Highlights
- •The potential effects of white matter changes on functional responses to pain are highlighted.
- •Brain structure and function were explored without microstructural changes seen in chronic pain.
- •These findings can inform the design of future experiments on midcingulate cortex function and pain.
Abstract
Despite a fundamental interest in the relationship between structure and function,
the relationships between measures of white matter microstructural coherence and functional
brain responses to pain are poorly understood. We investigated whether fractional
anisotropy (FA) in 2 white matter regions in pathways associated with pain is related
to the functional magnetic resonance imaging (fMRI) blood oxygen level-dependent (BOLD)
response to thermal stimulation. BOLD fMRI was measured from 16 healthy male subjects
during painful thermal stimulation of the right arm. Diffusion-weighted images were
acquired for each subject and FA estimates were extracted from the posterior internal
capsule and the cingulum (cingulate gyrus). These values were then included as covariates
in the fMRI data analysis. We found BOLD response in the midcingulate cortex (MCC)
to be positively related to FA in the posterior internal capsule and negatively related
to FA in the cingulum. Our results suggest that the MCC's involvement in processing
pain can be further delineated by considering how the magnitude of the BOLD response
is related to white matter microstructural coherence and to subjective perception
of pain. Considering relationships to white matter microstructural coherence in tracts
involved in transmitting information to different parts of the pain network can help
interpretation of MCC BOLD activation.
Perspective
Relationships between functional brain responses, white matter microstructural coherence,
and subjective ratings are crucial for understanding the role of the MCC in pain.
These findings provide a basis for investigating the effect of the reduced white matter
microstructural coherence observed in some pain disorders on the functional responses
to pain.
Key words
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References
- Human brain mechanisms of pain perception and regulation in health and disease.Eur J Pain. 2005; 9: 463-484
- Pain and the brain: Specificity and plasticity of the brain in clinical chronic pain.Pain. 2011; 152: S49-S64
- Manual for the Beck Depression Inventory-II.Psychological Corporation, San Antonio, TX1996
- Age-related differences in multiple measures of white matter integrity: A diffusion tensor imaging study of healthy aging.Hum Brain Mapp. 2010; 31: 378-390
- Habituation to painful stimulation involves the antinociceptive system–a 1-year follow-up of 10 participants.Pain. 2008; 140: 393-394
- Microstructural brain differences predict functional hemodynamic responses in a reward processing task.J Neurosci. 2010; 30: 11398-11402
- Pain intensity processing within the human brain: A bilateral, distributed mechanism.J Neurophysiol. 1999; 82: 1934-1943
- Statistical Power Analysis for the Behavioral Sciences.2nd ed. Erlbaum Associates, Hillsdale, NJ, L1988
- Central mechanisms of pain revealed through functional and structural MRI.J Neuroimmune Pharmacol. 2013; 8: 518-534
- Neural underpinnings of behavioural strategies that prioritize either cognitive task performance or pain.Pain. 2013; 154: 2060-2071
- Cortical thickness correlates of pain and temperature sensitivity.Pain. 2012; 153: 1602-1609
- Myelination: An overlooked mechanism of synaptic plasticity?.Neuroscientist. 2005; 11: 528-531
- Neuroscience. Change in the brain’s white matter.Science. 2010; 330: 768-769
- Improved assessment of significant activation in functional magnetic-resonance-imaging (fMRI): Use of a cluster-size threshold.Magn Reson Med. 1995; 33: 636-647
- Assessing the significance of focal activations using their spatial extent.Hum Brain Mapp. 1993; 1: 210-220
- Localization of function in anterior cingulate cortex: From psychosurgery to functional neuroimaging.Neurosci Biobehav Rev. 2013; 37: 340-348
- Tractography-guided stimulation of somatosensory fibers for thalamic pain relief.Stereotact Funct Neurosurg. 2013; 91: 328-334
- Improved optimization for the robust and accurate linear registration and motion correction of brain images.Neuroimage. 2002; 17: 825-841
- A global optimisation method for robust affine registration of brain images.Med Image Anal. 2001; 5: 143-156
- Diffusion MRI: Theory, Methods, and Applications.Oxford University Press, Oxford2011
- Distinct subdivisions of the cingulum bundle revealed by diffusion MRI fibre tracking: Implications for neuropsychological investigations.Neuropsychologia. 2013; 51: 67-78
