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Functional Neuroimaging Approaches to Human Memory

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Abstract

Historically, studies of brain-damaged humans and experimentally lesioned animals have provided abundant evidence regarding neural underpinning for episodic memory. These studies have revealed that the medial temporal lobe, including the hippocampus, plays a critical role in different memory stages including encoding, consolidation, and retrieval. Furthermore, these studies demonstrated differences in the level of impairment caused by a lesion across memory stages, suggesting that each stage might recruit different brain regions, although some of them might overlap. The advancement of neuroimaging methods such as functional magnetic resonance imaging (fMRI) enabled investigation of the thorough coverage of brain regions without invasion in healthy human subjects. In this chapter, we offer comprehensive and concise commentaries on functional neuroimaging approaches to reveal mechanisms underlying memory encoding, retrieval and consolidation. We further describe novel approaches such as multi-voxel pattern analysis used for decoding of memory representations and real-time fMRI that could show causality beyond correlation.

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References

  • Atkinson RC, Juola JF (1973) Factors influencing speed and accuracy of word recognition. Atten Perform IV:583–612

    Google Scholar 

  • Atkinson RC, Herrmann DJ, Wescourt KT (1974) Search processes in recognition memory. In: Solso R (ed) Theories in cognitive psychology: the Loyola symposium. Halsted Press, New York, pp 193–238

    Google Scholar 

  • Buzsaki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6(2):81–92

    Article  CAS  PubMed  Google Scholar 

  • Cabeza R, Ciaramelli E, Moscovitch M (2012) Cognitive contributions of the ventral parietal cortex: an integrative theoretical account. Trends Cogn Sci 16(6):338–352

    Article  PubMed  PubMed Central  Google Scholar 

  • Daselaar SM, Prince SE, Cabeza R (2004) When less means more: deactivations during encoding that predict subsequent memory. NeuroImage 23(3):921–927

    Article  CAS  PubMed  Google Scholar 

  • Daselaar SM, Fleck MS, Cabeza R (2006) Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. J Neurophysiol 96(4):1902–1911

    Article  CAS  PubMed  Google Scholar 

  • Davachi L, Mitchell JP, Wagner AD (2003) Multiple routes to memory: distinct medial temporal lobe processes build item and source memories. Proc Natl Acad Sci U S A 100(4):2157–2162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deuker L, Olligs J, Fell J, Kranz TA, Mormann F, Montag C, Reuter M, Elger CE, Axmacher N (2013) Memory consolidation by replay of stimulus-specific neural activity. J Neurosci 33(49):19373–19383

    Article  CAS  PubMed  Google Scholar 

  • Diana RA, Yonelinas AP, Ranganath C (2007) Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends Cogn Sci 11(9):379–386

    Article  PubMed  Google Scholar 

  • Dickerson BC, Miller SL, Greve DN, Dale AM, Albert MS, Schacter DL, Sperling RA (2007) Prefrontal-hippocampal-fusiform activity during encoding predicts intraindividual differences in free recall ability: an event-related functional-anatomic MRI study. Hippocampus 17(11):1060–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dolcos F, Denkova E, Dolcos S (2012) Neural correlates of emotional memories: a review of evidence from brain imaging studies. Psychologia 55(2):80–111

    Article  Google Scholar 

  • Duverne S, Motamedinia S, Rugg MD (2009) The relationship between aging, performance, and the neural correlates of successful memory encoding. Cereb Cortex 19(3):733–744

    Article  PubMed  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 Res Bull 55(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • Garoff RJ, Slotnick SD, Schacter DL (2005) The neural origins of specific and general memory: the role of the fusiform cortex. Neuropsychologia 43(6):847–859

    Article  PubMed  Google Scholar 

  • Gilmore AW, Nelson SM, McDermott KB (2015) A parietal memory network revealed by multiple MRI methods. Trends Cogn Sci 19(9):534–543

