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Modulation of medial temporal lobe activity in epilepsy patients with hippocampal sclerosis during verbal working memory

Published online by Cambridge University Press:  01 July 2009

PABLO CAMPO ,
FERNANDO MAESTÚ ,
IRENE GARCÍA-MORALES ,
ANTONIO GIL-NAGEL ,
BRYAN STRANGE ,
MANUEL MORALES  and
TOMÁS ORTIZ
PABLO CAMPO*
Affiliation:
Center of Magnetoencephalography Dr. Pérez-Modrego, Complutense University of Madrid, Madrid, Spain
FERNANDO MAESTÚ
Affiliation:
Center of Magnetoencephalography Dr. Pérez-Modrego, Complutense University of Madrid, Madrid, Spain Department of Basic Psychology II (Cognitive Processes), Faculty of Psychology, Complutense University of Madrid, Madrid, Spain
IRENE GARCÍA-MORALES
Affiliation:
Epilepsy Unit, Neurology Department, University Hospital of San Carlos, Madrid, Spain Epilepsy Unit, Neurology Department, Hospital Ruber Internacional, Madrid, Spain
ANTONIO GIL-NAGEL
Affiliation:
Epilepsy Unit, Neurology Department, Hospital Ruber Internacional, Madrid, Spain
BRYAN STRANGE
Affiliation:
Wellcome Department of Imaging Neuroscience, Institute of Neurology, London, United Kingdom
MANUEL MORALES
Affiliation:
Department of Experimental Psychology, University of Seville, Seville, Spain
TOMÁS ORTIZ
Affiliation:
Center of Magnetoencephalography Dr. Pérez-Modrego, Complutense University of Madrid, Madrid, Spain
*
*Correspondence and reprint requests to: Pablo Campo, Centro de Magnetoencefalografía Dr. Pérez Modrego, Pabellón nº 8 Facultad de Medicina, Universidad Complutense de Madrid, 28040 Madrid, Spain. E-mail: pcampo@arrakis.es
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Abstract

It has been traditionally assumed that medial temporal lobe (MTL) is not required for working memory (WM). However, animal lesion and electrophysiological studies and human neuropsychological and neuroimaging studies have provided increasing evidences of a critical involvement of MTL in WM. Based on previous findings, the central aim of this study was to investigate the contribution of the MTL to verbal WM encoding. Here, we used magnetoencephalography (MEG) to compare the patterns of MTL activation of 9 epilepsy patients suffering from left hippocampal sclerosis with those of 10 healthy matched controls while they performed a verbal WM task. MEG recordings allow detailed tracking of the time course of MTL activation. We observed impaired WM performance associated with changes in the dynamics of MTL activity in epilepsy patients. Specifically, whereas patients showed decreased activity in damaged MTL, activity in the contralateral MTL was enhanced, an effect that became significant in the 600- to 700-ms interval after stimulus presentation. These findings strongly support the crucial contribution of MTL to verbal WM encoding and provide compelling evidence for the proposal that MTL contributes to both episodic memory and WM. Whether this pattern is signaling reorganization or a normal use of a damaged structure is discussed. (JINS, 2009, 15, 536–546.)

