Cerebral Perfusion Effects of Cognitive Training and Transcranial Direct Current Stimulation in Mild-Moderate TBI

Davin K Quinn, Joel Upston, Thomas Jones, Emma Brandt, Jacqueline Story-Remer, Violet Fratzke, J Kevin Wilson, Rebecca Rieger, Michael A Hunter, Darbi Gill, Jessica D Richardson, Richard Campbell, Vincent P Clark, Ronald A Yeo, Claude William Shuttleworth, Andrew R Mayer, Davin K Quinn, Joel Upston, Thomas Jones, Emma Brandt, Jacqueline Story-Remer, Violet Fratzke, J Kevin Wilson, Rebecca Rieger, Michael A Hunter, Darbi Gill, Jessica D Richardson, Richard Campbell, Vincent P Clark, Ronald A Yeo, Claude William Shuttleworth, Andrew R Mayer

Abstract

Background: Persistent post-traumatic symptoms (PPS) after traumatic brain injury (TBI) can lead to significant chronic functional impairment. Pseudocontinuous arterial spin labeling (pCASL) has been used in multiple studies to explore changes in cerebral blood flow (CBF) that may result in acute and chronic TBI, and is a promising neuroimaging modality for assessing response to therapies. Methods: Twenty-four subjects with chronic mild-moderate TBI (mmTBI) were enrolled in a pilot study of 10 days of computerized executive function training combined with active or sham anodal transcranial direct current stimulation (tDCS) for treatment of cognitive PPS. Behavioral surveys, neuropsychological testing, and magnetic resonance imaging (MRI) with pCASL sequences to assess global and regional CBF were obtained before and after the training protocol. Results: Robust improvements in depression, anxiety, complex attention, and executive function were seen in both active and sham groups between the baseline and post-treatment visits. Global CBF decreased over time, with differences in regional CBF noted in the right inferior frontal gyrus (IFG). Active stimulation was associated with static or increased CBF in the right IFG, whereas sham was associated with reduced CBF. Neuropsychological performance and behavioral symptoms were not associated with changes in CBF. Discussion: The current study suggests a complex picture between mmTBI, cerebral perfusion, and recovery. Changes in CBF may result from physiologic effect of the intervention, compensatory neural mechanisms, or confounding factors. Limitations include a small sample size and heterogenous injury sample, but these findings suggest promising directions for future studies of cognitive training paradigms in mmTBI.

Keywords: cerebral perfusion; cognitive training; pCASL; transcranial direct current stimulation; traumatic brain injury.

Copyright © 2020 Quinn, Upston, Jones, Brandt, Story-Remer, Fratzke, Wilson, Rieger, Hunter, Gill, Richardson, Campbell, Clark, Yeo, Shuttleworth and Mayer.

Figures

Figure 1
Figure 1
Behavioral and cognitive performance for all subjects from baseline to post-treatment to 1 month followup visit. (A) Depression symptoms (HAM-D). (B) Attention performance (WAIS-CD-S). (C,D) Executive function performance (EXAMINER Executive composite and working memory composite scores). Red, active; blue, sham; gray regions, standard error.
Figure 2
Figure 2
(A) Changes in global cerebral perfusion (CP) between baseline and post-treatment visits. (a) Mild TBI participants (circles). (b) Moderate TBI participants (triangles). Difference in CP between mild and moderate TBI participants was not significant. Red, active group; blue, sham group. (B) Scatter plot of Hopkins Verbal Learning Test (HVLT) retention score with cerebral perfusion (CP) for active (red) and sham (blue) groups. HVLT correlated mildly (r = −0.44) with reductions in CP.
Figure 3
Figure 3
Cerebral perfusion (CP) in inferior frontal gyrus/pars triangularis (IFG) from baseline to post-treatment visit. (A) In left IFG, active group (red) demonstrated no change in CP, while sham (blue) decreased. In right IFG, CP increased in active group but decreased in sham group. (B) 3-D visualization of change in CP over time in active and sham groups. Blue, decreased CP; red, increased.

