Advertisement
Research Article| Volume 20, ISSUE 8, P898-907, August 2019

Differences in Neuronal Representation of Mental Rotation in Patients With Complex Regional Pain Syndrome and Healthy Controls

Published:January 30, 2019DOI:https://doi.org/10.1016/j.jpain.2019.01.330

      Abstract

      Spatial integration of parts of the body is impaired in patients with complex regional pain syndrome (CRPS). Because the training of mental rotation (MR) has been shown to be among the effective therapy strategies for CRPS, impairment of MR is also important for the pathophysiological understanding of CRPS. The aim of this study was to evaluate whether differences in the neural representation of MR occur between patients with CRPS and healthy controls (HC). Therefore, we included 15 patients with chronic CRPS and 15 age- and gender-matched HC. We assessed behavioral (accuracy and reaction time for MR of both hands), clinical (Disabilities of Arm, Shoulder and Hand questionnaire) and magnetic resonance imaging (T1-weighted, function magnetic resonance imaging during MR) data. Reaction times in the patient group were delayed compared with HC without a lateralization effect for the affected hand side. Although both groups showed an activation pattern typical for MR, only HC showed a highly significant contrast for the rotated versus unrotated hands in the right intraparietal sulcus. Patients with CRPS showed a reduction of functional magnetic resonance imaging activation in areas including the subthalamic nucleus, nucleus accumbens, and putamen. Regression analysis for the CRPS group emphasized the importance of putamen and nucleus accumbens activation for MR performance. This study highlights the reduced access of patients with CRPS for mental resources modulating arousal, emotional response, and subcortical sensorimotor integration.

