Experience-dependent behavioral plasticity is disturbed following traumatic injury to the immature brain
Abstract
Traumatic brain injury (TBI) is most prevalent in children and young adults. The long-term effects of pediatric TBI include cognitive and behavioral impairments; however, over time, it is difficult to distinguish individual variability in intellect and behavior from sequelae of early injury. Postnatal day (PND) 19 rats underwent lateral fluid percussion (FP) injury, followed by rearing in either standard (STD) or enriched environment (EE) conditions. The hypothesis was that the traditional enhancement of cognitive functioning following EE rearing would be attenuated when this rearing is preceded by TBI at PND19. Thirty days after injury, Morris water maze (MWM) acquisition and subsequent probe trial retention were used to assess the behavioral effects of injury on experience-dependent plasticity induced by housing in EE at two different time windows. MWM acquisition demonstrated improvements following early EE rearing in both sham and injured animals; however, the degree of improvement was greater for uninjured animals. When EE rearing was delayed for 2 weeks after injury, the injury effect was absent and the effect of rearing even stronger. Memory testing in the early EE groups using a delayed probe trial showed an effect of injury and housing, with the sham EE animals benefiting the most. After the delayed EE, sham EE animals again showed more probe target hits, while FPEE animals did not, demonstrating an enduring memory deficit. These data confirm that early TBI has effects on experience-dependent plasticity resulting in long-term neurobehavioral deficits. In addition, the ability to benefit from environmental stimulation following TBI is dependent upon time after injury.
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The developing brain may be more susceptible to poor outcomes following TBI; studies suggest children and adolescents experience prolonged recovery rates after TBI compared to adults and poorer outcome.
“In addition, the developing brain may be more susceptible to poor outcomes following TBI. Studies have suggested that children and adolescents experience prolonged recovery rates after TBI compared to adults [61] and poorer outcome [70].”
From The neuropathology of sport (2014) · cites this paper as [70]
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“Furthermore, and of significant relevance for pediatric rehabilitation, Giza et al.(58) have demonstrated that, in the acute stages after injury, the brains of young rats show experience-dependent plasticity leading to functional improvements.”
BackgroundSozda, C. N., Hoffman, A. N., Olsen, A. S., B, J. P. C. A., ZAFONTE, R. D., & Kline, A. E. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2010.1313 · Cited by 107 · see citing works
“In the developing rat pup, EE has been reported to improve behavioral performance after fluid percussion brain injury (Giza et al., 2005), and to enhance dendritic density in the occipital cortex ipsilateral to the injury (Ip et al., 2002).”
Kline, A. E., Wagner, A., Westergom, B. P., Malena, R. R., ZAFONTE, R. D., Olsen, A. S., Sozda, C. N., Luthra, P., Panda, M., & B, J. P. C. A. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.11.036 · Cited by 107 · see citing works
“In addition to the plasticityassociated adaptations, EE has also been shown to improve behavioral performance and sensory neglect after brain trauma in both adult [31,40,82] and developing rats [32].”
BackgroundConcussion Pathophysiology and Injury Biomechanics
Romeu-Mejia, R. A., Giza, C. C., & Goldman, J. (2019) · Current Reviews in Musculoskeletal Medicine · doi:10.1007/s12178-019-09536-8 · Cited by 102 · see citing works
Self-citationBondi, C. O., Klitsch, K. C., Leary, J. B., & Kline, A. E. (2014) · Journal of Neurotrauma · doi:10.1089/neu.2014.3328 · Cited by 101 · see citing works
“To further characterize the time-dependent behavioral responses to EE exposure after moderate TBI during development, PND 19 rats underwent lateral FP injury followed by rearing in EE or STD housing.(102) Experience-dependent plasticity was assessed by two different EE treatments consisting of an early EE group expose…”
BackgroundMethodMondello, S., Kobeissy, F., Vestri, A., Hayes, R. L., Kochanek, P. M., & Berger, R. P. (2016) · Scientific Reports · doi:10.1038/srep28203 · Cited by 110 · see citing works
Social dysfunction after pediatric traumatic brain injury: A translational perspective
Ryan, N. P., Catroppa, C., Godfrey, C., Noble‐Haeusslein, L. J., Shultz, S. R., O'Brien, T. J., Anderson, V. A., & Semple, B. D. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.02.020 · Cited by 95 · see citing works
“An enriching environment is important for optimal development for children (Belsky and de Haan, 2011), and evidence shows that the quality of the environment may play an even greater role in the context of recovery from early brain insult (Anderson et al., 2012; Giza et al., 2005; Greenough et al., 1987).”
