Cognitive and spectral coherence of EEG alterations in resting state in children with chronic TBI

Marlene Galicia-Alvarado, Javier Alducin-Castillo, Maura Jazmín Ramírez-Flores, Ana Laura Sánchez Quezada, Oscar Yáñez-Suárez, Blanca Flores-Ávalos

DOI: https://doi.org/10.17711/SM.0185-3325.2019.012

Abstract


Introduction. TBI is associated with alterations in cortico-subcortical connectivity. However, little attention has been paid to its clinical characteristics and functional connectivity in pediatric patients with chronic TBI.

Objective. To evaluate the cognitive performance and spectral coherence of a group of children with TBI in non-acute phase.

Method. Cross-sectional study of 15 children with chronic TBI and 17 healthy children. The Neuropsychological Assessment of Children (Evaluación Neuropsicológica Infantil, ENI) was used and the resting activity of the EEG with eyes-closed was recorded. Offline, two-second epochs of the EEG of each participant were chosen and the spectral coherence was estimated in a range of 1.6 to 30 Hz. The cognitive performance between groups was compared with T-test/Mann-Whitney U Test and MANOVA for the coherence values.

Results. The TBI group showed a lower performance (p ≤ 0.05) in metalinguistic, visuospatial skills, attention, memory, non-verbal flexibility, planning, and organization. Differences (p ≤ 0.000) were found both inter and intrahemispherically in the spectral coherence between the groups, particularly on F1-F3 (95% CI: 0.543 - 0.557) over the whole frequency range and F3-C3 (95% CI: 0.503 - 0.515) in delta, theta, alpha2, and beta frequencies.

Discussion and conclusión. Our findings suggest alterations of hypo and hyper functional connectivity, particularly on the frontal and parietal lobes of both hemispheres, even after several years of a TBI. It is possible that a subtle difference in the degree of connectivity is crucial in the genesis or successful development of attentional, mnesic, executive, and visuospatial processes.

Keywords


EEG; cognition; child; traumatic brain injury

Full Text:

HTML Pdf ePub

References


Adamson, C., Yuan, W., Babcock, L., Leach, J. L., Seal, M. L., Holland, S. K., & Wade, S. L. (2013). Diffusion tensor imaging detects white matter abnormalities and associated cognitive deficits in chronic adolescent TBI. Brain Injury, 27(4), 454-463. doi: 10.3109/02699052.2012.750756

Adelson, P. D., Bratton, S. L., Carney, N. A., Chesnut, R. M., Du Coudray, H. E., Goldstein, B., ... & Wright, D. W. (2003). Guidelines for the acute medical management of severe traumatic brain injury in infants, children, and adolescents. Chapter I: Introduction. Pediatric Critical Care Medicine: a journal of the Society of Critical Care Medicine and the World Federation of Pediatric Intensive and Critical Care Societies, 4(3 Suppl), S2-4. doi: 10.1097/01.CCM.0000066600.71233.01

Alducín-Castillo, J., Yañez-Suárez, O., & Brust-Carmona, H. (2016). Análisis electroencefalográfico de la conectividad funcional en habituación por teoría de gráficas. Revista Mexicana de Ingeniería Biomédica, 37(3), 181-200. doi: 10.17488/rmib.37.3.3

Alhaddad, M. J. (2012). Common Average Reference (CAR) improves p300 speller. International Journal of Engineering and Technology, 2(3), 21. Recuperado de: https://www.researchgate.net/publication/265881476_Common_Average_Reference_CAR_Improves_P300_Speller

AMAI (2013) Cuestionario regla AMAI NSE 8x7. Recuperado de: http://www.amai.org/NSE/CUESTIONARIO REGLA AMAI NSE 8X7_20110907.pdf

Anderson, P. (2002). Assessment and development of executive function (EF) during childhood. Child Neuropsychology, 8(2), 71-82. doi: 10.1076/chin.8.2.71.8724

Anderson, V. & Catroppa, C. (2005). Recovery of executive skills following pediatric traumatic brain injury (TBI): A 2 year follow-up. Brain Injury, 19(6), 459-470. doi: 10.1080/02699050400004823