    Article  PubMed  Google Scholar 

  • Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12(10):1222–1223

    Article  CAS  PubMed  Google Scholar 

  • Hammond DC (2011) What is neurofeedback: an update. J Neurother 15(4):305–336

    Article  Google Scholar 

  • Haynes JD, Rees G (2006) Decoding mental states from brain activity in humans. Nat Rev Neurosci 7(7):523–534

    Article  CAS  PubMed  Google Scholar 

  • Henson RN, Rugg MD, Shallice T, Josephs O, Dolan RJ (1999) Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. J Neurosci 19(10):3962–3972

    CAS  PubMed  Google Scholar 

  • Hirose S, Chikazoe J, Jimura K, Yamashita K, Miyashita Y, Konishi S (2009) Sub-centimeter scale functional organization in human inferior frontal gyrus. NeuroImage 47(2):442–450

    Article  PubMed  Google Scholar 

  • Huijbers W, Schultz AP, Vannini P, McLaren DG, Wigman SE, Ward AM, Hedden T, Sperling RA (2013) The encoding/retrieval flip: interactions between memory performance and memory stage and relationship to intrinsic cortical networks. J Cogn Neurosci 25(7):1163–1179

    Article  PubMed  PubMed Central  Google Scholar 

  • Jadhav SP, Kemere C, German PW, Frank LM (2012) Awake hippocampal sharp-wave ripples support spatial memory. Science 336(6087):1454–1458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kahn I, Davachi L, Wagner AD (2004) Functional-neuroanatomic correlates of recollection: implications for models of recognition memory. J Neurosci 24(17):4172–4180

    Article  CAS  PubMed  Google Scholar 

  • Kensinger EA, Schacter DL (2006) Amygdala activity is associated with the successful encoding of item, but not source, information for positive and negative stimuli. J Neurosci 26(9):2564–2570

    Article  CAS  PubMed  Google Scholar 

  • Kim H (2011) Neural activity that predicts subsequent memory and forgetting: a meta-analysis of 74 fMRI studies. NeuroImage 54(3):2446–2461

    Article  PubMed  Google Scholar 

  • Kim H, Cabeza R (2007) Trusting our memories: dissociating the neural correlates of confidence in veridical versus illusory memories. J Neurosci 27(45):12190–12197

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Daselaar SM, Cabeza R (2010) Overlapping brain activity between episodic memory encoding and retrieval: roles of the task-positive and task-negative networks. NeuroImage 49(1):1045–1054

    Article  PubMed  Google Scholar 

  • Kirwan CB, Stark CE (2004) Medial temporal lobe activation during encoding and retrieval of novel face-name pairs. Hippocampus 14(7):919–930

    Article  PubMed  PubMed Central  Google Scholar 

  • Konishi S, Wheeler ME, Donaldson DI, Buckner RL (2000) Neural correlates of episodic retrieval success. NeuroImage 12(3):276–286

    Article  CAS  PubMed  Google Scholar 

  • Mandler G (1979) Organization and repetition: organizational principles with special reference to rote learning. In: Nilsson L (ed) Perspectives on memory research. Wiley, New York, pp 293–327

    Google Scholar 

  • Mandler G, Pearlstone Z, Koopmans HS (1969) Effects of organization and semantic similarity on recall and recognition. J Verbal Learn Verbal Behav 8(3):410–423

    Article  Google Scholar 

  • Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN (2007) Wandering minds: the default network and stimulus-independent thought. Science 315(5810):393–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDermott KB, Jones TC, Petersen SE, Lageman SK, Roediger HL 3rd (2000) Retrieval success is accompanied by enhanced activation in anterior prefrontal cortex during recognition memory: an event-related fMRI study. J Cogn Neurosci 12(6):965–976

    Article  CAS  PubMed  Google Scholar 

  • Mur M, Bandettini PA, Kriegeskorte N (2009) Revealing representational content with pattern-information fMRI – an introductory guide. Soc Cogn Affect Neurosci 4(1):101–109

