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Age Differences in Hippocampus-Cortex Connectivity during True and False Memory Retrieval

Published online by Cambridge University Press:  23 September 2013

Pedro M. Paz-Alonso ,
Pamela Gallego  and
Simona Ghetti
Pedro M. Paz-Alonso*
Affiliation:
Basque Center on Cognition, Brain and Language (BCBL), Donostia-San Sebastián, Gipuzkoa, Spain Center for Mind and Brain, University of California, Davis, California
Pamela Gallego
Affiliation:
Center for Mind and Brain, University of California, Davis, California
Simona Ghetti
Affiliation:
Center for Mind and Brain, University of California, Davis, California Department of Psychology, University of California, Davis, California
*
Correspondence and reprint requests to: Pedro M. Paz-Alonso, BCBL, Paseo Mikeletegi 69, 2, Donostia-San Sebastián, 20009, Gipuzkoa, Spain. E-mail: [email protected]
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Abstract

The present functional magnetic resonance imaging (fMRI) study investigated developmental differences in functional connectivity associated with true and false memory retrieval. A sample of 8- to 9-year-olds and adults (N = 31) was assessed with the Deese/Roediger-McDermott (DRM) paradigm, known to induce high levels of false recognition of lures that are semantically associated with studied items. The strength of semantic association among list items was manipulated. Relative to children, adults correctly recognized more studied items and falsely recognized more critical lures. High-association lists resulted in higher recognition of both studied items and critical lures. Functional connectivity analysis revealed that, overall, true recognition was supported by coupling within two hippocampal-temporal and fronto-parietal set of regions; in contrast, coupling among more distributed hippocampal-temporal-parietal-frontal regions was observed during false recognition. Critically, adults, compared to children, exhibited stronger hippocampal/parietal coupling and stronger hippocampal/dorsolateral prefrontal cortex (PFC) coupling for veridical recognition of high-associative strength items. In contrast, children, compared to adults, exhibited stronger hippocampus/ventrolateral PFC coupling and stronger bilateral middle-temporal gyrus/ventrolateral PFC coupling for high-associative strength critical lures. Our results underscored a role for the anterior hippocampus in true and false recognition, showing different functional patterns as a function of age and association strength. (JINS, 2013, 19, 1–11)

Keywords

Episodic memoryRecognitionHippocampusMiddle-temporal gyrusPrefrontal cortexFunctional connectivity
Type
Symposia
Information
Journal of the International Neuropsychological Society , Volume 19 , Issue 10 , November 2013 , pp. 1031 - 1041
Copyright
Copyright © The International Neuropsychological Society 2013 