References

    1. Mayer AR, Quinn DK, Master CL. The spectrum of mild traumatic brain injury. Neurology. (2017) 89:623–32. 10.1212/WNL.0000000000004214
    1. McMahon PJ, Hricik A, Yue JK, Puccio AM, Inoue T, Lingsma HF, et al. . Symptomatology and functional outcome in mild traumatic brain injury: results from the prospective TRACK-TBI study. J Neurotrauma. (2014) 31:26–33. 10.1089/neu.2013.2984
    1. King PR, Donnelly KT, Donnelly JP, Dunnam M, Warner G, Kittleson CJ, et al. . Psychometric study of the neurobehavioral symptom inventory. J Rehabil Res Dev. (2012) 49:879. 10.1682/JRRD.2011.03.0051
    1. Linden SC, Jones E. “Shell shock” revisited: An examination of the case records of the national hospital in London. Med Hist. (2014) 58:519–45. 10.1017/mdh.2014.51
    1. Stevens A, Friedel E, Mehren G, Merten T. Malingering and uncooperativeness in psychiatric and psychological assessment: prevalence and effects in a German sample of claimants. Psychiatry Res. (2008) 157:191–200. 10.1016/j.psychres.2007.01.003
    1. Vanderploeg RD, Belanger HG, Curtiss G. Mild traumatic brain injury and posttraumatic stress disorder and their associations with health symptoms. Arch Phys Med Rehabil. (2009) 90:1084–93. 10.1016/j.apmr.2009.01.023
    1. Mayer AR, Bellgowan PSF, Hanlon FM. Functional magnetic resonance imaging of mild traumatic brain injury. Neurosci Biobehav Rev. (2015) 49:8–18. 10.1016/j.neubiorev.2014.11.016
    1. Mayer AR, Ling JM, Dodd AB, Gasparovic C, Klimaj SD, Meier TB. A longitudinal assessment of structural and chemical alterations in mixed martial arts fighters. J Neurotrauma. (2015) 32:1759–67. 10.1089/neu.2014.3833
    1. Mayer AR, Mannell MV, Ling J, Gasparovic C, Yeo RA. Functional connectivity in mild traumatic brain injury. Hum Brain Mapp. (2011) 32:1825–35. 10.1002/hbm.21151
    1. Quinn DK, Mayer AR, Master CL, Fann JR. Prolonged postconcussive symptoms. Am J Psychiatry. (2018) 175:103–111. 10.1176/appi.ajp.2017.17020235
    1. Yuh EL, Mukherjee P, Lingsma HF, Yue JK, Ferguson AR, Gordon WA, et al. . Magnetic resonance imaging improves 3-month outcome prediction in mild traumatic brain injury. Ann Neurol. (2013) 73:224–35. 10.1002/ana.23783
    1. Rathbone ATL, Tharmaradinam S, Jiang S, Rathbone MP, Kumbhare DA. A review of the neuro- and systemic inflammatory responses in post concussion symptoms: introduction of the “post-inflammatory brain syndrome” PIBS. Brain Behav Immun. (2015) 46:1–16. 10.1016/j.bbi.2015.02.009
    1. Toth P, Szarka N, Farkas E, Ezer E, Czeiter E, Amrein K, et al. . Traumatic brain injury-induced autoregulatory dysfunction and spreading depression-related neurovascular uncoupling : pathomechanisms, perspectives, and therapeutic implications. Am J Physiol Hear Circ Physiol. (2016) 311:H1118–31. 10.1152/ajpheart.00267.2016
    1. Iadecola C. The neurovascular unit coming of age : a journey through neurovascular coupling in health and disease. Neuron. (2017) 96:17–42. 10.1016/j.neuron.2017.07.030
