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Hippocampal Lateralization and Memory in Children and Adults

Published online by Cambridge University Press:  07 August 2013

Laura Hopf ,
Maher A. Quraan ,
Michael J. Cheung ,
Margot J. Taylor ,
Jennifer D. Ryan  and
Sandra N. Moses
Laura Hopf
Affiliation:
Rotman Research Institute, Baycrest, Toronto, Ontario Departments of Diagnostic Imaging and Neurosciences & Mental Health, Hospital for Sick Children, Toronto, Ontario
Maher A. Quraan
Affiliation:
Krembil Neuroscience Centre & Toronto Western Research Institute, University Health Network, Toronto, Ontario
Michael J. Cheung
Affiliation:
Rotman Research Institute, Baycrest, Toronto, Ontario Departments of Diagnostic Imaging and Neurosciences & Mental Health, Hospital for Sick Children, Toronto, Ontario
Margot J. Taylor
Affiliation:
Departments of Diagnostic Imaging and Neurosciences & Mental Health, Hospital for Sick Children, Toronto, Ontario Department of Pediatrics, University of Toronto, Toronto, Ontario Department of Psychology, University of Toronto, Toronto, Ontario
Jennifer D. Ryan*
Affiliation:
Rotman Research Institute, Baycrest, Toronto, Ontario Department of Psychology, University of Toronto, Toronto, Ontario Department of Psychiatry, University of Toronto, Toronto, Ontario
Sandra N. Moses
Affiliation:
Rotman Research Institute, Baycrest, Toronto, Ontario Departments of Diagnostic Imaging and Neurosciences & Mental Health, Hospital for Sick Children, Toronto, Ontario
*
Correspondence and reprint requests to: Jennifer Ryan, Rotman Research Institute, 3560 Bathurst Street, Toronto, Ontario, M6A 2E1. E-mail: [email protected]
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Abstract

The neural organization of cognitive processes, particularly hemispheric lateralization, changes throughout childhood and adolescence. Differences in the neural basis of relational memory between children and adults are not well characterized. In this study we used magnetoencephalography to observe the lateralization differences of hippocampal activation in children and adults during performance of a relational memory task, transverse patterning (TP). The TP task was paired with an elemental control task, which does not depend upon the hippocampus. We contrasted two hypotheses; the compensation hypothesis would suggest that more bilateral activation in children would lead to better TP performance, whereas the maturation hypothesis would predict that a more adult-like right-lateralized pattern of hippocampal activation would lead to better performance. Mean-centered partial least squares analysis was used to determine unique patterns of brain activation specific to each task per group, while diminishing activation that is consistent across tasks. Our findings support the maturation hypothesis that a more adult-like pattern of increased right hippocampal lateralization in children leads to superior performance on the TP task. We also found dynamic changes of lateralization throughout the time course for all three groups, suggesting that caution is needed when interpreting conclusions about brain lateralization. (JINS, 2013, 19, 1–11)

Keywords

Magnetoencephalography (MEG)HippocampusDevelopmentChildhood epilepsyLearningBrain mapping
Type
Symposia
Information
Journal of the International Neuropsychological Society , Volume 19 , Issue 10 , November 2013 , pp. 1042 - 1052
Copyright
Copyright © The International Neuropsychological Society 2013 