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References

Abe, N., Okuda, J., Suzuki, M., Sasaki, H., Matsuda, T., Mori, E., Fujii, T. (2008). Neural correlates of true memory, false memory, and deception. Cerebral Cortex, 18, 2811–2819.CrossRefGoogle ScholarPubMed
Achenbach, T.M. (1991). Manual for the child behavior checklist/4–18 and 1991 profile. Burlington, VT: University of Vermont.Google Scholar
Atkins, A.S., Reuter-Lorenz, P.A. (2011). Neural mechanisms of semantic interference and false recognition in short-term memory. Neuroimage, 56, 1726–1734.CrossRefGoogle ScholarPubMed
Badre, D., Wagner, A.D. (2007). Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia, 45, 2883–2901.CrossRefGoogle ScholarPubMed
Blumenfeld, H.K., Booth, J.R., Burman, D.D. (2006). Differential prefrontal-temporal neural correlates of semantic processing in children. Brain and Language, 99, 226–235.CrossRefGoogle ScholarPubMed
Brainerd, C.J., Reyna, V.F., Ceci, S.J. (2008). Developmental reversals in false memory: A review of data and theory. Psychological Bulletin, 134, 343–382.CrossRefGoogle ScholarPubMed
Brett, M., Anton, J.-L., Valabregue, R., Poline, J.B. (2002). Region of interest analysis using an SPM toolbox. In: 8th International Conference on Functional Mapping of the Human Brain. Sendai, Japan.Google Scholar
Burgund, E.D., Kang, H.C., Kelly, J.E., Buckner, R.L., Snyder, A.Z., Petersen, S.E., Schlaggar, B.L. (2002). The feasibility of a common stereotactic space for children and adults in fMRI studies of development. Neuroimage, 17, 184–200.CrossRefGoogle ScholarPubMed
Cabeza, R. (2008). Role of parietal regions in episodic memory retrieval: The dual attentional processes hypothesis. Neuropsychologia, 46, 1813–1827.CrossRefGoogle ScholarPubMed
Cabeza, R., Ciaramelli, E., Olson, I.R., Moscovith, M. (2008). Parietal cortex and episodic memory: An attentional account. Nature Review Neuroscience, 9, 613–625.CrossRefGoogle ScholarPubMed
Cabeza, R., Rao, S.M., Wagner, A.D., Mayer, A.R., Schacter, D.L. (2001). Can medial temporal lobe regions distinguish true from false? An event-related functional MRI study of veridical and illusory recognition memory. Proceeding of the National Academy of Sciences of the United States of America, 98, 4805–4810.CrossRefGoogle ScholarPubMed
Carneiro, P., Alburquerque, P., Fernandez, A., Esteves, F. (2007). Analyzing false memories in children with associative lists specific for their age. Child Development, 78, 1171–1185.CrossRefGoogle ScholarPubMed
Chadwick, M.J., Hassabis, D., Weiskopf, N., Maguire, E. (2010). Decoding individual episodic memory traces in the human hippocampus. Current Biology, 20, 544–547.CrossRefGoogle ScholarPubMed
Chou, T.L., Booth, J.R., Burman, D.D., Bitan, T., Bigio, J.D., Lu, D., Cone, N.E. (2006). Developmental changes in the neural correlates of semantic processing. Neuroimage, 29, 1141–1149.CrossRefGoogle ScholarPubMed
Cocosco, C.A., Kollokian, V., Kwan, R.K.-S., Evans, A.C. (1997). BrainWeb: Online interface to a 3D MRI simulated brain database. Neuroimage, 5, S425.Google Scholar
Del Prete, F., Mirandola, C., Cornoldi, C., Ghetti, S. (in press). Paradoxical effects of warning in the production of children's false memories. Journal of Cognition and Development.Google Scholar
DeMaster, D., Ghetti, S. (2013). Developmental differences in hippocampal and cortical contributions to episodic retrieval. Cortex, 49, 1482–1493.CrossRefGoogle ScholarPubMed
DeMaster, D.M., Pathman, T., Lee, J., Ghetti, S. (2013). Structural development of the hippocampus and episodic memory: Developmental differences along the anterior/posterior axis. Cerebral Cortex [Epub ahead of print].Google ScholarPubMed
Dennis, N.A., Bowman, C.R., Vandekar, S.N. (2012). True and phantom recollection: An fMRI investigation of similar and distinct neural correlates and connectivity. Neuroimage, 59, 2982–2993.CrossRefGoogle ScholarPubMed
Dennis, N.A., Kim, H., Cabeza, R. (2008). Age-related differences in brain activity during true and false memory retrieval. Journal of Cognitive Neuroscience, 20, 1390–1402.CrossRefGoogle ScholarPubMed
Diana, R.A., Yonelinas, A.P., Ranganath, C. (2007). Imaging recollection and familiarity in the medial temporal lobe: A three-component model. Trends in Cognitive Science, 11, 379–386.CrossRefGoogle ScholarPubMed
Dobbins, I.G., Simons, J.S., Schacter, D.L. (2004). fMRI evidence for separable and lateralized prefrontal memory monitoring processes. Journal of Cognitive Neuroscience, 16, 908–920.CrossRefGoogle ScholarPubMed