Keywords

MagnetoencephalographyHippocampusMemoryMemory disordersEpilepsyEpilepsy surgery
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 15 , Issue 4 , July 2009 , pp. 536 - 546
Copyright
Copyright © The International Neuropsychological Society 2009

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References

REFERENCES

Abrahams, S., Morris, R.G., Polkey, C.E., Jarosz, J.M., Cox, T.C., Graves, M., & Pickering, A. (1999). Hippocampal involvement in spatial and working memory: A structural MRI analysis of patients with unilateral mesial temporal lobe sclerosis. Brain and Cognition, 41(1), 39–65.CrossRefGoogle ScholarPubMed
Aine, C.J., Adair, J.C., Knoefel, J.E., Hudson, D., Qualls, C., Kovacevic, S., Woodruff, C.C., Cobb, W., Padilla, D., Lee, R.R., & Stephen, J.M. (2005). Temporal dynamics of age-related differences in auditory incidental verbal learning. Brain Research. Cognitive Brain Research, 24(1), 1–18.Google Scholar
Algarabel, S. (1996). Indices de interés psicolinguístico de 1917 palabras castellanas. Cognitiva, 8, 43–88.Google Scholar
Amaral, D. & Insausti, R. (1990). Hippocampal formation. In Paxinos, G. (Ed.), The human nervous system (pp. 711–755). San Diego, CA: Academic Press.Google Scholar
Axmacher, N., Mormann, F., Fernandez, G., Cohen, M.X., Elger, C.E., & Fell, J. (2007). Sustained neural activity patterns during working memory in the human medial temporal lobe. The Journal of Neuroscience, 27(29), 7807–7816.Google Scholar
Axmacher, N., Mormann, F., Fernandez, G., Elger, C.E., & Fell, J. (2006). Memory formation by neuronal synchronization. Brain Research Review, 52(1), 170–182.Google Scholar
Axmacher, N., Schmitz, D.P., Wagner, T., Elger, C.E., & Fell, J. (2008). Interactions between medial temporal lobe, prefrontal cortex, and inferior temporal regions during visual working memory: A combined intracranial EEG and functional magnetic resonance imaging study. The Journal of Neuroscience, 28(29), 7304–7312.CrossRefGoogle ScholarPubMed
Binder, J.R., Bellgowan, P.S., Hammeke, T.A., Possing, E.T., & Frost, J.A. (2005). A comparison of two FMRI protocols for eliciting hippocampal activation. Epilepsia, 46(7), 1061–1070.CrossRefGoogle ScholarPubMed
Breier, J.I., Simos, P.G., Zouridakis, G., & Papanicolaou, A.C. (2000). Lateralization of activity associated with language function using magnetoencephalography: A reliability study. Journal of Clinical Neurophysiology, 17(5), 503–510.Google Scholar
Cabeza, R., Daselaar, S.M., Dolcos, F., Prince, S.E., Budde, M., & Nyberg, L. (2004). Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cerebral Cortex, 14(4), 364–375.CrossRefGoogle ScholarPubMed
Cabeza, R., Dolcos, F., Graham, R., & Nyberg, L. (2002). Similarities and differences in the neural correlates of episodic memory retrieval and working memory. NeuroImage, 16(2), 317–330.CrossRefGoogle ScholarPubMed
Campo, P., Maestu, F., Capilla, A., Fernandez, S., Fernandez, A., & Ortiz, T. (2005a). Activity in human medial temporal lobe associated with encoding process in spatial working memory revealed by magnetoencephalography. The European Journal of Neuroscience, 21(6), 1741–1748.Google Scholar
Campo, P., Maestu, F., Capilla, A., Morales, M., Fernandez, S., del Rio, D., & Ortiz, T. (2008). Temporal dynamics of parietal activity during word-location binding. Neuropsychology, 22(1), 85–99.Google Scholar