BackgroundFound in translation: Understanding the biology and behavior of experimental traumatic brain injury
Bondi, C. O., Semple, B. D., Noble‐Haeusslein, L. J., Osier, N. D., Carlson, S. W., Dixon, C. E., Giza, C. C., & Kline, A. E. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.004 · Cited by 91 · see citing works
“, 2002) or behavioral enhancements, such as improved spatial learning and memory (Giza et al., 2005) typically induced by such experience (as described in the Bondi et al.”
BackgroundSelf-citationOjo, J. O., Mouzon, B., & Crawford, F. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.06.003 · Cited by 88 · see citing works
Neurochemical cascade of concussion
MacFarlane, M. P., & Glenn, T. C. (2015) · Brain Injury · doi:10.3109/02699052.2014.965208 · Cited by 88 · see citing works
Functional Assessment of Long-Term Deficits in Rodent models of Traumatic Brain Injury
Gold, E. M., Su, D., López-Velázquez, L., Haus, D. L., Perez, H. D., Lacuesta, G. A., Anderson, A. J., & Cummings, B. J. (2013) · Regenerative Medicine · doi:10.2217/rme.13.41 · Cited by 87 · see citing works
Phthalates and neurotoxic effects on hippocampal network plasticity
Holahan, M. R., & Smith, C. A. (2015) · NeuroToxicology · doi:10.1016/j.neuro.2015.02.008 · Cited by 85 · see citing works
Hitting a moving target: Basic mechanisms of recovery from acquired developmental brain injury
Giza, C. C., Kolb, B. E., Harris, N. G., Asarnow, R. F., & Prins, M. L. (2009) · Developmental Neurorehabilitation · doi:10.3109/17518420903087558 · Cited by 76 · see citing works
“However, even in the absence of cell death, injury-induced functional disturbances have been demonstrated in animal models of TBI [64,69,106].”
BackgroundSelf-citationClinical Features of Repetitive Traumatic Brain Injury and Chronic Traumatic Encephalopathy
Montenigro, P. H., Bernick, C. B., & Cantu, R. C. (2015) · Brain Pathology · doi:10.1111/bpa.12250 · Cited by 77 · see citing works
“(vi) Because of the unique features of the maturing brain, young athletes are more vulnerable to the effects of a concussion than adults (32, 76).”
BackgroundHotz, G., Castelblanco, A., Lara, I. M., Weiss, A. D., DUNCAN, R. C., & Kuluz, J. W. (2006) · Brain Injury · doi:10.1080/02699050600832635 · Cited by 74 · see citing works
“[17], studied baby rats following a fluid percussion injury reared in either a standard or enriched environment.”
BackgroundResponse of the Contralateral Hippocampus to Lateral Fluid Percussion Brain Injury
Tran, L. D., Lifshitz, J., Witgen, B., Schwarzbach, E., Cohen, A., & Grady, M. (2006) · Journal of Neurotrauma · doi:10.1089/neu.2006.23.1330 · Cited by 67 · see citing works
“The natural course of cognitive recovery after brain injury may include a stunned period of cellular and circuit dysfunction, not necessarily death (Witgen et al., 2005; Atkins et al., 2006), where implementing therapeutic interventions may be futile (Giza et al., 2005).”