      Perspective

      This study localized the underlying neural responses for impaired mental rotation in patients with complex regional pain syndrome as a decrease in basal ganglia (putamen) and nucleus accumbens activation.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to The Journal of Pain
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Alivisatos B
        • Petrides M
        Functional activation of the human brain during mental rotation.
        Neuropsychologia. 1997; 35: 111-118
        • Ashburner J
        A fast diffeomorphic image registration algorithm.
        Neuroimage. 2007; 38: 95-113
        • Azqueta-Gavaldon M
        • Schulte-Göcking H
        • Storz C
        • Azad S
        • Reiners A
        • Borsook D
        • Becerra L
        • Kraft E
        Basal ganglia dysfunction in complex regional pain syndrome – A valid hypothesis?.
        Eur J Pain (United Kingdom). 2017; : 415-424
        • Beerthuizen A
        • Stronks DL
        • Van'T Spijker A
        • Yaksh A
        • Hanraets BM
        • Klein J
        • Huygen FJPM
        Demographic and medical parameters in the development of complex regional pain syndrome type 1 (CRPS1): Prospective study on 596 patients with a fracture.
        Pain. 2012; : 1187-1192
        • Berneiser J
        • Jahn G
        • Grothe M
        • Lotze M
        From visual to motor strategies: Training in mental rotation of hands.
        Neuroimage. 2018; 167: 247-255
        • Bhatia KP
        • Marsden CD
        The behavioural and motor consequences of focal lesions of the basal ganglia in man.
        Brain. 1994; 117: 859-876
        • Birklein F
        Complex regional pain syndrome.
        J Neurol. 2005; 252: 131-138
        • Birklein F
        • Riedl B
        • Sieweke N
        • Weber M
        • Neundörfer B
        Neurological findings in complex regional pain syndromes–analysis of 145 cases.
        Acta Neurol Scand. 2000; 101: 262-269
        • Bittar RG
        • Otero S
        • Carter H
        • Aziz TZ
        Deep brain stimulation for phantom limb pain.
        J Clin Neurosci. 2005; 12: 399-404
        • Bittar RG
        • Yianni J
        • Wang SY
        • Liu X
        • Nandi D
        • Joint C
        • Scott R
        • Bain PG
        • Gregory R
        • Stein J
        • Aziz TZ
        Deep brain stimulation for generalised dystonia and spasmodic torticollis.
        J Clin Neurosci. 2005; 12: 12-16
        • Bode S
        • Koeneke S
        • Jäncke L
        Different strategies do not moderate primary motor cortex involvement in mental rotation: A TMS study.
        Behav Brain Funct. 2007; 3: 38
        • de Boer RDH
        • Marinus J
        • van Hilten JJ
        • Huygen FJ
        • van Eijs F
        • van Kleef M
        • Bauer MCR
        • van Gestel M
        • Zuurmond WWA
        • Perez RSGM
        Distribution of signs and symptoms of complex regional pain syndrome type I in patients meeting the diagnostic criteria of the International Association for the Study of Pain.
        Eur J Pain [Internet]. 2011; 15 (Available from:): 830.e1-830.e8
        • Bonda E
        • Petrides M
        • Frey S
        • Evans A
        Neural correlates of mental transformations of the body-in-space.
        Proc Natl Acad Sci U S A [Internet]. 1995; 92 (Available from): 11180-11184
        • Chang PC
        • Pollema-Mays SL
        • Centeno MV
        • Procissi D
        • Contini M
        • Baria AT
        • Martina M
        • Apkarian AV
        Role of nucleus accumbens in neuropathic pain: Linked multi-scale evidence in the rat transitioning to neuropathic pain.
        Pain. 2014; 155: 1128-1139
        • Deary IJ
        • Der G
        • Ford G
        Reaction times and intelligence differences. A population-based cohort study.
        Intelligence. 2001; 29: 389-399
        • Ganis G
        • Keenan JP
        • Kosslyn SM
        • Pascual-Leone A
        Transcranial magnetic stimulation of primary motor cortex affects mental rotation.
        Cereb Cortex. 2000; 10: 175-180
        • Geha PY
        • Baliki MN
        • Harden RN
        • Bauer WR
        • Parrish TB
        • Apkarian AV
        The brain in chronic CRPS pain: Abnormal gray-white matter interactions in emotional and autonomic regions.
        Neuron. 2008; 60: 570-581
        • Gentilucci M
        • Daprati E
        • Gangitano M
        Right-handers and left-handers have different representations of their own hand.
        Cogn Brain Res. 1998; 6: 185-192
        • Gustin SM
        • Schwarz A
        • Birbaumer N
        • Sines N
        • Schmidt AC
        • Veit R
        • Larbig W
        • Flor H
        • Lotze M
        NMDA-receptor antagonist and morphine decrease CRPS-pain and cerebral pain representation.
        Pain. 2010; 151: 69-76
        • Harris IM
        • Miniussi C
        Parietal lobe contribution to mental rotation demonstrated with rTMS.
        J Cogn Neurosci. 2003; 15: 315-323
        • Henderson LA
        • Peck CC
        • Petersen ET
        • Rae CD
        • Youssef AM
        • Reeves JM
        • Wilcox SL
        • Akhter R
        • Murray GM
        • Gustin SM
        Chronic pain: Lost inhibition?.
        J Neurosci. 2013; 33: 7574-7582
        • Juottonen K
        • Gockel M
        • Silén T
        • Hurri H
        • Hari R FN
        Altered central sensorimotor processing in patients with complex regional pain syndrome.
        Pain. 2002; 98: 315-323
        • Karnath HO
        • Baier B
        Right insula for our sense of limb ownership and self-awareness of actions.
        Brain Struct Funct. 2010; 214: 411-417
        • Keuken MC
        • Bazin PL
        • Backhouse K
        • Beekhuizen S
        • Himmer L
        • Kandola A
        • Lafeber JJ
        • Prochazkova L
        • Trutti A
        • Schäfer A
        • Turner R
        • Forstmann BU
        Effects of aging on T1, T2∗, and QSM MRI values in the subcortex.
        Brain Struct Funct. 2017; 222: 2487-2505
        • Kolb L
        • Lang C
        • Seifert F
        • Maihöfner C
        Cognitive correlates of “neglect-like syndrome” in patients with complex regional pain syndrome.
        Pain. 2012; 153: 1063-1073
        • Lebon F
        • Lotze M
        • Stinear CM
        • Byblow WD
        Task-dependent interaction between parietal and contralateral primary motor cortex during explicit versus implicit motor imagery.
        PLoS One. 2012; 7: e37850
        • Lee WJ
        • Choi SH
        • Jang JH
        • Moon JY
        • Kim YC
        • Noh E
        • Shin JE
        • Shin H
        • Kang DH