- The structural basis of inter-individual differences in human behaviour and cognition.Nat Rev Neurosci. 2011; 12: 231-242
- The B-matrix must be rotated when correcting for subject motion in DTI data.Magn Reson Med. 2009; 61: 1336-1349
- Cerebral white matter integrity and cognitive aging: Contributions from diffusion tensor imaging.Neuropsychol Rev. 2009; 19: 415-435
- Robust tensor estimation in diffusion tensor imaging.J Magn Reson. 2011; 213: 136-144
- Statistical instability of TBSS analysis based on DTI fitting algorithm.J Neuroimaging. 2015; 25: 883-891
- Chronic pain may change the structure of the brain.Pain. 2008; 137: 7-15
- Neuroimaging evidence of motor control and pain processing in the human midcingulate cortex.Cerebral Cortex. 2015; 25: 1906-1919
- White matter brain and trigeminal nerve abnormalities in temporomandibular disorder.Pain. 2012; 153: 1467-1477
- Anatomical connections between brain areas activated during rectal distension in healthy volunteers: A visceral pain network.Eur J Pain. 2010; 14: 142-148
- MRI Atlas of Human White Matter.Elsevier, Amsterdam2005
- Painful heat reveals hyperexcitability of the temporal pole in interictal and ictal migraine states.Cerebral Cortex. 2011; 21: 435-448
- A multisensory investigation of the functional significance of the “pain matrix”.Neuroimage. 2011; 54: 2237-2249
- Intelligence and neural efficiency.Neurosci Biobehav Rev. 2009; 33: 1004-1023
- The assessment and analysis of handedness: The Edinburgh inventory.Neuropsychologia. 1971; 9: 97-113
- Multimodal image analysis of sensorimotor gating in healthy women.Brain Res. 2013; 1499: 61-68
- Comprehensive approach for correction of motion and distortion in diffusion-weighted MRI.Magn Reson Med. 2004; 51: 103-114
- Improving lesion-symptom mapping.J Cogn Neurosci. 2007; 19: 1081-1088
- Diagnostic and Statistical Manual of Mental Disorders DSM-IV.(German version) [in German] Hogrefe, Goettingen1996
- White matter correlates of cognitive domains in normal aging with diffusion tensor imaging.Front Neurosci. 2013; 7: 32
- Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems.Cortex. 2008; 44: 1037-1066
- Fast robust automated brain extraction.Hum Brain Mapp. 2002; 17: 143-155
- Advances in functional and structural MR image analysis and implementation as FSL.Neuroimage. 2004; 23: S208-S219
- Manual for the State-Trait Anxiety Inventory.Consulting Psychologists Press, Palo Alto, CA1983
- Fiber tracking functionally distinct components of the internal capsule.Neuropsychologia. 2010; 48: 4155-4163
- Mechanisms of white matter changes induced by meditation.Proc Natl Acad Sci U S A. 2012; 109: 10570-10574
- Changes in brain gray matter due to repetitive painful stimulation.Neuroimage. 2008; 42: 845-849
- How neuroimaging studies have challenged us to rethink: Is chronic pain a disease?.J Pain. 2009; 10: 1113-1120
- Microstructural organization of the cingulum tract and the level of default mode functional connectivity.J Neurosci. 2008; 28: 10844-10851
- Assessment of corticospinal tract (CST) damage in acute stroke patients: Comparison of tract-specific analysis versus segmentation of a CST template.J Magn Reson Imaging. 2013; 37: 836-845
- Regions and subregions of the cingulate cortex.in: Vogt B.A. Cingulate Neurobiology and Disease. Oxford University Press, New York2009: 5-30
- Cingulate nociceptive circuitry and roles in pain processing: The cingulate premotor pain model.in: Vogt B.A. Cingulate Neurobiology and Disease. Oxford University Press, New York2009: 312-338
- The Axon: Structure, Function and Pathophysiology.Oxford University Press, New York, NY1995
- Bayesian analysis of neuroimaging data in FSL.Neuroimage. 2009; 45: S173-S186
- Temporal autocorrelation in univariate linear modeling of FMRI data.Neuroimage. 2001; 14: 1370-1386
- A three-dimensional statistical analysis for CBF activation studies in human brain.J Cereb Blood Flow Metab. 1992; 12: 900-918
Article info
Publication history
Published online: April 18, 2016
Accepted:
March 5,
2016
Received in revised form:
February 21,
2016
Received:
December 9,
2014
Footnotes
Current address for Ivan I. Maximov: Experimental Physics III, TU Dortmund University, Dortmund, Germany.
The work reported was made possible by institutional funding as part of the Programme Oriented Funding provided by the Helmholtz Society. N.J.S. is funded in part by the Helmholtz Alliance ICEMED—Imaging and Curing Environmental Metabolic Diseases, through the Initiative and Network Fund of the Helmholtz Association, and in part through the EU FP7 project TRIMAGE (grant number 602621).
The authors have no conflicts of interest to declare.
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© 2016 by the American Pain Society