Donaldson, D.I., Wheeler, M.E., Petersen, S.E. (2010). Remember the source: Dissociating frontal and parietal contributions to episodic memory. Journal of Cognitive Neuroscience, 22, 377–391.CrossRefGoogle ScholarPubMed
Eichenbaum, H., Yonelinas, A.R., Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annual Review Neuroscience, 30, 123–152.CrossRefGoogle ScholarPubMed
Gallo, D.A. (2010). False memories and fantastic beliefs: 15 years of the DRM illusion. Memory & Cognition, 38, 833–848.CrossRefGoogle ScholarPubMed
Ghetti, S., Angelini, L. (2008). The development of recollection and familiarity in childhood and adolescence: Evidence from the dual-process signal detection model. Child Development, 79, 339–358.CrossRefGoogle ScholarPubMed
Ghetti, S., DeMaster, D.M., Yonelinas, A.P., Bunge, S.A. (2010). Developmental differences in medial temporal lobe function during memory encoding. Journal of Neuroscience, 30, 9548–9556.CrossRefGoogle ScholarPubMed
Ghetti, S., Qin, J., Goodman, G.S. (2002). False memories in children and adults: Age, istinctiveness, and subjective experience. Developmental Psychology, 38, 705–718.CrossRefGoogle ScholarPubMed
Gogtay, N., Nugent, T.F., Herman, D.H., Ordonez, A., Greenstein, D., Hayashi, K.M., Thompson, P.M. (2006). Dynamic mapping of normal human hippocampal development. Hippocampus, 16, 664–672.CrossRefGoogle ScholarPubMed
Henson, R.N., Gagnepain, P. (2010). Predictive, interactive multiple memory systems. Hippocampus, 20, 1315–1326.CrossRefGoogle ScholarPubMed
Howe, M.L. (2005). Children (but not adults) can inhibit false memories. Psychological Science, 16, 927–931.CrossRefGoogle ScholarPubMed
Howe, M.L., Cicchetti, D., Toth, S.L., Cerrito, B.M. (2004). True and false memories in maltreated children. Child Development, 75, 1402–1417.CrossRefGoogle ScholarPubMed
Howe, M.L., Wimmer, M.C., Blease, K. (2009). The role of associative strength in children's false memory illusions. Memory, 17, 8–16.CrossRefGoogle ScholarPubMed
Kahn, I., Andrews-Hanna, J.R., Vincent, J.L., Snyder, A.Z., Buckner, R.L. (2008). Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. Journal of Neurophysiology, 100, 129–139.CrossRefGoogle ScholarPubMed
Kang, H.C., Burgund, E.D., Lugar, H.M., Petersen, S.E., Schlaggar, B.L. (2003). Comparison of functional activation foci in children and adults using a common stereotactic space. Neuroimage, 19, 16–28.CrossRefGoogle ScholarPubMed
Kim, H., Cabeza, R. (2007). Differential contributions of prefrontal, medial temporal, and sensory-perceptual regions to true and false memory formation. Cerebral Cortex, 17, 2143–2150.CrossRefGoogle ScholarPubMed
Konishi, S., Wheeler, M.E., Donaldson, D.I., Buckner, R.L. (2000). Neural correlates of episodic retrieval success. Neuroimage, 12, 276–286.CrossRefGoogle ScholarPubMed
Lebel, C., Beaulieu, C. (2011). Longitudinal development of human brain wiring continues from childhood into adulthood. Journal of Neuroscience, 31, 10937–10947.CrossRefGoogle ScholarPubMed
Loftus, E.F., Pickrell, J.E. (1995). The formation of false memories. Psychiatric Annals, 25, 720–725.CrossRefGoogle Scholar
Maril, A., Davis, P.E., Koo, J.J., Reggev, N., Zuckerman, M., Ehrenfeld, L., Rivkin, M.J. (2010). Developmental fMRI study of episodic verbal memory encoding in children. Neurology, 75, 2110–2116.CrossRefGoogle ScholarPubMed
McDermott, K.B., Jones, T.C., Petersen, S.E., Lageman, S.K., Roediger, H.L. (2000). Retrieval success is accompanied by enhanced activation in anterior prefrontal cortex during recognition memory: An event-related fMRI study. Journal of Cognitive Neuroscience, 12, 965–976.CrossRefGoogle ScholarPubMed
McDermott, K.B., Roediger, H.L. (1998). Attempting to avoid illusory memories: Robust false recognition of associates persists under conditions of explicit warnings and immediate testing. Journal of Memory and Language, 39, 508–520.CrossRefGoogle Scholar
Menon, V., Boyett-Anderson, J.M., Reiss, A.L. (2005). Maturation of medial temporal lobe response and connectivity during memory encoding. Brain Research: Cognitive Brain Research, 25, 379–385.Google ScholarPubMed
Nolde, S.F., Johnson, M.K., D'Esposito, M. (1998). Left prefrontal activation during episodic remembering: An event-related fMRI study. Neuroreport, 9, 3509–3514.CrossRefGoogle ScholarPubMed
Ofen, N., Chai, X.J., Schuil, K.D.I., Whitfield-Gabrieli, S., Gabrieli, J.D. (2012). The development of brain systems associated with successful memory retrieval of scenes. Journal of Neuroscience, 32, 10012–10020.CrossRefGoogle ScholarPubMed