Zanier, E., Lee, S. M., Vespa, P., Giza, C., & Hovda, D. (2003) · Journal of Neurotrauma · doi:10.1089/089771503765355496 · Cited by 66 · see citing works
Self-citationPathophysiology of Sports-Related Concussion
Giza, C. C., & DiFiori, J. P. (2010) · Sports Health A Multidisciplinary Approach · doi:10.1177/1941738110391732 · Cited by 64 · see citing works
“Rats reared in EE develop more elaborate neuronal connections, increased cerebral cortex thickness, higher levels of plasticity-related molecules (BDNF and NMDA receptors), and superior cognition.78 After concussive brain injury, immature rats do not respond to rearing in an EE.19,25,40 Rats do not show increases in c…”
BackgroundInfluentialSelf-citationSchneider, D. K., Galloway, R. T., Bazarian, J. J., Diekfuss, J. A., Dudley, J. A., Leach, J. L., Mannix, R., Talavage, T. M., Yuan, W., & Myer, G. D. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2019.6398 · Cited by 65 · see citing works
“65,71 A recent study of former National Football League players reported that early exposure to American football (before the age of 12 years) was associated with neurocognitive impairments in older adults, 70 which the authors attributed to damage to the corpus callosum from head impacts during…”
Gaulke, L. J., Horner, P. J., Fink, A. J. P., McNamara, C. L., & Hicks, R. R. (2005) · Molecular Brain Research · doi:10.1016/j.molbrainres.2005.08.011 · Cited by 59 · see citing works
“Besides gender [54,76], there are numerous other factors, including species, [6], age [81], the onset and duration of the EE [20,54], and the type of injury [5] that may also explain the differential effects of EE among various studies.”
BackgroundRepeat traumatic brain injury in the developing brain
Prins, M. L., & Giza, C. C. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.05.009 · Cited by 60 · see citing works
“…is less clear that these advantages translate to diffuse injuries such as TBI, where developmental plasticity is impaired after fluid percussion (Fineman et al., 2000; Giza et al., 2005), and where clinical developmental trajectories may diverge from normal over time (Babikian and Asarnow, 2009).”
Self-citationHolguin, S., Huang, Y., Liu, J., & Wurtman, R. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.042 · Cited by 57 · see citing works
“We observe that giving IC rats either dietary UMP or gavaged DHA improves performance on the hidden version of the Morris water maze (all P<0.05), a hippocampal-dependent task; co-administration of both phosphatide precursors further enhances the IC rats' performance on this task (P<0.001).”
BackgroundInfluentialEnvironmental enrichment protects against functional deficits caused by traumatic brain injury
Johnson, E. M., Traver, K. L., Hoffman, S. W., Harrison, C. R., & Herman, J. P. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00044 · Cited by 57 · see citing works
“The neurological and behavioral effects of EE reduce TBI-induced deficits and improve recovery time (Will et al., 1977, 2004; Passineau et al., 2001; Chen et al., 2005; Gaulke et al., 2005; Giza et al., 2005; Wagner et al., 2005; Kline et al., 2007).”
BackgroundMethodEnvironmental Contributions to Social and Mental Health Outcomes Following Pediatric Stroke
Greenham, M., Hearps, S. J. C., Gomes, A., Rinehart, N., Gonzalez, L., Gordon, A., Mackay, M. T., Lo, W. D., Yeates, K. O., & Anderson, V. A. (2015) · Developmental Neuropsychology · doi:10.1080/87565641.2015.1095191 · Cited by 52 · see citing works
Ratner, V. I., Kishkurno, S. V., Slinko, S., Sosunov, S. A., Sosunov, A. A., Polin, R. A., & Ten, V. S. (2007) · Neonatology · doi:10.1159/000100086 · Cited by 51 · see citing works
Kline, A. E., Olsen, A. S., Sozda, C. N., Hoffman, A. N., & B, J. P. C. A. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2012.2385 · Cited by 49 · see citing works
“…cortical impact (CCI; Chen et al., 2005; de Witt et al., 2011; Hoffman et al., 2008; Kline et al., 2007,2010; Matter et al., 2011; Sozda et al., 2010) and fluid percussion (Hamm et al., 1996; Hicks et al., 2002; Gaulke et al., 2005; Giza et al., 2005; Maegele et al., 2005; Passineau et al., 2001).”
