Brain white matter structural properties predict transition to chronic pain.

doi:10.1016/J.PAIN.2013.06.044

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Brain white matter structural properties predict transition to chronic pain.

Journal Article•DOI•

Brain white matter structural properties predict transition to chronic pain.

Ali Mansour¹, Marwan N. Baliki¹, Lejian Huang¹, Souraya Torbey¹, Kristi M. Herrmann¹, Thomas J. Schnitzer¹, A. Vania Apkarian¹ - Show less +3 more•Institutions (1)

Northwestern University¹

01 Oct 2013-Pain (NIH Public Access)-Vol. 154, Iss: 10, pp 2160-2168

TL;DR: It is concluded that brain structural differences, most likely existing before the back pain–inciting event and independent of the backPain, predispose subjects to pain chronification.

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Abstract: Neural mechanisms mediating the transition from acute to chronic pain remain largely unknown. In a longitudinal brain imaging study, we followed up patients with a single sub-acute back pain (SBP) episode for more than 1 year as their pain recovered (SBPr), or persisted (SBPp) representing a transition to chronic pain. We discovered brain white matter structural abnormalities (n=24 SBP patients; SBPp=12 and SBPr=12), as measured by diffusion tensor imaging (DTI), at entry into the study in SBPp in comparison to SBPr. These white matter fractional anisotropy (FA) differences accurately predicted pain persistence over the next year, which was validated in a second cohort (n=22 SBP patients; SBPp=11 and SBPr=11), and showed no further alterations over a 1-year period. Tractography analysis indicated that abnormal regional FA was linked to differential structural connectivity to medial vs lateral prefrontal cortex. Local FA was correlated with functional connectivity between medial prefrontal cortex and nucleus accumbens in SBPr. As we have earlier shown that the latter functional connectivity accurately predicts transition to chronic pain, we can conclude that brain structural differences, most likely existing before the back pain-inciting event and independent of the back pain, predispose subjects to pain chronification.

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Journal Article•DOI•

Nociception, pain, negative moods and behavior selection

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Marwan N. Baliki¹, A. Vania Apkarian¹•Institutions (1)

Northwestern University¹

05 Aug 2015-Neuron

TL;DR: This work deconstructs chronic pain into four distinct phases, each with specific mechanisms, and outlines current state of knowledge regarding these mechanisms: the limbic brain imparting risk, and the mesolimbic learning processes reorganizing the neocortex into a chronic pain state.

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451 citations

Cites background or methods or result from "Brain white matter structural prope..."

...Decreases in hippocampus and amygdala volumes have also been described in posttraumatic stress disorder (PTSD) (Chao et al., 2013, 2014; Gilbertson et al., 2002; Starcevic et al., 2014), and white matter microstructural predispositions in PTSD indicate that such structural differences reflect long-term vulnerability (Sekiguchi et al., 2014), as also observed for CBP (Mansour et al., 2013)....
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...The model is also intentionally kept as simple as possible becausemuch detail remains to be uncovered....
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...It should be noted, however, that this study remains one of a kind and thus awaits replication in other chronic pain conditions....
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...However, from the viewpoint of the current perspective, we can assert that these studies generally have not differentiated between nociception and pain, and ignored much of the rest of the brain, especially the limbic brain....
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...Approximately 10 years ago, we discovered regional anatomical brain abnormalities that correlated with intensity and duration in patients with chronic back pain (CBP) (Apkarian et al., 2004)....
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Journal Article•DOI•

Structural plasticity and reorganisation in chronic pain.

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Rohini Kuner¹, Herta Flor²•Institutions (2)

Heidelberg University¹, University of Mannheim²

01 Jan 2017-Nature Reviews Neuroscience

TL;DR: This Review discusses maladaptive structural plasticity in neural circuits of pain, spanning multiple anatomical and spatial scales in animal models and human patients, and addresses key questions on structure–function relationships.

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Abstract: Chronic pain is not simply a temporal continuum of acute pain. Studies on functional plasticity in neural circuits of pain have provided mechanistic insights and linked various modulatory factors to a change in perception and behaviour. However, plasticity also occurs in the context of structural remodelling and reorganisation of synapses, cells and circuits, potentially contributing to the long-term nature of chronic pain. This Review discusses maladaptive structural plasticity in neural circuits of pain, spanning multiple anatomical and spatial scales in animal models and human patients, and addresses key questions on structure-function relationships.