Anderson, V., Catroppa, C., Morse, S., Haritou, F., & Rosenfeld, J. (2000). Recovery of intellectual ability following traumatic brain injury in childhood: Impact of injury severity and age at injury. Pediatric Neurosurgery, 32(6), 282-290. doi: 10.1159/000028956

Anderson, V., Catroppa, C., Morse, S., Haritou, F., & Rosenfeld, J. (2005a). Attentional and processing skills following traumatic brain injury in early childhood. Brain Injury, 19(9), 699-710. doi: 10.1080/02699050400025281

Anderson, V., Catroppa, C., Morse, S., Haritou, F., & Rosenfeld, J. (2005b). Functional plasticity or vulnerability after early brain injury? Pediatrics, 116(6), 1374-1382. doi: 10.1542/peds.2004-1728

Aoki, Y., Inokuchi, R., Gunshin, M., Yahagi, N., & Suwa, H. (2012). Diffusion tensor imaging studies of mild traumatic brain injury: A meta-analysis. Journal of Neurology, Neurosurgery, & Psychiatry, 83(9), 870-876. doi: 10.1136/jnnp.2012-302742

Banich M. T. (1997). Spatial Processing. In: M. T. Banich (Ed), Neuropsychology: The Neural Bases of Mental function (pp. 202-233). Boston MA: Houghton Mifflin Company.

Barry, R. J., Clarke, A. R., McCarthy, R., Selikowitz, M., Johnstone, S. J., & Rushby, J. A. (2004). Age and gender effects in EEG coherence: I. Developmental trends in normal children. Clinical Neurophysiology, 115(10), 2252-2258. doi: 10.1016/j.clinph.2004.05.004

Bathelt, J., O’reilly, H., Clayden, J. D., Cross, J. H., & de Haan, M. (2013). Functional brain network organization of children between 2 and 5 years derived from reconstructed activity of cortical sources of high-density EEG recordings. NeuroImage, 82, 595-604. doi: 10.1016/j.neuroimage.2013.06.003

Bell, M. A. & Cuevas, K. (2012). Using EEG to study cognitive development: Issues and practices. Journal of Cognition and Development, 13(3), 281-294. doi: 10.1080/15248372.2012.691143

Blennow, K., Hardy, J., & Zetterberg, H. (2012). The neuropathology and neurobiology of traumatic brain injury. Neuron, 76(5), 886-899. doi: 10.1016/j.neuron.2012.11.021

Bonnelle, V., Leech, R., Kinnunen, K. M., Ham, T. E., Beckmann, C. F., De Boissezon, X., ... & Sharp, D. J. (2011). Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. Journal of Neuroscience, 31(38), 13442-13451. doi: 10.1523/JNEUROSCI.1163-11.2011

Buldú, J. M., Bajo, R., Maestú, F., Castellanos, N., Leyva, I., Gil, P., ... & Boccaletti, S. (2011). Reorganization of functional networks in mild cognitive impairment. PloS One, 6(5), e19584. doi: 10.1371/journal.pone.0019584

Caeyenberghs, K., Leemans, A., Heitger, M. H., Leunissen, I., Dhollander, T., Sunaert, S., ... & Swinnen, S. P. (2012). Graph analysis of functional brain networks for cognitive control of action in traumatic brain injury. Brain, 135(4), 1293-1307. doi: 10.1093/brain/aws048

Carlson, A. G., Rowe, E., & Curby, T. W. (2013). Disentangling fine motor skills’ relations to academic achievement: the relative contributions of visual-spatial integration and visual- motor coordination. The Journal of Genetic Psychology, 174(5), 514-533. doi: 10.1080/00221325.2012.717122

Catani, M. & ffytche, D. H. (2005). The rises and falls of disconnection syndromes. Brain, 128(10), 2224-2239. doi: 10.1093/brain/awh622

Corsi-Cabrera, M., Galindo-Vilchis, L., del-Río-Portilla, Y., Arce, C., & Ramos-Loyo, J. (2007). Within-subject reliability and inter-session stability of EEG power and coherent activity in women evaluated monthly over nine months. Clinical Neurophysiology, 118(1), 9-21. doi: 10.1016/j.clinph.2006.08.013