BackgroundEvidence for Impaired Plasticity after Traumatic Brain Injury in the Developing Brain
Li, N., Yang, Y., Glover, D. P., Zhang, J., Saraswati, M., Robertson, C., & Pelled, G. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2013.3059 · Cited by 48 · see citing works
Controlled contusion injury alters molecular systems associated with cognitive performance
Griesbach, G. S., Sutton, R. L., Hovda, D. A., Ying, Z., & Gómez‐Pinilla, F. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21893 · Cited by 48 · see citing works
“Enduring cognitive deficits are a major factor in TBI-induced disabilities, and the hippocampus is among the most vulnerable structures after TBI in humans (Wilde et al., 2007).”
InfluentialSelf-citationMonaco, C. M., Gebhardt, K. M., Chlebowski, S. M., Shaw, K. E., B, J. P. C. A., Henchir, J. J., Zupa, M. F., & Kline, A. E. (2014) · Journal of Neurotrauma · doi:10.1089/neu.2014.3541 · Cited by 45 · see citing works
Pre-clinical models in pediatric traumatic brain injury—challenges and lessons learned
Kochanek, P. M., Wallisch, J. S., Bayır, H., & Clark, R. S. B. (2017) · Child s Nervous System · doi:10.1007/s00381-017-3474-2 · Cited by 44 · see citing works
“[14, 53] carried out a series of studies in a pediatric model of TBI using a modification of FPI in rats.”
BackgroundMethodFoss, K. D. B., Yuan, W., Diekfuss, J. A., Leach, J. L., Meehan, W. P., III, DiCesare, C. A., Solomon, G. S., Schneider, D. K., MacDonald, J. P., Dudley, J. A., et al. (2019) · Clinical Journal of Sport Medicine · doi:10.1097/jsm.0000000000000753 · Cited by 42 · see citing works
Thompson, H. J., LeBold, D. G., Marklund, N., Morales, D. M., Hagner, A. P., & McIntosh, T. K. (2006) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2006-00337 · Cited by 41 · see citing works
Back to the future: rehabilitation of children after brain injury
Forsyth, R. (2010) · Archives of Disease in Childhood · doi:10.1136/adc.2009.161083 · Cited by 34 · see citing works
“presumably due to distraction from task-specific practice, and that environmental enrichment benefits vary with time after injury.”
BackgroundNwafor, D. C., Brichacek, A. L., Foster, C. H., Lucke-Wold, B. P., Ali, A., Colantonio, M. A., Brown, C. M., & Qaiser, R. A. (2022) · Journal of Central Nervous System Disease · doi:10.1177/11795735221098125 · Cited by 30 · see citing works
“Adaptions of the lateral and midline fluid percussion models to the pediatric rat have also been described.(57,58) More recently, a study byNewell et al.”
MethodMaria, N. S. S., Reger, M., Cai, Y., Baquing, M. A. T., Buen, F., Ponnaluri, A. V. S., Hovda, D., Harris, N. G., & Giza, C. C. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2016.4747 · Cited by 26 · see citing works
“16,17 Cortical thickness and dendritic arborization did not significantly increase in FPI animals when measured at approximately PID50.”
Self-citationConcussion History and Cognitive Function in a Large Cohort of Adolescent Athletes
Taylor, K. M., Kioumourtzoglou, M., Clover, J., Coull, B. A., Dennerlein, J. T., Bellinger, D. C., & Weisskopf, M. G. (2018) · The American Journal of Sports Medicine · doi:10.1177/0363546518798801 · Cited by 28 · see citing works
“Whether concussion at early ages is associated with lasting changes in brain plasticity or evolving cognitive functions remains controversial.(13,24) Most studies evaluating the effect of concussions on cognitive function were conducted among collegiate and professional athletes.”