Campo, P., Maestu, F., Ortiz, T., Capilla, A., Fernandez, S., & Fernandez, A. (2005b). Is medial temporal lobe activation specific for encoding long-term memories? NeuroImage, 25(1), 34–42.Google Scholar
Castillo, E.M., Simos, P.G., Davis, R.N., Breier, J., Fitzgerald, M.E., & Papanicolaou, A. (2003). Temporal dynamics of medial temporal lobe activation during encoding and recognition. A magnetoencephalography study. Revista Española de Neuropsicología, 5(2), 99–120.Google Scholar
Castillo, E.M., Simos, P.G., Davis, R.N., Breier, J., Fitzgerald, M.E., & Papanicolaou, A.C. (2001). Levels of word processing and incidental memory: Dissociable mechanisms in the temporal lobe. Neuroreport, 12(16), 3561–3566.CrossRefGoogle ScholarPubMed
Cave, C.B. & Squire, L.R. (1992). Intact verbal and nonverbal short-term memory following damage to the human hippocampus. Hippocampus, 2(2), 151–163.Google Scholar
Chugani, H.T., Muller, R.A., & Chugani, D.C. (1996). Functional brain reorganization in children. Brain & Development, 18(5), 347–356.Google Scholar
Cowan, N. (1995). Attention and memory, and integrated framework. New York: Oxford University Press.Google Scholar
Cowan, N. (1999). An embedded-process model of working memory. In Miyake, A. & Shah, P., (Eds.), Models of working memory (pp. 62–101) Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Davachi, L. & Goldman-Rakic, P.S. (2001). Primate rhinal cortex participates in both visual recognition and working memory tasks: Functional mapping with 2-DG. Journal of Neurophysiology, 85(6), 2590–2601.CrossRefGoogle ScholarPubMed
Davachi, L. & Wagner, A.D. (2002). Hippocampal contributions to episodic encoding: Insights from relational and item-based learning. Journal of Neurophysiology, 88(2), 982–990.CrossRefGoogle ScholarPubMed
Dupont, S., Van de Moortele, P.F., Samson, S., Hasboun, D., Poline, J.B., Adam, C., Lehericy, S., Le Bihan, D., Samson, Y., & Baulac, M. (2000). Episodic memory in left temporal lobe epilepsy: A functional MRI study. Brain, 123(Pt 8), 1722–1732.CrossRefGoogle ScholarPubMed
Eichenbaum, H. (1997). Declarative memory: Insights from cognitive neurobiology. Annual Review of Psychology, 48, 547–572.CrossRefGoogle ScholarPubMed
Fell, J., Klaver, P., Elfadil, H., Schaller, C., Elger, C.E., & Fernandez, G. (2003). Rhinal-hippocampal theta coherence during declarative memory formation: Interaction with gamma synchronization? The European Journal of Neuroscience, 17(5), 1082–1088.CrossRefGoogle ScholarPubMed
Fell, J., Klaver, P., Elger, C.E., & Fernandez, G. (2002). The interaction of rhinal cortex and hippocampus in human declarative memory formation. Review in the Neurosciences, 13(4), 299–312.CrossRefGoogle ScholarPubMed
Fernandez, G., Effern, A., Grunwald, T., Pezer, N., Lehnertz, K., Dumpelmann, M., Van Roost, D., & Elger, C.E. (1999). Real-time tracking of memory formation in the human rhinal cortex and hippocampus. Science, 285(5433), 1582–1585.Google Scholar
Fernandez, G., Klaver, P., Fell, J., Grunwald, T., & Elger, C.E. (2002). Human declarative memory formation: Segregating rhinal and hippocampal contributions. Hippocampus, 12(4), 514–519.Google Scholar
Fernandez, G. & Tendolkar, I. (2001). Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: Human declarative memory formation at the system level. Brain Research Bulletin, 55(1), 1–9.CrossRefGoogle ScholarPubMed