    1. Phillips AA, Chan FHN, Mu M, Zheng Z, Krassioukov AV, Ainslie PN. Neurovascular coupling in humans: physiology, methodological advances and clinical implications. J Cereb Blood Flow Metab. (2016) 36:647–64. 10.1177/0271678X15617954
    1. Douglas DB, Chaudhari R, Zhao JM, Gullo J, Kirkland J, Douglas PK, et al. . Perfusion imaging in acute traumatic brain injury. Neuroimaging Clin NA. (2020) 28:55–65. 10.1016/j.nic.2017.09.002
    1. Jang H, Hammer DX, Welle CG, Fisher JAN, Jang H, Huang S, et al. . Alterations in neurovascular coupling following acute traumatic brain injury. Neurophotonics. (2017) 4:1–15. 10.1117/1.NPh.4.4.045007
    1. Kenney K, Amyot F, Haber M, Pronger A, Bogoslovsky T, Moore C, et al. . Cerebral vascular injury in traumatic brain injury. Exp Neurol. (2016) 275:353–66. 10.1016/j.expneurol.2015.05.019
    1. Sankar SB, Pybus AF, Liew A, Sanders B, Shah KJ, Wood LB, et al. . Low cerebral blood flow is a non-invasive biomarker of neuroinflammation after repetitive mild traumatic brain injury. Neurobiol Dis. (2019) 124:544–54. 10.1016/j.nbd.2018.12.018
    1. Sharma A, Hind K, Hume P, Singh J, Neary JP. Neurovascular coupling by functional near infra-red spectroscopy and sport-related concussion in retired rugby players : the Uk rugby health project. Front Hum Neurosci. (2020) 14:1–9. 10.3389/fnhum.2020.00042
    1. Haller S, Zaharchuk G, Thomas DL, Lovblad K-O, Barkhof F, Golay X. Arterial spin labeling perfusion of the brain : emerging clinical applications. Radiology. (2016) 281:337–56. 10.1148/radiol.2016150789
    1. Andre JB. Arterial spin labeling magnetic resonance perfusion for traumatic brain injury : technical challenges and potentials. Top Magn Reson Imaging. (2015) 24:275–87. 10.1097/RMR.0000000000000065
    1. Wang Y, Nelson LD, Laroche AA, Pfaller AY, Nencka AS, Koch KM, et al. . Cerebral blood flow alterations in acute sport-related concussion. J Neurotrauma. (2016) 33:1227–36. 10.1089/neu.2015.4072
    1. Wang Y, West JD, Bailey JN, Westfall DR, Xiao H, Arnold W, et al. . Decreased cerebral blood flow in chronic pediatric mild TBI : an MRI perfusion study. Dev Neuropsychol. (2015) 40:40–4. 10.1080/87565641.2014.979927
    1. Clark AL, Bangen KJ, Sorg SF, Schiehser DM, Evangelista ND, Mckenna B, et al. . Clinical dynamic association between perfusion and white matter integrity across time since injury in veterans with history of TBI. Neuroimage. (2017) 14:308–15. 10.1016/j.nicl.2016.12.017
    1. Kim J, Whyte J, Avants B, Europa E, Wang J, Slattery J, et al. . Resting cerebral blood flow alterations in chronic traumatic brain injury : an arterial spin labeling perfusion fMRI study. J Neurotrauma. (2010) 27:1399–411. 10.1089/neu.2009.1215
    1. Kim J, Whyte J, Patel S, Europa E, Slattery J, Coslett HB, et al. . A perfusion fMRI study of the neural correlates of sustained-attention and working-memory deficits in chronic traumatic brain injury. Neurorehabil Neural Repair. (2012) 26:870–80. 10.1177/1545968311434553