        Different patterns in mental rotation of facial expressions in complex regional pain syndrome patients.
        Med (United States). 2017; 96: e7990
        • Lewis JS
        • Kersten P
        • McPherson KM
        • Taylor GJ
        • Harris N
        • McCabe CS
        • Blake DR
        Wherever is my arm? Impaired upper limb position accuracy in Complex Regional Pain Syndrome.
        Pain. 2010; 149: 463-469
        • Lotze M
        • Erb M
        • Flor H
        • Huelsmann E
        • Godde B
        • Grodd W
        fMRI evaluation of somatotopic representation in human primary motor cortex.
        Neuroimage. 2000; 11: 473-481
        • Lotze M
        • Moseley GL
        Role of distorted body image in pain.
        Curr Rheumatol Rep. 2007; 9: 488-496
        • Maihöfner C
        • Baron R
        • DeCol R
        • Binder A
        • Birklein F
        • Deuschl G
        • Handwerker HO
        • Schattschneider J
        The motor system shows adaptive changes in complex regional pain syndrome.
        Brain. 2007; 130: 2671-2687
        • Maihöfner C
        • Handwerker HO
        • Neundörfer B
        • Birklein F
        Patterns of cortical reorganization in complex regional pain syndrome.
        Neurology. 2003; 61: 1707-1715
        • Mogenson GJ
        • Jones DL
        • Yim CY
        From motivation to action: Functional interface between the limbic system and the motor system.
        Prog Neurobiol. 1980; 14: 69-97
        • Moseley GL
        Graded motor imagery for pathologic pain: A randomized controlled trial.
        Neurology. 2006; 67: 2129-2134
        • Moseley GL
        • Gallace A
        • Iannetti GD
        Spatially defined modulation of skin temperature and hand ownership of both hands in patients with unilateral complex regional pain syndrome.
        Brain. 2012; 135: 3676-3686
        • Moseley GL
        • Gallace A
        • Spence C
        Space-based, but not arm-based, shift in tactile processing in complex regional pain syndrome and its relationship to cooling of the affected limb.
        Brain. 2009; 132: 3142-3151
        • Obeso JA
        • Marin C
        • Rodriguez-Oroz C
        • Blesa J
        • Benitez-Temiño B
        • Mena-Segovia J
        • Rodríguez M
        • Olanow CW
        The basal ganglia in Parkinson's disease: Current concepts and unexplained observations.
        Ann Neurol. 2008; 64(Suppl 2): S30—S46
        • Offenbächer M
        • Ewert T
        • Sangha O
        • Stucki G
        Validation of a German version of the “Disabilities of Arm, Shoulder and Hand” questionnaire (DASH-G).
        Z Rheumatol. 2003; 62: 168-177
        • Oldfield RC
        The assessment and analysis of handedness: The Edinburgh inventory.
        Neuropsychologia. 1971; 9: 97-113
        • Parsons LM
        Imagined spatial transformations of one's hands and feet.
        Cogn Psychol. 1987; 19: 178-241
        • Parsons LM
        Temporal and kinematic properties of motor behavior reflected in mentally simulated action.
        J Exp Psychol Hum Percept Perform. 1994; 20: 709-730
        • Parsons LM
        • Fox PT
        • Downs JH
        • Glass T
        • Hirsch TB
        • Martin CC
        • Jerabek PA
        • Lancaster JL
        Use of implicit motor imagery for visual shape discrimination as revealed by PET.
        Nature. 1995; 375: 54-58
        • Pleger B
        • Tegenthoff M
        • Schwenkreis P
        • Janssen F
        • Ragert P
        • Dinse HR
        • Völker B
        • Zenz M
        • Maier C
        Mean sustained pain levels are linked to hemispherical side-to-side differences of primary somatosensory cortex in the complex regional pain syndrome I.
        Exp Brain Res. 2004; 155: 115-119
        • Reinersmann A
        • Haarmeyer GS
        • Blankenburg M
        • Frettlöh J
        • Krumova EK
        • Ocklenburg S
        • Maier C
        Left is where the L is right. Significantly delayed reaction time in limb laterality recognition in both CRPS and phantom limb pain patients.
        Neurosci Lett. 2010; 486: 240-245
        • Reinersmann A
        • Maier C
        • Schwenkreis P
        • Lenz M
        Complex regional pain syndrome: More than a peripheral disease.
        Pain Manag. 2013; 3: 495-502
        • Schwenkreis P
        • Janssen F
        • Rommel O
        • Pleger B
        • Völker B
        • Hosbach I
        • Dertwinkel R
        • Maier C
        • Tegenthoff M
        Bilateral motor cortex disinhibition in complex regional pain syndrome (CRPS) type I of the hand.
        Neurology. 2003; 61: 515-519
        • Schwoebel J
        • Coslett HB
        Evidence for multiple, distinct representations of the human body.
        J Cogn Neurosci. 2005; 17: 543-553
        • Simons LE
        • Elman I
        • Borsook D
        Psychological processing in chronic pain: A neural systems approach.
        Neurosci Biobehav Rev. 2014; 39: 61-78
        • Simons LE
        • Goubert L
        • Vervoort T
        • Borsook D
        Circles of engagement: Childhood pain and parent brain.
        Neurosci Biobehav Rev. 2016; 68: 537-546
        • Strauss S
        • Grothe M
        • Usichenko T
        • Neumann N
        • Byblow WD
        • Lotze M
        Inhibition of the primary sensorimotor cortex by topical anesthesia of the forearm in patients with complex regional pain syndrome.
        Pain. 2015; 156: 2556-2561
        • Tzourio-Mazoyer N
        • Landeau B
        • Papathanassiou D
        • Crivello F
        • Etard O
        • Delcroix N
        • Mazoyer B
        • Joliot M
        Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.
        Neuroimage. 2002; 15: 273-289
        • Vania Apkarian A
        • Baliki MN
        • Farmer MA
        Predicting transition to chronic pain.
        Curr Opin Neurol. 2013; 26: 360-367
        • Veldman PHJM
        • Reynen HM
        • Arntz IE
        • Goris RJA
        Signs and symptoms of reflex sympathetic dystrophy: Prospective study of 829 patients.
        Lancet. 1993; 342: 1012-1016
        • Vogel JJ
        • Bowers CA
        • Vogel DS
        Cerebral lateralization of spatial abilities: A meta-analysis cerebral lateralization of spatial abilities: A meta-analysis.
        Brain Cogn. 2003; 52: 197-204
        • Walz A
        • Usichenko T
        • Moseley G
        • Lotze M
        Graded motor imagery and the impact on pain processing in a case of CRPS.
        Clin J Pain. 2013; 29: 276-279
        • Wittayer M
        • Dimova V
        • Birklein F
        • Schlereth T
        Correlates and importance of neglect-like symptoms in complex regional pain syndrome.
        Pain. 2018; 159: 978-986