Fernandez, G., Weyerts, H., Schrader-Bolsche, M., Tendolkar, I., Smid, H.G., Tempelmann, C., Hinrichs, H., Scheich, H., Elger, C.E., Mangun, G.R., & Heinze, H.J. (1998). Successful verbal encoding into episodic memory engages the posterior hippocampus: A parametrically analyzed functional magnetic resonance imaging study. The Journal of Neuroscience, 18(5), 1841–1847.Google Scholar
Fontoura, D.R., Branco Dde, M., Anes, M., Costa, J.C., & Portuguez, M.W. (2008). Language brain dominance in patients with refractory temporal lobe epilepsy: A comparative study between functional magnetic resonance imaging and dichotic listening test. Arquivos de Neuro-psiquiatria, 66(1), 34–39.Google Scholar
Gabrieli, J.D. (1998). Cognitive neuroscience of human memory. Annual Review of Psychology, 49, 87–115.Google Scholar
Gazzaley, A., Rissman, J., & Desposito, M. (2004). Functional connectivity during working memory maintenance. Cognitive, Affective & Behavioral Neuroscience, 4(4), 580–599.CrossRefGoogle ScholarPubMed
Giovagnoli, A.R., Erbetta, A., Villani, F., & Avanzini, G. (2005). Semantic memory in partial epilepsy: Verbal and non-verbal deficits and neuroanatomical relationships. Neuropsychologia, 43(10), 1482–1492.Google Scholar
Glabus, M.F., Horwitz, B., Holt, J.L., Kohn, P.D., Gerton, B.K., Callicott, J.H., Meyer-Lindenberg, A., & Berman, K.F. (2003). Interindividual differences in functional interactions among prefrontal, parietal and parahippocampal regions during working memory. Cerebral Cortex, 13(12), 1352–1361.CrossRefGoogle ScholarPubMed
Golby, A.J., Poldrack, R.A., Illes, J., Chen, D., Desmond, J.E., & Gabrieli, J.D. (2002). Memory lateralization in medial temporal lobe epilepsy assessed by functional MRI. Epilepsia, 43(8), 855–863.CrossRefGoogle ScholarPubMed
Gonsalves, B.D., Kahn, I., Curran, T., Norman, K.A., & Wagner, A.D. (2005). Memory strength and repetition suppression: Multimodal imaging of, medial temporal cortical contributions to recognition. Neuron, 47, 751–761.Google Scholar
Grippo, A., Pelosi, L., Mehta, V., & Blumhardt, L.D. (1996). Working memory in temporal lobe epilepsy: An event-related potential study. Electroencephalography and Clinical Neurophysiology, 99(3), 200–213.CrossRefGoogle ScholarPubMed
Haettig, H., Schepler, P., Lehmann, T.N., & Meencke, H.J. (2004). Short-term memory outcome after temporal lobe surgery for epilepsy: A 12 month follow up. Paper presented at the Human Brain Mapping, Budapest, June, 12–16.Google Scholar
Hanlon, F.M., Weisend, M.P., Huang, M., Lee, R.R., Moses, S.N., Paulson, K.M., Thoma, R.J., Miller, G.A., & Canive, J.M. (2003). A non-invasive method for observing hippocampal function. Neuroreport, 14(15), 1957–1960.CrossRefGoogle ScholarPubMed
Haxby, J.V., Ungerleider, L.G., Horwitz, B., Rapoport, S.I., & Grady, C.L. (1995). Hemispheric differences in neural systems for face working memory: A PET-rCBF study. Human Brain Mapping, 3, 68–82.CrossRefGoogle Scholar
Helenius, P., Salmelin, R., Service, E., & Connolly, J.F. (1998). Distinct time courses of word and context comprehension in the left temporal cortex. Brain, 121(Pt 6), 1133–1142.Google Scholar
Henke, K., Treyer, V., Weber, B., Nitsch, R.M., Hock, C., Wieser, H.G., & Buck, A. (2003). Functional neuroimaging predicts individual memory outcome after amygdalohippocampectomy. Neuroreport, 14(9), 1197–1202.CrossRefGoogle ScholarPubMed
