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Journal of Neurology, Neurosurgery, and Psychiatry logoLink to Journal of Neurology, Neurosurgery, and Psychiatry
. 2000 Aug;69(2):210–216. doi: 10.1136/jnnp.69.2.210

Volume of focal brain lesions and hippocampal formation in relation to memory function after closed head injury in children

S Di 1, J Bachevalier 1, H Levin 1, J Song 1, R Scheibel 1, J Fletcher 1
PMCID: PMC1737037  PMID: 10896695

Abstract

OBJECTIVES—(1) A study of verbal learning and memory in children who had sustained a closed head injury (CHI) at least 3 months earlier. (2) To relate memory function to focal brain lesion and hippocampal formation volumes using morphometric analysis of MRI.
METHODS—A group of 245 children who had been admitted to hospital for CHI graded by the Glasgow coma scale (GCS), including 161 patients with severe and 84 with mild CHI completed the California verbal learning test (CVLT) and underwent MRI which was analysed for focal brain lesion volume independently of memory test data. Brain MRI with 1.5 mm coronal slices obtained in subsets of 25 patients with severe and 25 patients with mild CHI were analysed for hippocampal formation volume. Interoperator reliability in morphometry was satisfactory.
RESULTS—Severity of CHI and age at study significantly affected memory performance. Regression analysis showed that bifrontal, left frontal, and right frontal lesion volumes incremented prediction of various learning and memory indices after entering the GCS score and age into the model. Extrafrontal lesion volume did not contribute to predicting memory performance.
CONCLUSIONS—Prefrontal lesions contribute to residual impairment of learning and memory after severe CHI in children. Although effects of CHI on hippocampal formation volume might be difficult to demonstrate in non-fatal paediatric CHI, further investigation using functional brain imaging could potentially demonstrate hippocampal dysfunction.