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409 citations

Journal Article•DOI•

Role of the Prefrontal Cortex in Pain Processing.

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Wei-Yi Ong¹, Christian S. Stohler², Deron R. Herr¹•Institutions (2)

National University of Singapore¹, Columbia University²

01 Feb 2019-Molecular Neurobiology

TL;DR: The medial PFC (mPFC) could serve dual, opposing roles in pain: it mediates antinociceptive effects, due to its connections with other cortical areas, and as the main source of cortical afferents to the PAG for modulation of pain.

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Abstract: The prefrontal cortex (PFC) is not only important in executive functions, but also pain processing. The latter is dependent on its connections to other areas of the cerebral neocortex, hippocampus, periaqueductal gray (PAG), thalamus, amygdala, and basal nuclei. Changes in neurotransmitters, gene expression, glial cells, and neuroinflammation occur in the PFC during acute and chronic pain, that result in alterations to its structure, activity, and connectivity. The medial PFC (mPFC) could serve dual, opposing roles in pain: (1) it mediates antinociceptive effects, due to its connections with other cortical areas, and as the main source of cortical afferents to the PAG for modulation of pain. This is a 'loop' where, on one side, a sensory stimulus is transformed into a perceptual signal through high brain processing activity, and perceptual activity is then utilized to control the flow of afferent sensory stimuli at their entrance (dorsal horn) to the CNS. (2) It could induce pain chronification via its corticostriatal projection, possibly depending on the level of dopamine receptor activation (or lack of) in the ventral tegmental area-nucleus accumbens reward pathway. The PFC is involved in biopsychosocial pain management. This includes repetitive transcranial magnetic stimulation, transcranial direct current stimulation, antidepressants, acupuncture, cognitive behavioral therapy, mindfulness, music, exercise, partner support, empathy, meditation, and prayer. Studies demonstrate the role of the PFC during placebo analgesia, and in establishing links between pain and depression, anxiety, and loss of cognition. In particular, losses in PFC grey matter are often reversible after successful treatment of chronic pain.

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355 citations

Journal Article•DOI•

Pain vulnerability: a neurobiological perspective

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Franziska Denk¹, Stephen B. McMahon¹, Irene Tracey²•Institutions (2)

Wolfson Centre for Age-Related Diseases¹, University of Oxford²

01 Feb 2014-Nature Neuroscience

TL;DR: Particular focus will be given to genetic and epigenetic processes, priming effects on a cellular level, and alterations in brain networks concerned with reward, motivation/learning and descending modulatory control.

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Abstract: There are many known risk factors for chronic pain conditions, yet the biological underpinnings that link these factors to abnormal processing of painful signals are only just beginning to be explored. This Review will discuss the potential mechanisms that have been proposed to underlie vulnerability and resilience toward developing chronic pain. Particular focus will be given to genetic and epigenetic processes, priming effects on a cellular level, and alterations in brain networks concerned with reward, motivation/learning and descending modulatory control. Although research in this area is still in its infancy, a better understanding of how pain vulnerability emerges has the potential to help identify individuals at risk and may open up new therapeutic avenues.

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282 citations

Journal Article•DOI•

Corticolimbic anatomical characteristics predetermine risk for chronic pain

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Etienne Vachon-Presseau¹, Pascal Tétreault¹, Bogdan Petre¹, Lejian Huang¹, Sara E. Berger¹, Souraya Torbey², Alexis T. Baria¹, Ali Mansour¹, Javeria A. Hashmi³, James W. Griffith¹, Erika Comasco⁴, Thomas J. Schnitzer¹, Marwan N. Baliki¹, A. Vania Apkarian¹ - Show less +10 more•Institutions (4)

Northwestern University¹, University of Virginia², Dalhousie University³, Science for Life Laboratory⁴

01 Jul 2016-Brain

TL;DR: The results imply that persistence of chronic pain is predetermined by corticolimbic neuroanatomical factors.