Holscher, C. & Rolls, E.T. (2002). Perirhinal cortex neuronal activity is actively related to working memory in the macaque. Neural Plasticity, 9(1), 41–51.CrossRefGoogle ScholarPubMed
Jones-Gotman, M., Zatorre, R.J., Olivier, A., Andermann, F., Cendes, F., Staunton, H., McMackin, D., Siegel, A.M., & Wieser, H.G. (1997). Learning and retention of words and designs following excision from medial or lateral temporal-lobe structures. Neuropsychologia, 35(7), 963–973.CrossRefGoogle ScholarPubMed
Kapur, S., Craik, F.I., Tulving, E., Wilson, A.A., Houle, S., & Brown, G.M. (1994). Neuroanatomical correlates of encoding in episodic memory: Levels of processing effect. Proceedings of the National Academy of Sciences of the United States of America, 91(6), 2008–2011.Google Scholar
Karlsgodt, K.H., Shirinyan, D., van Erp, T.G., Cohen, M.S., & Cannon, T.D. (2005). Hippocampal activations during encoding and retrieval in a verbal working memory paradigm. NeuroImage, 25(4), 1224–1231.Google Scholar
Krauss, G.L., Summerfield, M., Brandt, J., Breiter, S., & Ruchkin, D. (1997). Mesial temporal spikes interfere with working memory. Neurology, 49(4), 975–980.Google Scholar
Lancelot, C., Samson, S., Ahad, P., & Baulac, M. (2003). Effect of unilateral temporal lobe resection on short-term memory for auditory object and sound location. Annals of the New York Academy of Sciences, 999, 377–380.CrossRefGoogle ScholarPubMed
Lee, A.C., Buckley, M.J., Gaffan, D., Emery, T., Hodges, J.R., & Graham, K.S. (2006). Differentiating the roles of the hippocampus and perirhinal cortex in processes beyond long-term declarative memory: A double dissociation in dementia. The Journal of Neuroscience, 26(19), 5198–5203.Google Scholar
Lepage, M., Habib, R., Cormier, H., Houle, S., & McIntosh, A.R. (2000). Neural correlates of semantic associative encoding in episodic memory. Brain Research. Cognitive Brain Research, 9(3), 271–280.CrossRefGoogle ScholarPubMed
Levy, D.A., Bayley, P.J., & Squire, L.R. (2004). The anatomy of semantic knowledge: Medial vs. lateral temporal lobe. Proceedings of the National Academy of Sciences of the United States of America, 101(17), 6710–6715.Google Scholar
Loring, D.W., Strauss, E., Hermann, B.P., Perrine, K., Trenerry, M.R., Barr, W.B., Westerveld, M., Chelune, G.J., Lee, G.P., & Meador, K.J. (1999). Effects of anomalous language representation on neuropsychological performance in temporal lobe epilepsy. Neurology, 53(2), 260–264.CrossRefGoogle ScholarPubMed
Maestu, F., Arrazola, J., Fernandez, A., Simos, P.G., Amo, C., Gil-Gregorio, P., Fernandez, S., Papanicolaou, A., & Ortiz, T. (2003). Do cognitive patterns of brain magnetic activity correlate with hippocampal atrophy in Alzheimer’s disease? Journal of Neurology, Neurosurgery, and Psychiatry, 74(2), 208–212.Google Scholar
Maestu, F., Campo, P., Gil-Gregorio, P., Fernandez, S., Fernandez, A., & Ortiz, T. (2006). Medial temporal lobe neuromagnetic hypoactivation and risk for developing cognitive decline in elderly population: A 2-year follow-up study. Neurobiology of Aging, 27(1), 32–37.Google Scholar
Maestu, F., Fernandez, A., Simos, P.G., Lopez-Ibor, M.I., Campo, P., Criado, J., Rodriguez-Palancas, A., Ferre, F., Amo, C., & Ortiz, T. (2004). Profiles of brain magnetic activity during a memory task in patients with Alzheimer’s disease and in non-demented elderly subjects, with or without depression. Journal of Neurology, Neurosurgery, and Psychiatry, 75(8), 1160–1162.Google Scholar