Dockree, P. M. & Robertson, I. H. (2011). Electrophysiological markers of cognitive deficits in traumatic brain injury: a review. International Journal of Psychophysiology, 82(1), 53-60. doi: 10.1016/j.ijpsycho.2011.01.004

Ewing-Cobbs, L. & Barnes, M. (2002). Linguistic outcomes following traumatic brain injury in children. Seminars in Pediatric Neurology, 9(3), 209-217. doi: 10.1053/spen.2002.35502

Ewing-Cobbs, L., Barnes, M., Fletcher, J. M., Levin, H. S., Swank, P. R., & Song, J. (2004). Modeling of longitudinal academic achievement scores after pediatric traumatic brain injury. Developmental Neuropsychology, 25(1-2), 107-133. doi: 10.1080/87565641.2004.9651924

Garduño-Hernández, F. (2008). Traumatismo craneoencefálico en niños: Mecanismos de la lesión primaria. Boletín Médico del Hospital Infantil de México, 65(2), 148-153.

Giovagnoli, G., Vicari, S., Tomassetti, S., & Menghini, D. (2016). The Role of Visual-Spatial Abilities in Dyslexia: Age Differences in Children’s Reading? Frontiers in Psychology, 7, 1997. doi: 10.3389/fpsyg.2016.01997

Gmehlin, D., Thomas, C., Weisbrod, M., Walther, S., Resch, F., & Oelkers-Ax, R. (2011). Development of brain synchronisation within school-age–Individual analysis of resting (alpha) coherence in a longitudinal data set. Clinical Neurophysiology, 122(10), 1973-1983. doi: 10.1016/j.clinph.2011.03.016

Gonzato, M. & Godino, J. D. (2010). Aspectos históricos, sociales y educativos de la orientación espacial. Revista Iberoamericana de Educación Matemática, 23, 45-58.

Gorji, A. & Speckmann, E. J. (2009). Epileptiform EEG spikes and their functional significance. Clinical EEG and Neuroscience, 40(4), 230-233. doi: 10.1177/155005940904000404

Han, K., Chapman, S. B., & Krawczyk, D. C. (2016). Disrupted intrinsic connectivity among default, dorsal attention, and frontoparietal control networks in individuals with chronic traumatic brain injury. Journal of the International Neuropsychological Society, 22(2), 263- 279. doi: 10.1017/S1355617715001393

Hannawi, Y. & Stevens, R. D. (2016). Mapping the Connectome following traumatic brain Injury. Current Neurology and Neuroscience Reports, 16(5), 44. doi: 10.1007/s11910-016-0642-9

Hayes, J. P., Bigler, E. D., & Verfaellie, M. (2016). Traumatic brain injury as a disorder of brain connectivity. Journal of the International Neuropsychological Society, 22(2), 120-137. doi: 10.1017/S1355617715000740

Hillary, F. G., Slocomb, J., Hills, E. C., Fitzpatrick, N. M., Medaglia, J. D., Wang, J., ... & Wylie, G. R. (2011). Changes in resting connectivity during recovery from severe traumatic brain injury. International Journal of Psychophysiology, 82(1), 115-123. doi: 10.1016/j.ijpsycho.2011.03.011

Hood, J. & Rankin, P. M. (2005). How do specific memory disorders present in the school classroom? Pediatric Rehabilitation, 8(4), 272-282. doi: 10.1080/13638490400022303

Instituto Nacional de Estadística y Geografía (INEGI). Consultado 09-02-2015 en http:/www.inegi.org.mx/sistemas/TabuladosBasicos/Default

Jiang, Z. Y. (2005). Study on EEG power and coherence in patients with mild cognitive impairment during working memory task. Journal of Zhejiang University Science B, 6(12), 1213-1219. doi: 10.1631/jzus.2005.B1213

Kennedy, M. R. T., Wozniak, J. R., Muetzel, R. L., Mueller, B. A., Chiou, H. H., Pantekoek, K., & Lim, K. O. (2009). White matter and neurocognitive changes in adults with chronic traumatic brain injury. Journal of the International Neuropsychological Society, 15(1), 130-136. doi: 10.1017/S1355617708090024