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Abstract: SEE TRACEY DOI101093/BRAIN/AWW147 FOR A SCIENTIFIC COMMENTARY ON THIS ARTICLE: Mechanisms of chronic pain remain poorly understood. We tracked brain properties in subacute back pain patients longitudinally for 3 years as they either recovered from or transitioned to chronic pain. Whole-brain comparisons indicated corticolimbic, but not pain-related circuitry, white matter connections predisposed patients to chronic pain. Intra-corticolimbic white matter connectivity analysis identified three segregated communities: dorsal medial prefrontal cortex-amygdala-accumbens, ventral medial prefrontal cortex-amygdala, and orbitofrontal cortex-amygdala-hippocampus. Higher incidence of white matter and functional connections within the dorsal medial prefrontal cortex-amygdala-accumbens circuit, as well as smaller amygdala volume, represented independent risk factors, together accounting for 60% of the variance for pain persistence. Opioid gene polymorphisms and negative mood contributed indirectly through corticolimbic anatomical factors, to risk for chronic pain. Our results imply that persistence of chronic pain is predetermined by corticolimbic neuroanatomical factors.

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259 citations

Cites background or methods or result from "Brain white matter structural prope..."

...recent human neuroimaging (Apkarian et al., 2004; Baliki et al., 2006, 2010, 2012; Geha et al., 2008; Hashmi et al., 2013; Mansour et al., 2013; Mutso et al., 2014) and complementary animal model (Neugebauer et al....
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...Portions of the data were used in previous publications (Baliki et al., 2012; Hashmi et al., 2013; Mansour et al., 2013; Petre et al., 2015)....
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...However, only recent human neuroimaging (Apkarian et al., 2004; Baliki et al., 2006, 2010, 2012; Geha et al., 2008; Hashmi et al., 2013; Mansour et al., 2013; Mutso et al., 2014) and complementary animal model (Neugebauer et al., 2003; Metz et al., 2009; Ji and Neugebauer, 2011; Ren et al., 2011;…...
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...Earlier analyses of subsamples of these data (Baliki et al., 2012; Mansour et al., 2013) show that functional and white matter properties of some limbic regions impart risk for chronic pain....
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...This finding is consistent with and generalizes from a previous report that white matter regional fractional anisotropy distinguishes between SBP groups (based on a subsample of the current cohort; Mansour et al., 2013)....
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References

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Fast robust automated brain extraction

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Stephen M. Smith¹•Institutions (1)

John Radcliffe Hospital¹

01 Nov 2002-Human Brain Mapping

TL;DR: An automated method for segmenting magnetic resonance head images into brain and non‐brain has been developed and described and examples of results and the results of extensive quantitative testing against “gold‐standard” hand segmentations, and two other popular automated methods.

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Abstract: An automated method for segmenting magnetic resonance head images into brain and non-brain has been developed. It is very robust and accurate and has been tested on thousands of data sets from a wide variety of scanners and taken with a wide variety of MR sequences. The method, Brain Extraction Tool (BET), uses a deformable model that evolves to fit the brain's surface by the application of a set of locally adaptive model forces. The method is very fast and requires no preregistration or other pre-processing before being applied. We describe the new method and give examples of results and the results of extensive quantitative testing against "gold-standard" hand segmentations, and two other popular automated methods.

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9,887 citations

Journal Article•DOI•

Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data.

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Stephen M. Smith¹, Mark Jenkinson¹, Heidi Johansen-Berg¹, Daniel Rueckert², Thomas E. Nichols³, Clare E. Mackay¹, Kate E. Watkins¹, Olga Ciccarelli⁴, M Z Cader¹, Paul M. Matthews¹, Timothy E.J. Behrens¹ - Show less +7 more•Institutions (4)

University of Oxford¹, Imperial College London², University of Michigan³, University College London⁴

15 Jul 2006-NeuroImage

TL;DR: TBSS aims to improve the sensitivity, objectivity and interpretability of analysis of multi-subject diffusion imaging studies by solving the question of how to align FA images from multiple subjects in a way that allows for valid conclusions to be drawn from the subsequent voxelwise analysis.