Crowe, L. M., Catroppa, C., & Anderson, V. A. (2015) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63521-1.00041-8 · Cited by 28 · see citing works
Experimental Injury Biomechanics of the Pediatric Head and Brain
Margulies, S. S., & Coats, B. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4154-0_4 · Cited by 27 · see citing works
Bridging the Gap: Mechanisms of plasticity and repair after Pediatric TBI
Maria, N. S. S., Sargolzaei, S., Prins, M., Dennis, E., Asarnow, R., Hovda, D., Harris, N., & Giza, C. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.04.016 · Cited by 25 · see citing works
“FPI in young rats showed reduced amplitude of NMDA-mediated excitatory post-synaptic currents (EPSCs) (down 40-50”
BackgroundInfluentialSelf-citationGurkoff, G. G., Giza, C. C., Shin, D., Auvin, S., Sankar, R., & Hovda, D. A. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.021 · Cited by 26 · see citing works
Self-citationZamani, A., Ryan, N. P., Wright, D. K., Caeyenberghs, K., & Semple, B. D. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2019.6895 · Cited by 25 · see citing works
Cellular and molecular neuronal plasticity
Griesbach, G. S., & Hovda, D. A. (2015) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63521-1.00042-x · Cited by 25 · see citing works
Self-citationMidline (central) fluid percussion model of traumatic brain injury in pediatric and adolescent rats.
Rowe, R. K., Harrison, J., Ellis, T., Adelson, P., & Lifshitz, J. (2018) · Journal of Neurosurgery: Pediatrics · doi:10.3171/2018.1.peds17449 · Cited by 24 · see citing works
Epidemiology and treatment outcome of head injury in children: A prospective study
Nnadi, M., Bankole, O. B., & Fente, B. G. (2014) · Journal of Pediatric Neurosciences · doi:10.4103/1817-1745.147577 · Cited by 24 · see citing works
Hou, X., Zhang, Y., Fei, X., Zhou, Q., & Li, J. (2023) · The American Journal of Sports Medicine · doi:10.1177/03635465221142855 · Cited by 21 · see citing works
“26,49 Several studies reported poorer cognitive function in concussed adolescents compared with control groups, 30,57,107 whereas other studies did not.”
ResultDevelopmental functions of microglia: Impact of psychosocial and physiological early life stress
Smail, M. A., & Lenz, K. M. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110084 · Cited by 22 · see citing works
“While most characterization of these models has focused on neuronal damage, white matter alterations, and behavioral outcomes (Raghupathi and Huh, 2007; Mychasiuk et al., 2015; DeMaster et al., 2017; Semple et al., 2012; Giza et al., 2005), their impact on microglia has in some cases been examined.”
Holcomb, J. M., Fisicaro, R. A., Miller, L. E., Yu, F. F., Davenport, E. M., Xi, Y., Urban, J. E., Wagner, B. C., Powers, A. K., Whitlow, C. T., et al. (2021) · Journal of Neurotrauma · doi:10.1089/neu.2020.7580 · Cited by 21 · see citing works
The Pathophysiology of Sports Concussion
Seifert, T., & Shipman, V. (2015) · Current Pain and Headache Reports · doi:10.1007/s11916-015-0513-0 · Cited by 20 · see citing works
The utility of the Convergence Insufficiency Symptom Survey (CISS) post-concussion
Trbovich, A. M., Sherry, N. S., Henley, J., Emami, K., & Kontos, A. P. (2019) · Brain Injury · doi:10.1080/02699052.2019.1658131 · Cited by 19 · see citing works
A SPECT study of language and brain reorganization three years after pediatric brain injury
Wong, S. B., Chapman, S. B., Cook, L. G., Anand, R., Gamino, J. F., & Devous, M. D. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)57011-6 · Cited by 19 · see citing works
“Studies are needed to determine whether stage-by-stage discourse intervention, in particular, can help mitigate the detrimental and later-emerging effects of disrupted frontal function (Giza et al., 2005).”
BackgroundLimperopoulos, C. (2010) · Seminars in Perinatology · doi:10.1053/j.semperi.2009.12.001 · Cited by 18 · see citing works
Lasting effects of pediatric traumatic brain injury
Giza, C. C. (2006) · Indian Journal of Neurotrauma · doi:10.1016/s0973-0508(06)80005-5 · Cited by 17 · see citing works
Self-citationThe Neurophysiology of Concussion
Hovda, D. A. (2014) · Progress in neurological surgery · doi:10.1159/000358749 · Cited by 16 · see citing works
Self-citationRachubinski, A. L., Maclean, K. N., Evans, J. R., & Bjugstad, K. B. (2012) · Experimental Gerontology · doi:10.1016/j.exger.2012.06.013 · Cited by 16 · see citing works
“A study by Giza et al. (2005) suggests that enrichment given immediately after a brain injury does not have the same preventative actions as enrichment given several weeks after injury.”