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References

Alvarado, M.C., Bachvalier, J. (2000). Revisiting the maturation of medial temporal lobe functions in primates. Learning & Memory, 7, 244–256.CrossRefGoogle ScholarPubMed
Alvarado, M.C., Rudy, J.W. (1995). Rats with damage to the hippocampal-formation are impaired on the transverse-patterning problem but not on elemental discriminations. Behavioral Neuroscience, 109, 204–211.CrossRefGoogle Scholar
Benes, F.M. (1989). Myelination of cortical-hippocampal relays during late adolescence. Schizophrenia Bulletin, 15, 585–593.CrossRefGoogle ScholarPubMed
Benes, F.M., Turtle, M., Khan, Y., Farol, P. (1994). Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Archives of General Psychiatry, 51, 477–484.CrossRefGoogle ScholarPubMed
Brauer, J., Friederici, A.D. (2007). Functional neural networks of semantic and syntactic processes in the developing brain. Journal of Cognitive Neuroscience, 19, 1609–1623.CrossRefGoogle ScholarPubMed
Broman, M., Rose, A.L., Hotson, G., Casey, C.M. (1997). Severe anterograde amnesia with onset in childhood as a result of anoxic encephalopathy. Brain, 120(3), 417–433.CrossRefGoogle ScholarPubMed
Chou, T.L., Booth, J.R., Bitan, T., Burman, D.D., Bigio, J.D., Cone, N.E., Cao, F. (2006). Developmental and skill effects on the neural correlates of semantic processing to visually presented words. Human Brain Mapping, 27, 915–924.CrossRefGoogle ScholarPubMed
Cohen, N.J., Eichenbaum, H. (1993). Memory, amnesia, and the hippocampal system. Massachusetts: The MIT Press.Google Scholar
Driscoll, I., Howard, S.R., Prusky, G.T., Rudy, J.W., Sutherland, R.J. (2005). Seahorse wins all races: Hippocampus participates in both linear and non-linear visual discrimination learning. Behavioural Brain Research, 164, 29–35.CrossRefGoogle ScholarPubMed
Efron, B., Tibshirani, R. (1986). Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Statistical science, 54–75.Google Scholar
Everts, R., Harvey, A.S., Lillywhite, L., Wrennall, J., Abbott, D.F., Gonzalez, L., Aderson, V. (2010). Language lateralization correlates with verbal memory performance in children with focal epilepsy. Epilepsia, 51, 627–638.CrossRefGoogle ScholarPubMed
Everts, R., Lidzba, K., Wilke, M., Keifer, C., Mordansini, M., Schroth, G., Steinlin, M. (2009). Strengthening of laterality of verbal and visuospatial functions during childhood and adolescence. Human Brain Mapping, 30, 473–483.CrossRefGoogle ScholarPubMed
Giedd, J.N., Snell, J.W., Lange, N., Rajapakse, J.C., Casey, B.J., Kozuch, P.L., Rapoport, J.L. (1996). Quantitative magnetic resonance imaging of human brain development: Ages 4–18. Cerebral Cortex, 6, 551–560.CrossRefGoogle ScholarPubMed
Gogtay, N., Nugent III, T.F., Herman, D.H., Ordonez, A., Greenstein, D., Hayashi, K.M., Clasen, L., Toga, A.W., Giedd, J.N., Rapoport, J.L., Thompson, P.M. (2006). Dynamic mapping of normal human hippocampal development. Hippocampus, 16, 664–672.CrossRefGoogle ScholarPubMed
Gonzalez, L.M., Anderson, V.A., Wood, S.J., Mitchell, L.A., Harvey, A.S. (2007). The localization and lateralization of memory deficits in children with temporal lobe epilepsy. Epilepsia, 48, 124–132. doi:10.1111/j.1528-1167.2006.00907CrossRefGoogle ScholarPubMed
Hanlon, F.M., Houck, J.M., Lundy, S.L., Euler, M.J., Weisend, M.P., Thoma, R.J., Tesche, C.D. (2011). Bilateral hippocampal dysfunction in schizophrenia. Neuroimage, 58, 1158–1168.CrossRefGoogle ScholarPubMed
Hanlon, F.M., Weisend, M.P., Huang, M., Lee, R.R., Moses, S.N., Paulson, K.M., Cañive, J.M. (2003). A non-invasive method for observing hippocampal function. Neuroreport, 14, 1957–1960.CrossRefGoogle ScholarPubMed
Hanlon, F.M., Weisend, M.P., Yeo, R.A., Huang, M., Lee, R.R., Thoma, R.J., Cañive, J.M. (2005). A specific test of hippocampal deficit in schizophrenia. Behavioral Neuroscience, 119, 863–875.CrossRefGoogle ScholarPubMed
Helton, W.S., Warm, J.S., Tripp, L.D., Matthews, G., Parasuraman, R., Hancock, P.A. (2010). Cerebral lateralization of vigilance: A function of task difficulty. Neuropsychologia, 48(6), 1683–1688.CrossRefGoogle ScholarPubMed
Holland, S.K., Plante, E., Weber Byars, A., Strawsburg, R.H., Schmithorst, V.J., Ball, W.S. (2001). Normal fMRI brain activation patterns in children performing a verb generation task. Neuroimage, 14(4), 837–843. doi:10.1006/nimg.2001.0875CrossRefGoogle ScholarPubMed
Hömberg, V., Bickmann, U., Müller, K. (1993). Ontogeny is different for explicit and implicit memory in humans. Neuroscience Letters, 150, 187–190.CrossRefGoogle ScholarPubMed
Kartsounis, L.D., Rudge, P., Stevens, J.M. (1995). Bilateral lesion of CAl-CA fields of the hippocampus are sufficient to cause a severe amnesic syndrome in humans. Journal of Neurology, Neurosurgery, and Psychiatry, 59, 95–96.CrossRefGoogle Scholar
Kretschmann, H.J., Kammradt, G., Krauthausen, I., Sauer, B., Wingert, F. (1986). Growth of the hippocampal formation in man. Bibliotheca Anatomica, 28, 27–52.Google Scholar
Lebel, C., Beaulieu, C. (2009). Lateralization of the arcuate fasciculus from childhood to adulthood and its relation to cognitive abilities in children. Human Brain Mapping, 30, 3563–3573.CrossRefGoogle ScholarPubMed
Leirer, V.M., Wienbruch, C., Paul-Jordanov, I., Kolassa, S., Elbert, T., Kolassa, I.T. (2010). Hippocampal activity during the transverse patterning task declines with cognitive competence but not with age. BMC Neuroscience, 11, 113.CrossRefGoogle Scholar
McIntosh, A.R., Lobaugh, N.J. (2004). Partial least squares analysis of neuroimaging data: Applications and advances. Neuroimage, 23, S250–S263.CrossRefGoogle ScholarPubMed
McIntosh, A.R., Bookstein, F.L., Haxby, J.V., Grady, C.L. (1996). Spatial pattern analysis of functional brain images using Partial Least Squares. Neuroimage, 3(3), 143–157.CrossRefGoogle ScholarPubMed
Meltzer, J.A., Nigishi, M., Constable, T. (2008). Biphasic hemodynamic responses influence deactivation and may mask activation in block-design fMRI paradigms. Human Brain Mapping, 29, 385–399.CrossRefGoogle ScholarPubMed
Mills, T., Lalancette, M., Moses, S.N., Taylor, M.J., Quraan, M.A. (2012). Techniques for detection and localization of weak hippocampal and medial frontal sources using beamformers in MEG. Brain Topography, 25(3), 248–263.CrossRefGoogle ScholarPubMed
Moses, S.N., Ostreicher, M.L., Rosenbaum, R.S., Ryan, J.D. (2008). Successful transverse patterning in amnesia using semantic knowledge. Hippocampus, 18, 121–124.CrossRefGoogle ScholarPubMed
Moses, S.N., Ryan, J.D., Bardouille, T., Kovacevis, N., Hanlon, F.M., McIntosh, A.R. (2009). Semantic information alters neural activation during transverse patterning performance. Neuroimage, 45(3), 863–873.CrossRefGoogle Scholar
Opitz, B., Friederici, A.D. (2003). Interactions of the hippocampal system and the prefrontal cortex in learning language-like rules. Neuroimage, 19(4), 1730–1737.CrossRefGoogle ScholarPubMed
Ostergaard, A.L. (1987). Episodic, semantic and procedural memory in a case of amnesia at an early age. Neuropsychologia, 25(2), 341–357.CrossRefGoogle Scholar
Overman, W.H., Pate, B.J., Moore, K., Peuster, A. (1996). Ontogeny of place learning in children as measured in the radial arm maze, Morris search task, and open field task. Behavioral Neuroscience, 110, 1205–1228.CrossRefGoogle ScholarPubMed
Quraan, M.A., Moses, S.N., Hung, Y., Mills, T., Taylor, M.J. (2011). Detection and localization of evoked deep brain activity using MEG. Human Brain Mapping, 32(5), 812–827.CrossRefGoogle ScholarPubMed
Quraan, M.A., Cheyne, D. (2010). Reconstruction of correlated brain activity with adaptive spatial filters in MEG. Neuroimage, 49(3), 2387–2400.CrossRefGoogle ScholarPubMed
Reed, J.M., Squire, L.R. (1999). Impaired transverse patterning in human amnesia is a special case of impaired memory for two-choice discrimination tasks. Behavioral Neuroscience, 113, 3–9.CrossRefGoogle ScholarPubMed
Rickard, T.C., Grafman, J. (1998). Losing their configural mind: Amnesic patients fail on transverse patterning. Journal of Cognitive Neuroscience, 10, 509–516.CrossRefGoogle ScholarPubMed
Rickard, T.C., Verfaellie, M., Grafman, J. (2006). Transverse patterning and human amnesia. Journal of Cognitive Neuroscience, 18, 1723–1733.CrossRefGoogle ScholarPubMed
Reiterer, S.M., Erb, M., Droll, C.D., Anders, S., Ethofer, T., Grodd, W., Wildgruber, D. (2005). Impact of task difficulty on lateralization of pitch and duration discrimination. Neuroreport, 16(3), 239–242.CrossRefGoogle ScholarPubMed
Rempel-Clower, N.L., Zola, S.M., Squire, L.R., Amaral, D.G. (1996). Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. The Journal of Neuroscience, 16(16), 5233–5255.CrossRefGoogle ScholarPubMed
Ressel, V., Wilke, M., Lidzba, K., Lutzenberger, W., Krägeloh-Mann, I. (2008). Increases in language lateralization in normal children as observed using magnetoencephalography. Brain and Language, 106, 167–176.CrossRefGoogle ScholarPubMed
Rowland, L.M., Griego, J.A., Spieker, E.A., Cortes, C.R., Holcomb, H.H. (2010). Neural changes associated with relational learning in schizophrenia. Schizophrenia Bulletin, 36, 496–503.CrossRefGoogle ScholarPubMed
Rudy, J.W., Keith, J.R., Georgen, K. (1993). The effect of age on children's learning of problems that require a configural association solution. Developmental Psychobiology, 26, 171–184.CrossRefGoogle ScholarPubMed
Saksida, L.M., Busey, T.J., Buckmaster, C.A., Murray, E.A. (2007). Impairment and facilitation of transverse patterning after lesions of the perirhinal cortex and hippocampus, respectively. Cerebral Cortex, 17, 108–115.CrossRefGoogle ScholarPubMed
Sekihara, K., Nagarajan, S.S., Poeppel, D., Marantz, A., Miyashita, Y. (2001). Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique. IEEE Transactions on Biomedical Engineering, 48(7), 760–771.CrossRefGoogle ScholarPubMed
Sowell, E.R., Delis, D., Stiles, J., Jernigan, T.L. (2001). Improved memory functioning and frontal lobe maturation between childhood and adolescence: A structural MRI study. Journal of the International Neurological Society, 7, 312–322.Google ScholarPubMed
Szaflarski, J.P., Holland, S.K., Schmithorst, V.J., Byars, A.W. (2006). fMRI study of language lateralization in children and adults. Human Brain Mapping, 27, 202–212. doi:10.1002/hbm.20177CrossRefGoogle ScholarPubMed
Tsujii, T., Yamamto, E., Masuda, S., Watanabe, S. (2009). Longitudinal study of spatial working memory development in young children. Neuroreport, 20, 759–763.CrossRefGoogle ScholarPubMed
Utsunomiya, H., Takano, K., Okazaki, M., Mitsudome, A. (1999). Development of the temporal lobe in infants and children: Analysis by MR-based volumetry. AJR American Journal of Neuroradiology, 20, 717–723.Google ScholarPubMed
Victor, M., Agamanolis, D. (1990). Amnesia due to lesions confined to the hippocampus: A clinical-pathologic study. Journal of Cognitive Neuroscience, 2(3), 246–257.CrossRefGoogle Scholar
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence (WASI). San Antonio, TX: Harcourt Assessment.Google Scholar
Zola-Morgan, S., Squire, L.R., Amaral, D.G. (1986). Human amnesia and the medial temporal region: Enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. The Journal of Neuroscience, 6(10), 2950–2967.CrossRefGoogle ScholarPubMed