Maestu, F., Garcia-Segura, J., Ortiz, T., Montoya, J., Fernandez, A., Gil-Gregorio, P., Campo, P., Fernandez, S., Viano, J., & Portera, A. (2005). Evidence of biochemical and biomagnetic interactions in Alzheimer’s disease: An MEG and MR spectroscopy study. Dementia and Geriatric Cognitive Disorders, 20(2–3), 145–152.Google Scholar
Maestu, F., Ortiz, T., Fernandez, A., Amo, C., Martin, P., Fernandez, S., & Sola, R.G. (2002). Spanish language mapping using MEG: A validation study. NeuroImage, 17(3), 1579–1586.CrossRefGoogle ScholarPubMed
Manoach, D.S., Greve, D.N., Lindgren, K.A., & Dale, A.M. (2003). Identifying regional activity associated with temporally separated components of working memory using event-related functional MRI. NeuroImage, 20(3), 1670–1684.Google Scholar
Martin, A. (1999). Automatic activation of the medial temporal lobe during encoding: Lateralized influences of meaning and novelty. Hippocampus, 9(1), 62–70.Google Scholar
Miyake, A. & Shah, P. (1999). Models of working memory. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Monk, C.S., Zhuang, J., Curtis, W.J., Ofenloch, I.T., Tottenham, N., Nelson, C.A., & Hu, X. (2002). Human hippocampal activation in the delayed matching- and nonmatching-to-sample memory tasks: An event-related functional MRI approach. Behavioral Neuroscience, 116(4), 716–721.CrossRefGoogle ScholarPubMed
Moré, J. (1977). The Levenberg-Marquardt algorithm: Implementation and theory. In Watson, G. (Ed.), Numerical analysis (pp. 105–116). New York: Springer Verlag.Google Scholar
Mormann, F., Fernandez, G., Klaver, P., Weber, B., Elger, C.E., & Fell, J. (2007). Declarative memory formation in hippocampal sclerosis: An intracranial event-related potentials study. Neuroreport, 18(4), 317–321.Google Scholar
Nichols, E.A., Kao, Y.C., Verfaellie, M., & Gabrieli, J.D. (2006). Working memory and long-term memory for faces: Evidence from fMRI and global amnesia for involvement of the medial temporal lobes. Hippocampus, 16(7), 604–616.Google Scholar
Oldfield, R.C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97–113.CrossRefGoogle ScholarPubMed
Olson, I.R., Moore, K.S., Stark, M., & Chatterjee, A. (2006). Visual working memory is impaired when the medial temporal lobe is damaged. Journal of Cognitive Neuroscience, 18(7), 1087–1097.Google Scholar
Owen, A.M., Morris, R.G., Sahakian, B.J., Polkey, C.E., & Robbins, T.W. (1996). Double dissociations of memory and executive functions in working memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Brain, 119(Pt 5), 1597–1615.Google Scholar
Paller, K.A. & Wagner, A.D. (2002). Observing the transformation of experience into memory. Trends in Neurosciences, 6, 93–102.Google Scholar
Papanicolaou, A.C., Simos, P.G., Breier, J.I., Zouridakis, G., Wilmore, L.J., Wheless, J.W., Constantinou, J.C., Gormley, W., & Maggio, W.W. (1999). Magnetoencephalographic mapping of the language specific cortex. Journal of Neurosurgery, 90(1), 85–93.Google Scholar
Papanicolaou, A.C., Simos, P.G., Castillo, E.M., Breier, J.I., Katz, J.S., & Wright, A.A. (2002). The hippocampus and memory of verbal and pictorial material. Learn & Memory (Cold Spring Harbor, N.Y.), 9(3), 99–104.Google Scholar
Papanicolaou, A.C., Simos, P.G., Castillo, E.M., Breier, J.I., Sarkari, S., Pataraia, E., Billingsley, R.L., Buchanan, S., Wheless, J., Maggio, V., & Maggio, W.W. (2004). Magnetocephalography: A noninvasive alternative to the Wada procedure. Journal of Neurosurgery, 100(5), 867–876.Google Scholar