    Article  PubMed  PubMed Central  Google Scholar 

  • Otten LJ, Rugg MD (2001) When more means less: neural activity related to unsuccessful memory encoding. Curr Biol 11(19):1528–1530

    Article  CAS  PubMed  Google Scholar 

  • Paller KA, Kutas M, Mayes AR (1987) Neural correlates of encoding in an incidental learning paradigm. Electroencephalogr Clin Neurophysiol 67(4):360–371

    Article  CAS  PubMed  Google Scholar 

  • Polyn SM, Natu VS, Cohen JD, Norman KA (2005) Category-specific cortical activity precedes retrieval during memory search. Science 310(5756):1963–1966

    Article  CAS  PubMed  Google Scholar 

  • Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Nat Acad Sci U S A 98(2):676–682

    Article  CAS  Google Scholar 

  • Ritchey M, Wing EA, LaBar KS, Cabeza R (2013) Neural similarity between encoding and retrieval is related to memory via hippocampal interactions. Cereb Cortex 23(12):2818–2828

    Article  PubMed  Google Scholar 

  • Rugg MD, Vilberg KL (2013) Brain networks underlying episodic memory retrieval. Curr Opin Neurobiol 23(2):255–260

    Article  CAS  PubMed  Google Scholar 

  • Rugg MD, Fletcher PC, Frith CD, Frackowiak RS, Dolan RJ (1996) Differential activation of the prefrontal cortex in successful and unsuccessful memory retrieval. Brain 119(Pt 6):2073–2083

    Article  PubMed  Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20(1):11–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherwood MS, Kane JH, Weisend MP, Parker JG (2016) Enhanced control of dorsolateral prefrontal cortex neurophysiology with real-time functional magnetic resonance imaging (rt-fMRI) neurofeedback training and working memory practice. NeuroImage 124(Pt A):214–223

    Article  PubMed  Google Scholar 

  • Simons JS, Spiers HJ (2003) Prefrontal and medial temporal lobe interactions in long-term memory. Nat Rev Neurosci 4(8):637–648

    Article  CAS  PubMed  Google Scholar 

  • Sommer T, Rose M, Weiller C, Buchel C (2005) Contributions of occipital, parietal and parahippocampal cortex to encoding of object-location associations. Neuropsychologia 43(5):732–743

    Article  PubMed  Google Scholar 

  • Spaniol J, Davidson PS, Kim AS, Han H, Moscovitch M, Grady CL (2009) Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 47(8–9):1765–1779

    Article  PubMed  Google Scholar 

  • Squire LR (1982) The neuropsychology of human memory. Annu Rev Neurosci 5:241–273

    Article  CAS  PubMed  Google Scholar 

  • Squire LR, Alvarez P (1995) Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol 5(2):169–177

    Article  CAS  PubMed  Google Scholar 

  • Staresina BP, Alink A, Kriegeskorte N, Henson RN (2013) Awake reactivation predicts memory in humans. Proc Natl Acad Sci U S A 110(52):21159–21164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stoeckel LE, Garrison KA, Ghosh S, Wighton P, Hanlon CA, Gilman JM, Greer S, Turk-Browne NB, deBettencourt MT, Scheinost D, Craddock C, Thompson T, Calderon V, Bauer CC, George M, Breiter HC, Whitfield-Gabrieli S, Gabrieli JD, LaConte SM, Hirshberg L, Brewer JA, Hampson M, Van Der Kouwe A, Mackey S, Evins AE (2014) Optimizing real time fMRI neurofeedback for therapeutic discovery and development. Neuroimage: Clinical 5:245–255

    Article  CAS  Google Scholar 

  • Sulzer J, Haller S, Scharnowski F, Weiskopf N, Birbaumer N, Blefari ML, Bruehl AB, Cohen LG, DeCharms RC, Gassert R, Goebel R, Herwig U, LaConte S, Linden D, Luft A, Seifritz E, Sitaram R (2013) Real-time fMRI neurofeedback: progress and challenges. NeuroImage 76:386–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutherland GR, McNaughton B (2000) