0.03) (PrCG, offset; r = -0.39, P = 0.02). CONCLUSIONOur results suggest that the increased sensitivity exhibited by FM patients in response to the onset and offset of painful stimuli may reflect a more generalized hypersensitivity to salient sensory events, and that brain hyperactivation may be a mechanism potentially involved in the generalized hypervigilance to salient stimuli in FM. Objective While much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased pain‐related brain activity often reported in FM studies may be partially explained by stronger responses to salient aspects of the stimulation rather than, or in addition to, the stimulation's painfulness. Therefore, this study was undertaken to test our hypothesis that FM patients would demonstrate elevated brain responses to both pain onset and offset—2 salient sensory events of opposing valences. Methods Thirty‐eight FM patients (mean ± SD age 46.1 ± 13.4 years; 33 women) and 15 healthy controls (mean ± SD age 45.5 ± 12.4; 10 women) received a moderately painful pressure stimulus to the leg during blood oxygen level–dependent (BOLD) functional magnetic resonance imaging. Stimulus onset and offset transients were analyzed using a general linear model as stick functions. Results During pain onset, higher BOLD signal response was observed in FM patients compared to healthy controls in dorsolateral and ventrolateral prefrontal cortices (DLPFC and VLPFC, respectively), orbitofrontal cortex (OFC), frontal pole, and precentral gyrus (PrCG). During pain offset, higher and more widespread BOLD signal response was demonstrated in FM patients compared to controls in frontal regions significantly hyperactivated in response to onset. In FM patients, some of these responses were positively correlated with pain unpleasantness ratings (VLPFC, onset; r = 0.35, P = 0.03), pain catastrophizing scores (DLPFC, offset; r = 0.33, P = 0.04), or negatively correlated with stimulus intensity (OFC, offset; r = −0.35, P = 0.03) (PrCG, offset; r = −0.39, P = 0.02). Conclusion Our results suggest that the increased sensitivity exhibited by FM patients in response to the onset and offset of painful stimuli may reflect a more generalized hypersensitivity to salient sensory events, and that brain hyperactivation may be a mechanism potentially involved in the generalized hypervigilance to salient stimuli in FM. Objective While much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased pain‐related brain activity often reported in FM studies may be partially explained by stronger responses to salient aspects of the stimulation rather than, or in addition to, the stimulation's painfulness. Therefore, this study was undertaken to test our hypothesis that FM patients would demonstrate elevated brain responses to both pain onset and offset—2 salient sensory events of opposing valences. Methods Thirty‐eight FM patients (mean ± SD age 46.1 ± 13.4 years; 33 women) and 15 healthy controls (mean ± SD age 45.5 ± 12.4; 10 women) received a moderately painful pressure stimulus to the leg during blood oxygen level–dependent (BOLD) functional magnetic resonance imaging. Stimulus onset and offset transients were analyzed using a general linear model as stick functions. Results During pain onset, higher BOLD signal response was observed in FM patients compared to healthy controls in dorsolateral and ventrolateral prefrontal cortices (DLPFC and VLPFC, respectively), orbitofrontal cortex (OFC), frontal pole, and precentral gyrus (PrCG). During pain offset, higher and more widespread BOLD signal response was demonstrated in FM patients compared to controls in frontal regions significantly hyperactivated in response to onset. In FM patients, some of these responses were positively correlated with pain unpleasantness ratings (VLPFC, onset; r = 0.35, P = 0.03), pain catastrophizing scores (DLPFC, offset; r = 0.33, P = 0.04), or negatively correlated with stimulus intensity (OFC, offset; r = −0.35, P = 0.03) (PrCG, offset; r = −0.39, P = 0.02). Conclusion Our results suggest that the increased sensitivity exhibited by FM patients in response to the onset and offset of painful stimuli may reflect a more generalized hypersensitivity to salient sensory events, and that brain hyperactivation may be a mechanism potentially involved in the generalized hypervigilance to salient stimuli in FM. ObjectiveWhile much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased pain‐related brain activity often reported in FM studies may be partially explained by stronger responses to salient aspects of the stimulation rather than, or in addition to, the stimulation's painfulness. Therefore, this study was undertaken to test our hypothesis that FM patients would demonstrate elevated brain responses to both pain onset and offset—2 salient sensory events of opposing valences.MethodsThirty‐eight FM patients (mean ± SD age 46.1 ± 13.4 years; 33 women) and 15 healthy controls (mean ± SD age 45.5 ± 12.4; 10 women) received a moderately painful pressure stimulus to the leg during blood oxygen level–dependent (BOLD) functional magnetic resonance imaging. Stimulus onset and offset transients were analyzed using a general linear model as stick functions.ResultsDuring pain onset, higher BOLD signal response was observed in FM patients compared to healthy controls in dorsolateral and ventrolateral prefrontal cortices (DLPFC and VLPFC, respectively), orbitofrontal cortex (OFC), frontal pole, and precentral gyrus (PrCG). During pain offset, higher and more widespread BOLD signal response was demonstrated in FM patients compared to controls in frontal regions significantly hyperactivated in response to onset. In FM patients, some of these responses were positively correlated with pain unpleasantness ratings (VLPFC, onset; r = 0.35, P = 0.03), pain catastrophizing scores (DLPFC, offset; r = 0.33, P = 0.04), or negatively correlated with stimulus intensity (OFC, offset; r = −0.35, P = 0.03) (PrCG, offset; r = −0.39, P = 0.02).ConclusionOur results suggest that the increased sensitivity exhibited by FM patients in response to the onset and offset of painful stimuli may reflect a more generalized hypersensitivity to salient sensory events, and that brain hyperactivation may be a mechanism potentially involved in the generalized hypervigilance to salient stimuli in FM. While much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased pain-related brain activity often reported in FM studies may be partially explained by stronger responses to salient aspects of the stimulation rather than, or in addition to, the stimulation's painfulness. Therefore, this study was undertaken to test our hypothesis that FM patients would demonstrate elevated brain responses to both pain onset and offset-2 salient sensory events of opposing valences. Thirty-eight FM patients (mean ± SD age 46.1 ± 13.4 years; 33 women) and 15 healthy controls (mean ± SD age 45.5 ± 12.4; 10 women) received a moderately painful pressure stimulus to the leg during blood oxygen level-dependent (BOLD) functional magnetic resonance imaging. Stimulus onset and offset transients were analyzed using a general linear model as stick functions. During pain onset, higher BOLD signal response was observed in FM patients compared to healthy controls in dorsolateral and ventrolateral prefrontal cortices (DLPFC and VLPFC, respectively), orbitofrontal cortex (OFC), frontal pole, and precentral gyrus (PrCG). During pain offset, higher and more widespread BOLD signal response was demonstrated in FM patients compared to controls in frontal regions significantly hyperactivated in response to onset. In FM patients, some of these responses were positively correlated with pain unpleasantness ratings (VLPFC, onset; r = 0.35, P = 0.03), pain catastrophizing scores (DLPFC, offset; r = 0.33, P = 0.04), or negatively correlated with stimulus intensity (OFC, offset; r = -0.35, P = 0.03) (PrCG, offset; r = -0.39, P = 0.02). Our results suggest that the increased sensitivity exhibited by FM patients in response to the onset and offset of painful stimuli may reflect a more generalized hypersensitivity to salient sensory events, and that brain hyperactivation may be a mechanism potentially involved in the generalized hypervigilance to salient stimuli in FM. |
| Author | Hubbard, Catherine S. Lazaridou, Asimina Napadow, Vitaly Cahalan, Christine M. Kim, Jieun Loggia, Marco L. Edwards, Robert R. |
| AuthorAffiliation | 3 Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, HMS, Boston, MA 4 Department of Psychiatry, Brigham and Women’s Hospital, HMS, Boston, MA 1 MGH/MIT/HMS Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, MA 2 Department of Radiology, Harvard Medical School (HMS), Massachusetts General Hospital, Boston, MA |
| AuthorAffiliation_xml | – name: 2 Department of Radiology, Harvard Medical School (HMS), Massachusetts General Hospital, Boston, MA – name: 3 Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, HMS, Boston, MA – name: 1 MGH/MIT/HMS Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, MA – name: 4 Department of Psychiatry, Brigham and Women’s Hospital, HMS, Boston, MA |
| Author_xml | – sequence: 1 givenname: Catherine S. surname: Hubbard fullname: Hubbard, Catherine S. organization: Harvard Medical School and Massachusetts General Hospital – sequence: 2 givenname: Asimina surname: Lazaridou fullname: Lazaridou, Asimina organization: Brigham and Women's Hospital – sequence: 3 givenname: Christine M. surname: Cahalan fullname: Cahalan, Christine M. organization: Brigham and Women's Hospital – sequence: 4 givenname: Jieun surname: Kim fullname: Kim, Jieun organization: Massachusetts General Hospital – sequence: 5 givenname: Robert R. surname: Edwards fullname: Edwards, Robert R. organization: Brigham and Women's Hospital and Harvard Medical School – sequence: 6 givenname: Vitaly surname: Napadow fullname: Napadow, Vitaly organization: Massachusetts General Hospital, and Brigham and Women's Hospital – sequence: 7 givenname: Marco L. orcidid: 0000-0002-8026-5265 surname: Loggia fullname: Loggia, Marco L. email: marco.loggia@mgh.harvard.edu organization: Massachusetts General Hospital, and Brigham and Women's Hospital |
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| CitedBy_id | crossref_primary_10_1016_j_neubiorev_2023_105235 crossref_primary_10_2147_JPR_S290795 crossref_primary_10_1002_art_42013 crossref_primary_10_4103_1673_5374_322471 crossref_primary_10_2139_ssrn_4179156 crossref_primary_10_1002_ejp_1820 crossref_primary_10_1002_art_41405 crossref_primary_10_1155_2022_7355102 crossref_primary_10_3390_rheumato2030007 crossref_primary_10_1097_j_pain_0000000000002387 crossref_primary_10_3390_jcm10153277 crossref_primary_10_1007_s10072_021_05806_x crossref_primary_10_3389_fnint_2022_920271 crossref_primary_10_1016_j_jpain_2023_05_006 crossref_primary_10_1111_1756_185X_15066 crossref_primary_10_3389_fpain_2021_627860 crossref_primary_10_1111_1756_185X_14293 |
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While much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the... While much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased... ObjectiveWhile much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased... OBJECTIVEWhile much brain research on fibromyalgia (FM) focuses on the study of hyperresponsiveness to painful stimuli, some studies suggest that the increased... |
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| SubjectTerms | Brain Brain mapping Cortex (frontal) Cortex (somatosensory) Fibromyalgia Functional magnetic resonance imaging Hypersensitivity Magnetic resonance imaging Neuroimaging Pain Precentral gyrus Stimulation Stimuli |
| Title | Aberrant Salience? Brain Hyperactivation in Response to Pain Onset and Offset in Fibromyalgia |
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