Khundrakpam, B. S., Lewis, J. D., Zhao, L., Chouinard-Decorte, F., & Evans, A. C. (2016). Brain connectivity in normally developing children and adolescents. Neuroimage, 134, 192-203. doi: 10.1016/j.neuroimage.2016.03.062

Kinnunen, K. M., Greenwood, R., Powell, J. H., Leech, R., Hawkins, P. C., Bonnelle, V., ... & Sharp, D. J. (2011). White matter damage and cognitive impairment after traumatic brain injury. Brain, 134(2), 449-463. doi:

Kirkwood, M. W., Yeates, K. O., Taylor, H. G., Randolph, C., McCrea, M., & Anderson, V. A. (2008). Management of pediatric mild traumatic brain injury: A neuropsychological review from injury through recovery. The Clinical Neuropsychologist, 22(5), 769-800. doi: 10.1080/13854040701543700

Kraus, M. F., Susmaras, T., Caughlin, B. P., Walker, C. J., Sweeney, J. A., & Little, D. M. (2007). White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain, 130(10), 2508-2519. doi: 10.1093/brain/awm216

Levin, H. S. & Hanten, G. (2005). Executive functions after traumatic brain injury in children. Pediatric Neurology, 33(2), 79-93. doi: 10.1016/j.pediatrneurol.2005.02.002

Lonnemann, J., Krinzinger, H., Knops, A., & Willmes, K. (2008). Spatial representations of numbers in children and their connection with calculation abilities. Cortex, 44(4), 420-428. doi: 10.1016/j.cortex.2007.08.015

Matute, E., Rosselli, M., Ardila, A., & Ostrosky-Solís, F. (2007). ENI: Evaluación Neuropsicológica Infantil. Guadalajara, México: Manual Moderno/Universidad de Guadalajara.

Monsell, S. (2003). Task switching. Trends in Cognitive Sciences, 7(3), 134-140. doi: 10.1016/S1364-6613(03)00028-7

Murias, M., Swanson, J. M., & Srinivasan, R. (2007). Functional connectivity of frontal cortex in healthy and ADHD children reflected in EEG coherence. Cerebral Cortex, 17(8), 1788- 1799. doi: 10.1093/cercor/bhl089

Muscara, F., Catroppa, C., & Anderson, V. (2008). The impact of injury severity on executive function 7–10 years following pediatric traumatic brain injury. Developmental Neuropsychology, 33(5), 623-636. doi: 10.1080/87565640802171162

Nadebaum, C., Anderson, V., & Catroppa, C. (2007). Executive function outcomes following traumatic brain injury in young children: a five year follow-up. Developmental Neuropsychology, 32(2), 703-728. doi: 10.1080/87565640701376086

Nakayama, N., Okumura, A., Shinoda, J., Yasokawa, Y. T., Miwa, K., Yoshimura, S. I., & Iwama, T. (2006). Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. Journal of Neurology, Neurosurgery & Psychiatry, 77(7), 850-855. doi: 10.1136/jnnp.2005.077875

Nunez, P. L., Srinivasan, R., Westdorp, A. F., Wijesinghe, R. S., Tucker, D. M., Silberstein, R. B., & Cadusch, P. J. (1997). EEG coherency: I: statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. Electroencephalography and Clinical Neurophysiology, 103(5), 499-515. doi: 10.1016/S0013-4694(97)00066-7

Olde Dubbelink, K. T. E., Felius, A., Verbunt, J. P. A., Van Dijk, B. W., Berendse, H. W., Stam, C. J., & Delemarre-van de Waal, H. A. (2008). Increased resting-state functional connectivity in obese adolescents; a magnetoencephalographic pilot study. PLoS One, 3(7), e2827. doi: 10.1371/journal.pone.0002827

Olive, T. & Passerault, J. M. (2012). The visuospatial dimension of writing. Written Communication, 29(3), 326-344. doi: 10.1177/0741088312451111