    1. Hamer J, Churchill NW, Hutchison MG, Graham SJ. Sex differences in cerebral blood flow associated with a history of concussion. J Neurotrauma. (2020) 7:1–7. 10.1089/neu.2019.6800
    1. Brooks BL, Low TA, Plourde V, Virani S, Jadavji Z, Macmaster FP, et al. . Cerebral blood flow in children and adolescents several years after concussion. Brian Inj. (2019) 33:233–41. 10.1080/02699052.2018.1540798
    1. Barlow KM, Marcil LD, Dewey D, Carlson HL, Macmaster FP, Brooks BL, et al. . Cerebral perfusion changes in post-concussion syndrome : a prospective controlled cohort study. J Neurotrauma. (2017) 34:996–1004. 10.1089/neu.2016.4634
    1. Ge Y, Patel MB, Chen Q, Grossman EJ, Zhang K, Babb JS, et al. . Assessment of thalamic perfusion in patients with mild traumatic brain injury by true FISP arterial spin labelling MR imaging at 3T. Brain Inj. (2009) 23:666–74. 10.1080/02699050903014899
    1. Lin C, Tseng Y, Hsu H, Chen C, Yen- D. Arterial spin labeling perfusion study in the patients with subacute mild traumatic brain injury. PLoS ONE. (2016) 11:1–11. 10.1371/journal.pone.0149109
    1. Doshi H, Wiseman N, Liu J, Wang W, Welch RD, Neil JO, et al. . Cerebral hemodynamic changes of mild traumatic brain injury at the acute stage. PLoS ONE. (2015) 10:1–18. 10.1371/journal.pone.0118061
    1. Stephens JA, Liu P, Lu H, Suskauer SJ. Cerebral blood flow after mild traumatic brain injury: associations between symptoms and post-injury perfusion. J Neurotrauma. (2017) 35:241–8. 10.1089/neu.2017.5237
    1. Dhaliwal SK, Meek BP, Modirrousta MM. Non-invasive brain stimulation for the treatment of symptoms following traumatic brain injury. Front Psychiatry. (2015) 6:1–13. 10.3389/fpsyt.2015.00119
    1. Zheng X, Alsop DC, Schlaug G. Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. Neuroimage. (2011) 58:26–33. 10.1016/j.neuroimage.2011.06.018
    1. Stagg CJ, Lin RL, Mezue M, Segerdahl A, Kong Y, Xie J, et al. . Widespread modulation of cerebral perfusion induced during and after transcranial direct current stimulation applied to the left dorsolateral prefrontal cortex. J Neurosci. (2013) 33:11425–31. 10.1523/JNEUROSCI.3887-12.2013
    1. Mielke D, Wrede A, Schulz-schaeffer W, Taghizadeh- A, Nitsche MA, Rohde V, et al. . Cathodal transcranial direct current stimulation induces regional, long-lasting reductions of cortical blood flow in rats. Neurol Res. (2013) 35:1029–37. 10.1179/1743132813Y.0000000248
    1. Bragina OA, Lara DA, Nemoto EM, Shuttleworth CW, Bragin DE. Increases in microvascular perfusion and tissue oxygenation via vasodilatation after anodal transcranial direct current stimulation in the healthy and traumatized mouse brain. Adv Exp Med Biol. (2019) 1072:27–31. 10.1007/978-3-319-91287-5_5
    1. Antal A, Fischer T, Saiote C, Miller R, Chaieb L, Wang DJJ, et al. . Transcranial electrical stimulation modifies the neuronal response to psychosocial stress exposure. Hum Brain Mapp. (2014) 35:3750–9. 10.1002/hbm.22434