Petersson, K.M., Gisselgard, J., Gretzer, M., & Ingvar, M. (2006). Interaction between a verbal working memory network and the medial temporal lobe. NeuroImage, 33(4), 1207–1217.Google Scholar
Petrides, M. & Milner, B. (1982). Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia, 20(3), 249–262.Google Scholar
Piekema, C., Kessels, R.P., Mars, R.B., Petersson, K.M., & Fernandez, G. (2006). The right hippocampus participates in short-term memory maintenance of object-location associations. NeuroImage, 33(1), 374–382.Google Scholar
Powell, H.W., Koepp, M.J., Richardson, M.P., Symms, M.R., Thompson, P.J., & Duncan, J.S. (2004). The application of functional MRI of memory in temporal lobe epilepsy: A clinical review. Epilepsia, 45(7), 855–863.Google Scholar
Powell, H.W., Richardson, M.P., Symms, M.R., Boulby, P.A., Thompson, P.J., Duncan, J.S., & Koepp, M.J. (2007). Reorganization of verbal and nonverbal memory in temporal lobe epilepsy due to unilateral hippocampal sclerosis. Epilepsia, 48(8), 1512–1525.CrossRefGoogle ScholarPubMed
Rabin, M.L., Narayan, V.M., Kimberg, D.Y., Casasanto, D.J., Glosser, G., Tracy, J.I., French, J.A., Sperling, M.R., & Detre, J.A. (2004). Functional MRI predicts post-surgical memory following temporal lobectomy. Brain, 127(Pt 10), 2286–2298.Google Scholar
Ranganath, C. & Blumenfeld, R.S. (2005). Doubts about double dissociations between short- and long-term memory. Trends in Cognitive Sciences, 9(8), 374–380.CrossRefGoogle ScholarPubMed
Ranganath, C., DeGutis, J., & D’Esposito, M. (2004). Category-specific modulation of inferior temporal activity during working memory encoding and maintenance. Cognitive Brain Research, 20, 37–45.Google Scholar
Ranganath, C. & D’Esposito, M. (2001). Medial temporal lobe activity associated with active maintenance of novel information. Neuron, 31(5), 865–873.Google Scholar
Rausch, R. & Babb, T.L. (1993). Hippocampal neuron loss and memory scores before and after temporal lobe surgery for epilepsy. Archives of Neurology, 50(8), 812–817.Google Scholar
Ribbler, A. & Rausch, R. (1990). Performance of patients with unilateral temporal lobectomy on selective reminding procedures using either related or unrelated words. Cortex, 26(4), 575–584.CrossRefGoogle ScholarPubMed
Richardson, M.P., Strange, B.A., Duncan, J.S., & Dolan, R.J. (2003). Preserved verbal memory function in left medial temporal pathology involves reorganisation of function to right medial temporal lobe. NeuroImage, 20(Suppl 1), S112–119.Google Scholar
Richardson, M.P., Strange, B.A., Duncan, J.S., & Dolan, R.J. (2006). Memory fMRI in left hippocampal sclerosis: Optimizing the approach to predicting postsurgical memory. Neurology, 66(5), 699–705.Google Scholar
Riggs, L., Moses, S.N., Bardouille, T., Herdman, A.T., Ross, B., & Ryan, J.D. (2009). A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography. NeuroImage, 45(2), 627–642.Google Scholar
Rorden, C. & Brett, M. (2000). Stereotaxic display of brain lesions. Behavioral neurology, 12, 191–200.CrossRefGoogle ScholarPubMed
Sarvas, J. (1987). Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. Physics in Medicine and Biology, 32(1), 11–22.Google Scholar
Sass, K.J., Buchanan, C.P., Kraemer, S., Westerveld, M., Kim, J.H., & Spencer, D.D. (1995). Verbal memory impairment resulting from hippocampal neuron loss among epileptic patients with structural lesions. Neurology, 45(12), 2154–2158.CrossRefGoogle ScholarPubMed