Palacios, E. M., Sala-Llonch, R., Junque, C., Roig, T., Tormos, J. M., Bargallo, N., & Vendrell, P. (2013). Resting-state functional magnetic resonance imaging activity and connectivity and cognitive outcome in traumatic brain injury. JAMA Neurology, 70(7), 845-851. doi: 10.1001/jamaneurol.2013.38

Pan, S. Y., Ugnat, A. M., Semenciw, R., Desmeules, M., Mao, Y., & Macleod, M. (2006). Trends in childhood injury mortality in Canada, 1979-2002. Injury Prevention, 12(3), 155-160. doi: 10.1136/ip.2005.010561

Paus, T. (2007). Maturation of structural and functional connectivity in the human brain. In: V. K. Jirsa, A. McIntosh (Eds), Handbook of Brain Connectivity, Understanding Complex Systems (pp. 463-475). Springer, Berlin, Heidelberg. 10.1007/978-3-540-71512-2_16

Pentland, V. A. L. (1998). Residual attention deficits following childhood head injury: Implications for ongoing development. Neuropsychological Rehabilitation, 8(3), 283-300. doi: 10.1080/713755569

Ramlackhansingh, A. F., Brooks, D. J., Greenwood, R. J., Bose, S. K., Turkheimer, F. E., Kinnunen, K. M., ... & Sharp, D. J. (2011). Inflammation after trauma: microglial activation and traumatic brain injury. Annals of Neurology, 70(3), 374-383. doi: 10.1002/ana.22455

Rigon, A., Duff, M. C., McAuley, E., Kramer, A. F., & Voss, M. W. (2016). Is traumatic brain injury associated with reduced inter-hemispheric functional connectivity? A study of large-scale resting state networks following traumatic brain injury. Journal of Neurotrauma, 33(11), 977-989. doi: 10.1089/neu.2014.3847

Sakkalis, V. (2011). Review of advanced techniques for the estimation of brain connectivity measured with EEG/MEG. Computers in Biology and Medicine, 41(12), 1110-1117. doi: 10.1016/j.compbiomed.2011.06.020

Sharp, D. J., Beckmann, C. F., Greenwood, R., Kinnunen, K. M., Bonnelle, V., De Boissezon, X., ... & Leech, R. (2011). Default mode network functional and structural connectivity after traumatic brain injury. Brain, 134(8), 2233-2247. doi: 10.1093/brain/awr175

Smith, D. H., Meaney, D. F., & Shull, W. H. (2003). Diffuse axonal injury in head trauma. The Journal of Head Trauma Rehabilitation, 18(4), 307-316. PMID: 16222127

Sours, C., Zhuo, J., Roys, S., Shanmuganathan, K., & Gullapalli, R. P. (2015). Disruptions in resting state functional connectivity and cerebral blood flow in mild traumatic brain injury patients. PloS One, 10(8), e0134019. doi: 10.1371/journal.pone.0134019

Sporns, O. (2003). Graph theory methods for the analysis of neural connectivity patterns. In: R. Kötter (Ed.), Neuroscience databases (pp. 171-185). Boston, MA: Springer. doi: 10.1007/978-1-4615-1079-6_12

Stam, C. J. & de Bruin, E. A. (2004). Scale‐free dynamics of global functional connectivity in the human brain. Human Brain Mapping, 22(2), 97-109. doi: 10.1002/hbm.20016

Stam, C. J. & van Straaten, E. C. W. (2012). The organization of physiological brain networks. Clinical Neurophysiology, 123(6), 1067-1087. doi: 10.1016/j.clinph.2012.01.011

Stevens, M. C., Lovejoy, D., Kim, J., Oakes, H., Kureshi, I., & Witt, S. (2012). Multiple resting state network functional connectivity abnormalities in mild traumatic brain injury. Brain Imaging and Behavior, 6(2), 293-318. doi: 10.1007/s11682-012-9157-4

Stocchetti, N., Conte, V., Ghisoni, L., Canavesi, K., & Zanaboni, C. (2010). Traumatic brain injury in pediatric patients. Minerva Anestesiologica, 76(12), 1052-1059. PMID:21178914

Strogatz, S. H. (2001). Exploring complex networks. Nature, 410(6825), 268-276. doi: 10.1038/35065725

Taylor, H. G. & Alden, J. (1997). Age-related differences in outcomes following childhood brain insults: an introduction and overview. Journal of the International Neuropsychological Society, 3(6), 555-567.