    1. Li S, Zaninotto AL, Neville IS, Paiva WS, Nunn D, Fregni F. Clinical utility of brain stimulation modalities following traumatic brain injury: current evidence. Neuropsychiatr Dis Treat. (2015) 11:1573–86. 10.2147/NDT.S65816
    1. Sacco K, Galetto V, Dimitri D, Geda E, Perotti F, Zettin M, et al. . Concomitant use of transcranial direct current stimulation and computer-assisted training for the rehabilitation of attention in traumatic brain injured patients : behavioral and neuroimaging results. Front Behav Neurosci. (2016) 10:1–11. 10.3389/fnbeh.2016.00057
    1. Ulam F, Shelton C, Richards L, Davis L, Hunter B, Fregni F, et al. . Cumulative effects of transcranial direct current stimulation on EEG oscillations and attention/working memory during subacute neurorehabilitation of traumatic brain injury. Clin Neurophysiol. (2015) 126:486–96. 10.1016/j.clinph.2014.05.015
    1. O'Neil-Pirozzi TM, Doruk D, Thomson JM, Fregni F. Immediate memory and electrophysiologic effects of prefrontal cortex transcranial direct current stimulation on neurotypical individuals and individuals with chronic traumatic brain injury: a pilot study. Int J Neurosci. (2017) 127:592–600. 10.1080/00207454.2016.1216415
    1. Trofimov AO, Kalentiev G, Karelsky M, Ksenofontova C, Ruzavina A, Yuriev M, et al. . Cerebral hemodynamics after transcranial direct current stimulation (tDCS) in patients with consequences of traumatic brain injury. Adv Exp Med Biol. (2018) 1072:59–62. 10.1007/978-3-319-91287-5_10
    1. Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry. (1960) 23:56–62. 10.1136/jnnp.23.1.56
    1. Beck AT, Steer RA, Brown GK. Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation; (1996).
    1. Weathers FW, Litz BT, Keane TM, Palmieri PA, Marx BP, Schnurr PP. Posttraumatic Stress Disorder Checklist-Civilian Version (PCL-C). National Center for PTSD; (2013). Available online at: (accessed March 24, 2020).
    1. Han K, Martinez D, Chapman SB, Krawczyk DC. Neural correlates of reduced depressive symptoms following cognitive training for chronic traumatic brain injury. Hum Brain Mapp. (2018) 39:2955–71. 10.1002/hbm.24052
    1. Wright J. Glasgow outcome scale-extended (GOS-E). In: Kreutzer JS, Deluca J, Caplan B. editors. Encyclopedia of Clinical Neuropsychology. New York, NY: Springer Science and Business Media; (2011).
    1. Grace J. Frontal systems behavior scale (FrSBe). In: Kreutzer JS, Deluca J, Caplan B. editors. Encyclopedia of Clinical Neuropsychology. New York, NY: Springer; (2011).
    1. Wechsler D. Wechsler Adult Intelligence Scale-Fourth Edition (WAIS-IV). San Antonio, TX: Pearson Assessment; (2008).
    1. Pearson Advanced Clinical Solutions for WAIS-IV and WMS-IV: Clinical and interpretive manual. San Antonio, TX: Pearson; (2009).
    1. Belkonen S. Hopkins verbal learning test-revised (HVLT-R). In: Kreutzer JS, Deluca J, Caplan B. editors. Encyclopedia of Clinical Neuropsychology. New York, NY: Springer; (2011).