Sawrie, S.M., Martin, R.C., Knowlton, R., Faught, E., Gilliam, F., & Kuzniecky, R. (2001). Relationships among hippocampal volumetry, proton magnetic resonance spectroscopy, and verbal memory in temporal lobe epilepsy. Epilepsia, 42(11), 1403–1407.Google Scholar
Schon, K., Hasselmo, M.E., Lopresti, M.L., Tricarico, M.D., & Stern, C.E. (2004). Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding: A functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task. The Journal of Neuroscience, 24(49), 11088–11097.Google Scholar
Springer, J.A., Binder, J.R., Hammeke, T.A., Swanson, S.J., Frost, J.A., Bellgowan, P.S., Brewer, C.C., Perry, H.M., Morris, G.L., & Mueller, W.M. (1999). Language dominance in neurologically normal and epilepsy subjects: A functional MRI study. Brain, 122(Pt 11), 2033–2046.Google Scholar
Squire, L.R., Stark, C.E., & Clark, R.E. (2004). The medial temporal lobe. Annual Review of Neuroscience, 27, 279–306.CrossRefGoogle ScholarPubMed
Staresina, B.P., Bauer, H., Deecke, L., & Walla, P. (2005). Neurocognitive correlates of incidental verbal memory encoding: A magnetoencephalographic (MEG) study. NeuroImage, 25(2), 430–443.CrossRefGoogle ScholarPubMed
Stern, C.E., Sherman, S.J., Kirchhoff, B.A., & Hasselmo, M.E. (2001). Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli. Hippocampus, 11(4), 337–346.Google Scholar
Suzuki, W.A., Miller, E.K., & Desimone, R. (1997). Object and place memory in the macaque entorhinal cortex. Journal of Neurophysiology, 78(2), 1062–1081.Google Scholar
Tarkiainen, A., Liljestrom, M., Seppa, M., & Salmelin, R. (2003). The 3D topography of MEG source localization accuracy: Effects of conductor model and noise. Clinical Neurophysiology, 114(10), 1977–1992.Google Scholar
Tendolkar, I., Rugg, M., Fell, J., Vogt, H., Scholz, M., Hinrichs, H., & Heinze, H.J. (2000). A magnetoencephalographic study of brain activity related to recognition memory in healthy young human subjects. Neuroscience Letters, 280(1), 69–72.CrossRefGoogle ScholarPubMed
Tesche, C.D. & Karhu, J. (2000). Theta oscillations index human hippocampal activation during a working memory task. Proceedings of the National Academy of Sciences of the United States of America, 97(2), 919–924.Google Scholar
Thom, M., Zhou, J., Martinian, L., & Sisodiya, S. (2005). Quantitative post-mortem study of the hippocampus in chronic epilepsy: Seizures do not inevitably cause neuronal loss. Brain, 128(Pt 6), 1344–1357.Google Scholar
Trenerry, M.R., Jack, C.R. Jr., Ivnik, R.J.,, Sharbrough, F.W., Cascino, G.D., Hirschorn, K.A., Marsh, W.R., Kelly, P.J., & Meyer, F.B. (1993). MRI hippocampal volumes and memory function before and after temporal lobectomy. Neurology, 43(9), 1800–1805.Google Scholar
Ver Hoef, L.W., Sawrie, S., Killen, J., & Knowlton, R.C. (2008). Left mesial temporal sclerosis and verbal memory: A magnetoencephalography study. Journal of Clinical Neurophysiology, 25(1), 1–6.Google Scholar
Wagner, D.D., Sziklas, V., Garver, K.E., & Jones-Gotman, M. (2008). Material-specific lateralization of working memory in the medial temporal lobe. Neuropsychologia, 47(1), 112–122.Google Scholar
Young, B.J., Otto, T., Fox, G.D., & Eichenbaum, H. (1997). Memory representation within the parahippocampal region. The Journal of Neuroscience, 17(13), 5183–5195.Google Scholar