Understanding the mechanisms underlying recovery after stroke
Kwakkel, G., Buma, F. E., & Selzer, M. E. (2014) · Cambridge University Press eBooks · doi:10.1017/cbo9780511995590.004 · Cited by 15 · see citing works
Borniger, J. C., Ungerleider, K., Zhang, N., Karelina, K., Magalang, U. J., & Weil, Z. M. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.01.064 · Cited by 15 · see citing works
“What is not clear, however, is whether enrichment can improve sleep in the injured brain as there is evidence that both sleep disruption and brain injury can impair enrichment-induced plasticity (Mirmiran et al., 1983; Giza et al., 2005; Sta Maria et al., 2017).”
An Emotional Go/No-Go fMRI study in adolescents with depressive symptoms following concussion
Ho, R. A., Hall, G. B., Noseworthy, M. D., & DeMatteo, C. A. (2017) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2017.09.021 · Cited by 15 · see citing works
Therapeutic strategies to target acute and long-term sequelae of pediatric traumatic brain injury
Huh, J. W., & Raghupathi, R. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.06.025 · Cited by 14 · see citing works
Wartman, B. C., Gervais, N. J., Smith, C., Comba, R., Mumby, D. G., & Holahan, M. R. (2012) · Brain Research · doi:10.1016/j.brainres.2012.08.012 · Cited by 13 · see citing works
Biegon, A. R., Zaltsman, S. L., & Shohami, E. (2018) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000612 · Cited by 13 · see citing works
Effects of lateral fluid percussion injury on cholinergic markers in the newborn piglet brain
Donat, C. K., Walter, B. L., Kayser, T., Deuther‐Conrad, W., Schliebs, R., Nieber, K., Bauer, R., Härtig, W., & Brust, P. (2009) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2009.10.001 · Cited by 13 · see citing works
“However, previous studies revealed a loss of developmental plasticity leading to sustained post-injury dysfunction with compromised learning and memory capacities after diffuse moderate TBI injury likely without marked impact of secondary injury (Giza et al., 2005).”
Moritz, K. E., Geeck, K., Underly, R. G., Searles, M. A., & Smith, J. S. (2014) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-140414 · Cited by 11 · see citing works
“…symptoms of a large number of experimentally controlled lesions and central nervous percussion injury (FPI) (Passineau et al., 2001), lateral FPI Giza et al., 2005; Hicks et al. 2002), hippocampal lesions (Galani et al., 1997) and blast-induced injury Although benefits observed with the EE…”
Mild Traumatic Brain Injury in Adults and Concussion in Sports
Pardini, J., Bailes, J. E., & Maroon, J. C. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-5316-3.00336-1 · Cited by 10 · see citing works
Pediatric Issues in Sports Concussions
Giza, C. C. (2014) · CONTINUUM Lifelong Learning in Neurology · doi:10.1212/01.con.0000458973.71142.7d · Cited by 10 · see citing works
“Basic neuroscience work also supports the concept that enhancing neural activity outside of the acute injury period may facilitate expression of neurotrophins and promote better cognitive recovery.(44,45)”
BackgroundSelf-citationTrbovich, A. M., Zynda, A. J., Togashi, T., Burley, C., Mucha, A., Collins, M. W., & Kontos, A. P. (2025) · Journal of Neurotrauma · doi:10.1177/08977151251359960 · Cited by 10 · see citing works
Koerte, I. K., Esopenko, C., Hinds, S. R., Shenton, M. E., Bonke, E. M., Bazarian, J. J., Bickart, K. C., Bigler, E. D., Sylvain Bouix, A., Buckley, T. A., et al. (2020) · Brain Imaging and Behavior · doi:10.1007/s11682-020-00370-y · Cited by 9 · see citing works
“Even subtle chronic cognitive dysfunction may adversely affect an adolescent’s developmental trajectory and may lead to impaired psychosocial functioning and ultimately failure to obtain developmental potential (Babikian et al. 2015; Giza et al. 2005; Koerte et al. 2017).”