Okado, Y., Stark, C. (2003). Neural processing associated with true and false memory retrieval. Cognitive Affective Behavioral Neuroscience, 3, 323–334.CrossRefGoogle ScholarPubMed
Patterson, K., Nestor, P.J., Rogers, T.T. (2007). Where do you know what you know? The representation of semantic knowledge in the human brain. Nature Review Neuroscience, 12, 976–987.CrossRefGoogle Scholar
Paz-Alonso, P.M., Bunge, S.A., Anderson, M.C., Ghetti, S. (2013). Strengthening of coupling within a mnemonic control network differentiates those who can and cannot suppress memory retrieval. Journal of Neuroscience, 33, 5017–5026.CrossRefGoogle Scholar
Paz-Alonso, P.M., Ghetti, S., Donohue, S.E., Goodman, G.S., Bunge, S.A. (2008). Neurodevelopmental correlates of true and false recognition. Cerebral Cortex, 18, 2208–2216.CrossRefGoogle ScholarPubMed
Paz-Alonso, P.M., Ghetti, S., Ramsay, I., Solomon, M., Yoon, J., Carter, C.S., Ragland, J.D. (2013). Semantic processes leading to true and false memory formation in schizophrenia. Schizophrenia Research, 147, 320–325.CrossRefGoogle ScholarPubMed
Poppenk, J., Moscovitch, M. (2011). A hippocampal marker of recollection memory ability among healthy young adults: Contributions of posterior and anterior segments. Neuron, 6, 931–937.CrossRefGoogle Scholar
Power, J.D., Barnes, K.A., Snyder, A.Z., Schlaggar, B.L., Petersen, S.E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage, 59, 2142–2154.CrossRefGoogle ScholarPubMed
Prince, S.E., Daselaar, S.M., Cabeza, R. (2005). Neural correlates of relational memory: Successful encoding and retrieval of semantic and perceptual associations. Journal of Neuroscience, 25, 1203–1210.CrossRefGoogle ScholarPubMed
Ranganath, C., Ritchey, M. (2012). Two cortical systems for memory-guided behaviour. Nature Review Neuroscience, 13, 713–726.CrossRefGoogle ScholarPubMed
Ranganath, C., Yonelinas, A.P., Cohen, M.X., Dy, C.J., Tom, S.M., D'Esposito, M. (2004). Dissociable correlates of recollection and familiarity within the medial temporal lobes. Neuropsychologia, 42, 2–13.CrossRefGoogle ScholarPubMed
Rissman, J., Gazzaley, A., D'Esposito, M. (2004). Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage, 23, 752–763.CrossRefGoogle ScholarPubMed
Roediger, H.L., McDermott, K.B. (1995). Creating false memories: Remembering words not presented in lists. Journal of Experimental Psychology, 21, 803–814.Google Scholar
Schacter, D.L. (1999). The seven sins of memory insights from psychology and cognitive neuroscience. American Psychologist, 54, 182–203.CrossRefGoogle ScholarPubMed
Shannon, B.J., Buckner, R.L. (2004). Functional-anatomic correlates of memory retrieval that suggests nontraditional processing roles for multiple distinct regions within posterior parietal cortex. Journal of Neuroscience, 24, 10084–10092.CrossRefGoogle ScholarPubMed
Slotnick, S.D., Schacter, D.L. (2004). A sensory signature that distinguishes true from false memories. Nature Neuroscience, 7, 664–672.CrossRefGoogle ScholarPubMed
Stadler, M.A., Roediger, H.L., McDermott, K.B. (1999). Norms for word lists that create false memories. Memory & Cognition, 27, 494–500.CrossRefGoogle ScholarPubMed
Stark, C.E., Squire, L.R. (2000). fMRI activity in the medial temporal lobe during recognition memory as a function of study-test interval. Hippocampus, 10, 329–337.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Van Dijk, K.R.A., Sabuncu, M.R., Buckner, R.L. (2011). The influence of head motion on intrinsic functional connectivity MRI. Neuroimage, 59, 431–438.CrossRefGoogle ScholarPubMed
Wagner, A.D., Desmond, J.E., Demb, J.B., Glover, G.H., Gabrieli, J.D. (1997). Semantic repetition priming for verbal and pictorial knowledge: A functional MRI study of left inferior prefrontal cortex. Journal of Cognitive Neuroscience, 9, 714–726.CrossRefGoogle ScholarPubMed
Wimmer, M.C., Howe, M.L. (2009). The development of automatic associative processes and children's false memories. Journal of Experimental Child Psychology, 104, 447–465.CrossRefGoogle ScholarPubMed
Xia, M., Wang, J., He, Y. (2013). BrainNet Viewer: A network visualization tool for human brain connectomics. PLoS One, 8, e68910.CrossRefGoogle ScholarPubMed
Yonelinas, A.P., Otten, L.J., Shaw, K.N., Rugg, M.D. (2005). Separating the brain regions involved in recollection and familiarity in recognition memory. Journal of Neuroscience, 25, 3002–3008.CrossRefGoogle ScholarPubMed
Zhu, B., Cheng, C., Loftus, E.F., Lin, C., Dong, Q. (2013). The relationship between DRM and misinformation false memories. Memory & Cognition, 41, 832–838.CrossRefGoogle ScholarPubMed
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