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Selected References

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  1. Adams J. H., Graham D. I., Murray L. S., Scott G. Diffuse axonal injury due to nonmissile head injury in humans: an analysis of 45 cases. Ann Neurol. 1982 Dec;12(6):557–563. doi: 10.1002/ana.410120610. [DOI] [PubMed] [Google Scholar]
  2. Benes F. M., Turtle M., Khan Y., Farol P. Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch Gen Psychiatry. 1994 Jun;51(6):477–484. doi: 10.1001/archpsyc.1994.03950060041004. [DOI] [PubMed] [Google Scholar]
  3. Berryhill P., Lilly M. A., Levin H. S., Hillman G. R., Mendelsohn D., Brunder D. G., Fletcher J. M., Kufera J., Kent T. A., Yeakley J. Frontal lobe changes after severe diffuse closed head injury in children: a volumetric study of magnetic resonance imaging. Neurosurgery. 1995 Sep;37(3):392–400. doi: 10.1227/00006123-199509000-00004. [DOI] [PubMed] [Google Scholar]
  4. Bigler E. D., Blatter D. D., Anderson C. V., Johnson S. C., Gale S. D., Hopkins R. O., Burnett B. Hippocampal volume in normal aging and traumatic brain injury. AJNR Am J Neuroradiol. 1997 Jan;18(1):11–23. [PMC free article] [PubMed] [Google Scholar]
  5. Brink J. D., Garrett A. L., Hale W. R., Nickel V. L., Woo-Sam J. Recovery of motor and intellectual function in children sustaining severe head injuries. Dev Med Child Neurol. 1970 Oct;12(5):565–571. doi: 10.1111/j.1469-8749.1970.tb01963.x. [DOI] [PubMed] [Google Scholar]
  6. Chugani H. T., Chugani D. C. Basic mechanisms of childhood epilepsies: studies with positron emission tomography. Adv Neurol. 1999;79:883–891. [PubMed] [Google Scholar]
  7. Diamond A. Rate of maturation of the hippocampus and the developmental progression of children's performance on the delayed non-matching to sample and visual paired comparison tasks. Ann N Y Acad Sci. 1990;608:394–433. doi: 10.1111/j.1749-6632.1990.tb48904.x. [DOI] [PubMed] [Google Scholar]
  8. Free S. L., Bergin P. S., Fish D. R., Cook M. J., Shorvon S. D., Stevens J. M. Methods for normalization of hippocampal volumes measured with MR. AJNR Am J Neuroradiol. 1995 Apr;16(4):637–643. [PMC free article] [PubMed] [Google Scholar]
  9. Gennarelli T. A., Thibault L. E., Adams J. H., Graham D. I., Thompson C. J., Marcincin R. P. Diffuse axonal injury and traumatic coma in the primate. Ann Neurol. 1982 Dec;12(6):564–574. doi: 10.1002/ana.410120611. [DOI] [PubMed] [Google Scholar]
  10. Giedd J. N., Vaituzis A. C., Hamburger S. D., Lange N., Rajapakse J. C., Kaysen D., Vauss Y. C., Rapoport J. L. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. J Comp Neurol. 1996 Mar 4;366(2):223–230. doi: 10.1002/(SICI)1096-9861(19960304)366:2<223::AID-CNE3>3.0.CO;2-7. [DOI] [PubMed] [Google Scholar]
  11. Goldman P. S. Functional recovery after lesions of the nervous systems. 3. Developmental processes in neural plasticity. Recovery of function after CNS lesions in infant monkeys. Neurosci Res Program Bull. 1974 Jun;12(2):217–222. [PubMed] [Google Scholar]
  12. Grasby P. M., Frith C. D., Friston K. J., Bench C., Frackowiak R. S., Dolan R. J. Functional mapping of brain areas implicated in auditory--verbal memory function. Brain. 1993 Feb;116(Pt 1):1–20. doi: 10.1093/brain/116.1.1. [DOI] [PubMed] [Google Scholar]
  13. Hillman G. R., Kent T. A., Kaye A., Brunder D. G., Tagare H. Measurement of brain compartment volumes in MR using voxel composition calculations. J Comput Assist Tomogr. 1991 Jul-Aug;15(4):640–646. doi: 10.1097/00004728-199107000-00021. [DOI] [PubMed] [Google Scholar]
  14. Huttenlocher P. R., Dabholkar A. S. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol. 1997 Oct 20;387(2):167–178. doi: 10.1002/(sici)1096-9861(19971020)387:2<167::aid-cne1>3.0.co;2-z. [DOI] [PubMed] [Google Scholar]
  15. Janowsky J. S., Shimamura A. P., Kritchevsky M., Squire L. R. Cognitive impairment following frontal lobe damage and its relevance to human amnesia. Behav Neurosci. 1989 Jun;103(3):548–560. doi: 10.1037//0735-7044.103.3.548. [DOI] [PubMed] [Google Scholar]
  16. Jetter W., Poser U., Freeman R. B., Jr, Markowitsch H. J. A verbal long term memory deficit in frontal lobe damaged patients. Cortex. 1986 Jun;22(2):229–242. doi: 10.1016/s0010-9452(86)80047-8. [DOI] [PubMed] [Google Scholar]
  17. Kotapka M. J., Gennarelli T. A., Graham D. I., Adams J. H., Thibault L. E., Ross D. T., Ford I. Selective vulnerability of hippocampal neurons in acceleration-induced experimental head injury. J Neurotrauma. 1991 Winter;8(4):247–258. doi: 10.1089/neu.1991.8.247. [DOI] [PubMed] [Google Scholar]
  18. Kotapka M. J., Graham D. I., Adams J. H., Doyle D., Gennarelli T. A. Hippocampal damage in fatal paediatric head injury. Neuropathol Appl Neurobiol. 1993 Apr;19(2):128–133. doi: 10.1111/j.1365-2990.1993.tb00417.x. [DOI] [PubMed] [Google Scholar]