BackgroundSelf-citationNeurovascular Coupling in Special Operations Forces Combat Soldiers
Roby, P. R., DeCicco, J. P., Chandran, A. S., Barczak‐Scarboro, N. E., DeLellis, S. M., Ford, C. B., Healy, M. L., Means, G. E., Kane, S. F., Lynch, J. H., et al. (2020) · Annals of Biomedical Engineering · doi:10.1007/s10439-020-02604-y · Cited by 9 · see citing works
Epidemiological and clinico-radiological evaluation of head injury in pediatric population
Pandey, S., Sharma, M., Kumar, P., Singh, K., Kumar, P., & Jha, R. P. (2020) · Journal of Pediatric Neurosciences · doi:10.4103/jpn.jpn_44_19 · Cited by 8 · see citing works
Minchew, H. M., Radabaugh, H. L., LaPorte, M. J., Free, K. E., B, J. P. C. A., & Bondi, C. O. (2021) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2021.174174 · Cited by 8 · see citing works
Office-based concussion evaluation, diagnosis, and management: adult
Charek, D. B., Collins, M. W., & Kontos, A. P. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63954-7.00010-0 · Cited by 8 · see citing works
Traumatic Brain Injury in Children
Lerner, J. T., & Giza, C. C. (2017) · Elsevier eBooks · doi:10.1016/b978-0-323-37101-8.00102-8 · Cited by 8 · see citing works
Self-citationPediatric and Adolescent Concussion
Apps, J. N., & Walter, K. D. (2011) · Springer eBooks · doi:10.1007/978-0-387-89545-1 · Cited by 7 · see citing works
Finding effective biomarkers for pediatric traumatic brain injury
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“[1] Following TBI, a child can experience two outcomes: on the one hand, the child can display superior recovery rates to adults, on the other hand, they can demonstrate extended and exacerbated symptoms than those experienced by older patients.[2,3] While knowledge of potential mortality following TBI and improved aw…”
BackgroundDo astrocytes act as immune cells after pediatric TBI?
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“These anatomical changes result in long-term consequences on both motor and cognitive functions (Giza et al., 2005; Ajao et al., 2012; Kamper et al., 2013; Ichkova et al., 2019).”
Effects of VEGF Administration or Neutralization on the BBB of Developing Rat Brain
Ortuzar, N., Argandoña, E., Bengoetxea, H., Leis, O., Bulnes, S., & Lafuente, J. V. (2009) · Acta neurochirurgica. Supplementum · doi:10.1007/978-3-211-98811-4_9 · Cited by 7 · see citing works
“Clinical experience suggests that injury to the immature brain can result in abnormal development and long-standing neurobehavioral impairment ( 10 ), even if there is little evidence of morphological damage (11).”
BackgroundPediatric Emergency Medicine Physicians’ Perspectives of Concussion in Young Children
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A Brief History of Behavioral Assessment Following Experimental Traumatic Brain Injury in Juveniles
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- Authors
- Giza, C. C., Griesbach, G. S., & Hovda, D. A.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Giza, Christopher C.
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2005-02
- Volume
- 157
- Issue
- 1
- Pages
- 11-22
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W2163694945
- Cited by
- 135
- References
- 67
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 4 · 2020: 8 · 2019: 6 · 2018: 8 · 2017: 4 · 2016: 5 · 2015: 18 · 2014: 14 · 2013: 4 · 2012: 9
- FWCI
- 3.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (P50NS030308, NS-27544, R01NS027544, K08NS002197, R21NS048535, NS02197, NS 30308)
- Topics
- Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- traumatic brain injury, pediatric brain injury, experience-dependent plasticity, fluid percussion injury, spatial memory, memory impairment, behavioral plasticity, postnatal development, neurobehavioral deficits
- MeSH terms
- Adaptation, Psychological, Age Factors, Animals, Association Learning, Behavior, Animal, Brain Injuries, Disease Models, Animal, Environment, Housing, Animal, Male, Rats, Sprague-Dawley, Maze Learning, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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