    1. Tombaugh TN. Test of memory malingering. Psychol Assess. (1997) 9:260–8. 10.1037/1040-3590.9.3.260
    1. Kramer JH, Mungas D, Possin KL, Rankin KP, Boxer AL, Rosen HJ, et al. . NIH EXAMINER: conceptualization and development of an executive function battery. J Int Neuropsychol Soc. (2014) 20:11–9. 10.1017/S1355617713001094
    1. Seibt O, Brunoni AR, Huang Y, Bikson M. The pursuit of DLPFC: non-neuronavigated methods to target the left dorsolateral pre-frontal cortex with symmetric bicephalic transcranial direct current stimulation (tDCS). Brain Stimul. (2015) 8:590–602. 10.1016/j.brs.2015.01.401
    1. Clark VP, Coffman BA, Trumbo MC, Gasparovic C. Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochemistry: a 1H magnetic resonance spectroscopy study. Neurosci Lett. (2011) 500:67–71. 10.1016/j.neulet.2011.05.244
    1. Clark VP, Coffman BA, Mayer AR, Weisend MP, Lane TDR, Calhoun VD, et al. . TDCS guided using fMRI significantly accelerates learning to identify concealed objects. Neuroimage. (2012) 59:117–28. 10.1016/j.neuroimage.2010.11.036
    1. Bikson M, Grossman P, Thomas C, Zannou AL, Jiang J, Adnan T, et al. . Safety of transcranial direct current stimulation: evidence based update 2016. Brain Stimul. (2016) 9:641–61. 10.1016/j.brs.2016.06.004
    1. Braver TS. The variable nature of cognitive control: a dual-mechanisms framework. Trends Cogn Sci. (2012) 16:106–13. 10.1016/j.tics.2011.12.010
    1. Jaeggi SM, Seewer R, Nirkko AC, Eckstein D, Schroth G, Groner R, et al. . Does excessive memory load attenuate activation in the prefrontal cortex? Load-dependent processing in single and dual tasks : functional magnetic resonance imaging study. Neuroimage. (2003) 19:210–25. 10.1016/S1053-8119(03)00098-3
    1. Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol. (2000) 41:49–100. 10.1006/cogp.1999.0734
    1. Diamond A. Executive functions. Annu Rev Psychol. (2013) 64:135–68. 10.1146/annurev-psych-113011-143750
    1. Larson MJ, Farrer TJ, Clayson PE. Cognitive control in mild traumatic brain injury: conflict monitoring and conflict adaptation. Int J Psychophysiol. (2011) 82:69–78. 10.1016/j.ijpsycho.2011.02.018
    1. Larson MJ, Perlstein WM, Demery JA, Stigge-Kaufman DA. Cognitive control impairments in traumatic brain injury. J Clin Exp Neuropsychol. (2006) 28:968–86. 10.1080/13803390600646860
    1. Cox R. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res. (1996) 29:162–73. 10.1006/cbmr.1996.0014
    1. Wang Z, Wang J, Connick TJ, Wetmore GS, Detre JA. Continuous ASL (CASL) perfusion MRI with an array coil and parallel imaging at 3T. Magn Reson Med. (2005) 54:732–7. 10.1002/mrm.20574
    1. Talairach J, Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain 3-Dimensional Proportional System: An Approach to Cerebral Imaging. Stuttgart, New York, NY: Thompson; (1988).
    1. Coffman BA, Trumbo MC, Clark VP. Enhancement of object detection with transcranial direct current stimulation is associated with increased attention. BMC Neurosci. (2012) 13:108. 10.1186/1471-2202-13-108
    1. Tzsourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. (2002) 15:273–89. 10.1006/nimg.2001.0978
    1. R Core Team R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; (2019). Available online at:
    1. Mendez MF, Owens EM, Reza G, Peppers DC, Angeles VAGL, Angeles L, et al. . Mild traumatic brain injury from primary blast vs. blunt forces : Post-concussion consequences and functional neuroimaging. NeuroRehabilitation. (2013) 32:397–407. 10.3233/NRE-130861
    1. Mayer AR, Stephenson DD, Wertz CJ, Dodd AB, Shaff NA, Ling JM, et al. . Proactive inhibition deficits with normal perfusion after pediatric mild traumatic brain injury. Hum Brain Mapp. (2019) 40:5370–81. 10.1002/hbm.24778
    1. Lipszyc J, Levin H, Hanten G, Hunter J, Dennis M, Schachar R. Frontal white matter damage impairs response inhibition in children following traumatic brain injury. Arch Clin Neuropsychol. (2014) 29:289–99. 10.1093/arclin/acu004
    1. Cunillera T, Brignani D, Cucurell D, Fuentemilla L, Miniussi C. The right inferior frontal cortex in response inhibition: a tDCS–ERP co-registration study. Neuroimage. (2016) 140:66–75. 10.1016/j.neuroimage.2015.11.044
    1. Kito S, Hasegawa T, Koga Y. Neuroanatomical correlates of therapeutic efficacy of low-frequency right prefrontal transcranial magnetic stimulation in treatment-resistant depression. Psychiatry Clin Neurosci. (2011) 65:175–82. 10.1111/j.1440-1819.2010.02183.x
    1. Giglia G, Brighina F, Rizzo S, Puma A, Indovina S, Maccora S, et al. . Anodal transcranial direct current stimulation of the right dorsolateral prefrontal cortex enhances memory-guided responses in a visuospatial working memory task. Funct Neurol. (2014) 29:189–93.