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5,959 citations

"Brain white matter structural prope..." refers methods in this paper

...For each of the 46 SBP subjects, we transformed the gray matter and white matter masks into standard space using FSL linear registration tool (FLIRT)....
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...Easythresh (part of the FSL toolbox) was used to cluster the TBSS resultant significance map into clusters that are P50 voxels at P-corrected .05 and P-cluster .05....
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...Analysis was performed using tools from the FMRIB Software Library (FSL) (www.fmrib.ox.ac.uk/fsl) and in-house software....
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...Voxel-wise statistical analysis of FA data was carried out using the tract-based spatial statistics (TBSS) part of FSL [34]....
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Journal Article•DOI•

The basis of anisotropic water diffusion in the nervous system – a technical review

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Christian Beaulieu¹•Institutions (1)

University of Alberta¹

01 Nov 2002-NMR in Biomedicine

TL;DR: The purpose of this review is to characterize the relationship of nuclear magnetic resonance measurements of water diffusion and its anisotropy (i.e. directional dependence) with the underlying microstructure of neural fibres.

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Abstract: Anisotropic water diffusion in neural fibres such as nerve, white matter in spinal cord, or white matter in brain forms the basis for the utilization of diffusion tensor imaging (DTI) to track fibre pathways. The fact that water diffusion is sensitive to the underlying tissue microstructure provides a unique method of assessing the orientation and integrity of these neural fibres, which may be useful in assessing a number of neurological disorders. The purpose of this review is to characterize the relationship of nuclear magnetic resonance measurements of water diffusion and its anisotropy (i.e. directional dependence) with the underlying microstructure of neural fibres. The emphasis of the review will be on model neurological systems both in vitro and in vivo. A systematic discussion of the possible sources of anisotropy and their evaluation will be presented followed by an overview of various studies of restricted diffusion and compartmentation as they relate to anisotropy. Pertinent pathological models, developmental studies and theoretical analyses provide further insight into the basis of anisotropic diffusion and its potential utility in the nervous system.

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4,216 citations

"Brain white matter structural prope..." refers background in this paper

...gree of diffusion anisotropy within a voxel (range 0–1, where larger values indicate directional dependence of Brownian motion due to white matter tracts and smaller values indicate more isotropic diffusion and less coherence) [12]....
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Journal Article•DOI•

Cellular and Molecular Mechanisms of Pain

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Allan I. Basbaum¹, Diana M. Bautista², Grégory Scherrer¹, David Julius¹•Institutions (2)

University of California, San Francisco¹, University of California, Berkeley²

16 Oct 2009-Cell

TL;DR: Genetic, electrophysiological, and pharmacological studies are elucidating the molecular mechanisms that underlie detection, coding, and modulation of noxious stimuli that generate pain.

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3,394 citations

"Brain white matter structural prope..." refers background in this paper

...Extensive human and animal evidence shows that chronic pain is associated with peripheral and central nervous system reorganization, with a large list of neuronal and glial changes associated with pain persistence [11]....
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Journal Article•DOI•

Characterization and propagation of uncertainty in diffusion-weighted MR imaging.

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Timothy E.J. Behrens¹, Mark W. Woolrich¹, Mi Jenkinson¹, Heidi Johansen-Berg¹, Rita G. Nunes¹, Stuart Clare¹, Paul M. Matthews¹, J M Brady¹, Stephen M. Smith¹ - Show less +5 more•Institutions (1)

University of Oxford¹

01 Nov 2003-Magnetic Resonance in Medicine

TL;DR: A fully probabilistic framework is presented for estimating local probability density functions on parameters of interest in a model of diffusion, allowing for the quantification of belief in tractography results and the estimation of the cortical connectivity of the human thalamus.

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Abstract: A fully probabilistic framework is presented for estimating local probability density functions on parameters of interest in a model of diffusion. This technique is applied to the estimation of parameters in the diffusion tensor model, and also to a simple partial volume model of diffusion. In both cases the parameters of interest include parameters defining local fiber direction. A technique is then presented for using these density functions to estimate global connectivity (i.e., the probability of the existence of a connection through the data field, between any two distant points), allowing for the quantification of belief in tractography results. This technique is then applied to the estimation of the cortical connectivity of the human thalamus. The resulting connectivity distributions correspond well with predictions from invasive tracer methods in nonhuman primate.

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2,970 citations

"Brain white matter structural prope..." refers methods in this paper

...We performed probabilistic tractography using FDT software [13] by first running Markov chain Monte Carlo sampling to build up distributions on the diffusion parameters at each voxel in the individual subject’s space....
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