  19. Kotapka M. J., Graham D. I., Adams J. H., Gennarelli T. A. Hippocampal pathology in fatal human head injury without high intracranial pressure. J Neurotrauma. 1994 Jun;11(3):317–324. doi: 10.1089/neu.1994.11.317. [DOI] [PubMed] [Google Scholar]
  20. Levin H. S., Culhane K. A., Fletcher J. M., Mendelsohn D. B., Lilly M. A., Harward H., Chapman S. B., Bruce D. A., Bertolino-Kusnerik L., Eisenberg H. M. Dissociation between delayed alternation and memory after pediatric head injury: relationship to MRI findings. J Child Neurol. 1994 Jan;9(1):81–89. doi: 10.1177/088307389400900121. [DOI] [PubMed] [Google Scholar]
  21. Levin H. S., Culhane K. A., Mendelsohn D., Lilly M. A., Bruce D., Fletcher J. M., Chapman S. B., Harward H., Eisenberg H. M. Cognition in relation to magnetic resonance imaging in head-injured children and adolescents. Arch Neurol. 1993 Sep;50(9):897–905. doi: 10.1001/archneur.1993.00540090008004. [DOI] [PubMed] [Google Scholar]
  22. Levin H. S., High W. M., Jr, Ewing-Cobbs L., Fletcher J. M., Eisenberg H. M., Miner M. E., Goldstein F. C. Memory functioning during the first year after closed head injury in children and adolescents. Neurosurgery. 1988 Jun;22(6 Pt 1):1043–1052. doi: 10.1227/00006123-198806010-00012. [DOI] [PubMed] [Google Scholar]
  23. Levin H. S. Memory deficit after closed head injury. J Clin Exp Neuropsychol. 1990 Jan;12(1):129–153. doi: 10.1080/01688639008400960. [DOI] [PubMed] [Google Scholar]
  24. Levin H. S., Mendelsohn D., Lilly M. A., Yeakley J., Song J., Scheibel R. S., Harward H., Fletcher J. M., Kufera J. A., Davidson K. C. Magnetic resonance imaging in relation to functional outcome of pediatric closed head injury: a test of the Ommaya-Gennarelli model. Neurosurgery. 1997 Mar;40(3):432–441. doi: 10.1097/00006123-199703000-00002. [DOI] [PubMed] [Google Scholar]
  25. Massagli T. L., Jaffe K. M., Fay G. C., Polissar N. L., Liao S., Rivara J. B. Neurobehavioral sequelae of severe pediatric traumatic brain injury: a cohort study. Arch Phys Med Rehabil. 1996 Mar;77(3):223–231. doi: 10.1016/s0003-9993(96)90102-1. [DOI] [PubMed] [Google Scholar]
  26. Petrides M., Alivisatos B., Evans A. C. Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5803–5807. doi: 10.1073/pnas.92.13.5803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Povlishock J. T., Erb D. E., Astruc J. Axonal response to traumatic brain injury: reactive axonal change, deafferentation, and neuroplasticity. J Neurotrauma. 1992 Mar;9 (Suppl 1):S189–S200. [PubMed] [Google Scholar]
  28. Schacter D. L., Savage C. R., Alpert N. M., Rauch S. L., Albert M. S. The role of hippocampus and frontal cortex in age-related memory changes: a PET study. Neuroreport. 1996 Apr 26;7(6):1165–1169. doi: 10.1097/00001756-199604260-00014. [DOI] [PubMed] [Google Scholar]
  29. Seress L., Mrzljak L. Postnatal development of mossy cells in the human dentate gyrus: a light microscopic Golgi study. Hippocampus. 1992 Apr;2(2):127–141. doi: 10.1002/hipo.450020205. [DOI] [PubMed] [Google Scholar]
  30. Seress L., Ribak C. E. Postnatal development and synaptic connections of hilar mossy cells in the hippocampal dentate gyrus of rhesus monkeys. J Comp Neurol. 1995 Apr 24;355(1):93–110. doi: 10.1002/cne.903550111. [DOI] [PubMed] [Google Scholar]
  31. Squire L. R., Knowlton B., Musen G. The structure and organization of memory. Annu Rev Psychol. 1993;44:453–495. doi: 10.1146/annurev.ps.44.020193.002321. [DOI] [PubMed] [Google Scholar]
  32. Squire L. R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992 Apr;99(2):195–231. doi: 10.1037/0033-295x.99.2.195. [DOI] [PubMed] [Google Scholar]
  33. Stern C. E., Corkin S., González R. G., Guimaraes A. R., Baker J. R., Jennings P. J., Carr C. A., Sugiura R. M., Vedantham V., Rosen B. R. The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8660–8665. doi: 10.1073/pnas.93.16.8660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stuss D. T., Kaplan E. F., Benson D. F., Weir W. S., Chiulli S., Sarazin F. F. Evidence for the involvement of orbitofrontal cortex in memory functions: an interference effect. J Comp Physiol Psychol. 1982 Dec;96(6):913–925. doi: 10.1037/0735-7036.96.6.913. [DOI] [PubMed] [Google Scholar]
  35. Yeates K. O., Blumenstein E., Patterson C. M., Delis D. C. Verbal learning and memory following pediatric closed-head injury. J Int Neuropsychol Soc. 1995 Jan;1(1):78–87. doi: 10.1017/s1355617700000138. [DOI] [PubMed] [Google Scholar]
  36. Zola-Morgan S., Squire L. R. Neuroanatomy of memory. Annu Rev Neurosci. 1993;16:547–563. doi: 10.1146/annurev.ne.16.030193.002555. [DOI] [PubMed] [Google Scholar]

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