    1. Min SK, Lee BO. Laterality in Somatization. Psychosom Med. (1997) 59:236–40. 10.1097/00006842-199705000-00005
    1. Clark L, Manes F, Antoun N, Sahakian BJ, Robbins TW. The contributions of lesion laterality and lesion volume to decision-making impairment following frontal lobe damage. Neuropsychologia. (2003) 41:1474–83. 10.1016/S0028-3932(03)00081-2
    1. Richard NM, O'Connor C, Dey A, Robertson IH, Levine B. External modulation of the sustained attention network in traumatic brain injury. Neuropsychology. (2018) 32:541–53. 10.1037/neu0000442
    1. Dmochowski JP, Datta A, Huang Y, Richardson JD, Bikson M, Fridriksson J, et al. . Targeted transcranial direct current stimulation for rehabilitation after stroke. Neuroimage. (2013) 75:12–9. 10.1016/j.neuroimage.2013.02.049
    1. Doron KW, Bassett DS, Gazzaniga MS. Dynamic network structure of interhemispheric coordination. PNAS. (2012) 109:18661–8. 10.1073/pnas.1216402109
    1. Sours C, Rosenberg J, Kane R. Associations between interhemispheric functional connectivity and the automated neuropsychological assessment metrics (ANAM) in civilian mild TBI. Brain Imaging Behav. (2015) 9:190–203. 10.1007/s11682-014-9295-y
    1. Almeida JRC, Greenberg T, Lu H, Chase HW, Fournier JC, Cooper CM, et al. . Test-retest reliability of cerebral blood fl ow in healthy individuals using arterial spin labeling : findings from the EMBARC study. Magn Reson Imaging. (2018) 45:26–33. 10.1016/j.mri.2017.09.004
    1. Kito S, Fujita K, Koga Y. Regional cerebral blood flow changes after low-frequency transcranial magnetic stimulation of the right dorsolateral prefrontal cortex in treatment-resistant depression. Neuropsychobiology. (2008) 58:29–36. 10.1159/000154477
    1. Teneback CC, Speer AM, Stallings LE, Pharm D, Spicer KM, Ph D, et al. . Changes in prefrontal cortex and paralimbic activity in depression following two weeks of daily left prefrontal TMS. J Neuropsychiatry Clin Neurosci. (1999) 11:426–35.
    1. Newsome M, Scheibel R, Chu Z, Hunter J, Li X, Wilde E, et al. . The relationship of resting cerebral blood flow and brain activation during a social cognition task in adolescents with chronic moderate to severe traumatic brain injury: a preliminary investigation. Int J Dev Neurosci. (2012) 30:255–66. 10.1016/j.ijdevneu.2011.10.008
    1. Churchill NW, Hutchison MG, Graham SJ, Schweizer TA. Evaluating cerebrovascular reactivity during the early symptomatic phase of sport concussion. J Neurotrauma. (2019) 36:1518–25. 10.1089/neu.2018.6024
    1. Byrnes KR, Wilson CM, Brabazon F, Von Leden R, Jurgens JS, Oakes TR, et al. . FDG-PET imaging in mild traumatic brain injury: a critical review. Front Neuroenerget. (2014) 5:1–24. 10.3389/fnene.2013.00013

Source: PubMed

3
S'abonner