Taylor, H. G., Yeates, K. O., Wade, S. L., Drotar, D., Stancin, T., & Minich, N. (2002). A prospective study of short-and long-term outcomes after traumatic brain injury in children: behavior and achievement. Neuropsychology, 16(1), 15-27. doi: 10.1037/0894-4105.16.1.15

Thatcher, R. W., Krause, P. J., & Hrybyk, M. (1986). Cortico-cortical associations and EEG coherence: a two-compartmental model. Electroencephalography and Clinical Neurophysiology, 64(2), 123-143. doi: 10.1016/0013-4694(86)90107-0

Thatcher, R. W., North, D. M., & Biver, C. J. (2008). Development of cortical connections as measured by EEG coherence and phase delays. Human Brain Mapping, 29(12), 1400-1415. doi: 10.1002/hbm.20474

van Diessen, E., Numan, T., van Dellen, E., van der Kooi, A. W., Boersma, M., Hofman, D., ... & Stam, C. J. (2015). Opportunities and methodological challenges in EEG and MEG resting state functional brain network research. Clinical Neurophysiology, 126(8), 1468-1481. doi: 10.1016/j.clinph.2014.11.018

van Duinkerken, E., Klein, M., Schoonenboom, N. S., Hoogma, R. P., Moll, A. C., Snoek, F. J., ... & Diamant, M. (2009). Functional Brain Connectivity and Neurocognitive Functioning in Patients with Long-standing Type 1 Diabetes with and without Microvascular Complications: a Magnetoencephalography Study. Diabetes, 58(10), 2335-2343. doi: 10.2337/db09-0425

Vidyasagar, T. R. & Pammer, K. (2010). Dyslexia: a deficit in visuo-spatial attention, not in phonological processing. Trends in Cognitive Sciences, 14(2), 57-63. doi: 10.1016/j.tics.2009.12.003

von Stein, A. & Sarnthein, J. (2000). Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. International Journal of Psychophysiology, 38(3), 301-313. doi: 10.1016/S0167- 8760(00)00172-0

von Stein, A., Rappelsberger, P., Sarnthein, J., & Petsche, H. (1999). Synchronization between temporal and parietal cortex during multimodal object processing in man. Cerebral Cortex, 9(2), 137-150. doi: 10.1093/cercor/9.2.137

Welch, P. (1967). The use of fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Transactions on Audio and Electroacoustics, 15(2), 70-73. doi: 10.1109/TAU.1967.1161901

Whittington, M. A., Faulkner, H. J., Doheny, H. C., & Traub, R. D. (2000). Neuronal fast oscillations as a target site for psychoactive drugs. Pharmacology & Therapeutics, 86(2), 171-190. doi: 10.1016/S0163-7258(00)00038-3

Wood, G. & Fischer, M. H. (2008). Numbers, space, and action–from finger counting to the mental number line and beyond. Cortex, 44(4), 353-358. doi: 10.1016/j.cortex.2008.01.002

Xu, J., Rasmussen, I. A., Lagopoulos, J., & Håberg, A. (2007). Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. Journal of Neurotrauma, 24(5), 753-765. doi: 10.1089/neu.2006.0208

Yeates, K. O., Blumenstein, E., Patterson, C. M., & Delis, D. C. (1995). Verbal learning and memory following pediatric closed-head injury. Journal of the International Neuropsychological Society, 1(1), 78-87. doi: 10.1017/S1355617700000138

Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., ... & Buckner, R. L. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106(3), 1125-1165. doi: 10.1152/jn.00338.2011

Zhou, Y., Milham, M. P., Lui, Y. W., Miles, L., Reaume, J., Sodickson, D. K., ... & Ge, Y. (2012). Default-mode network disruption in mild traumatic brain injury. Radiology, 265(3), 882- 892. doi: 10.1148/radiol.12120748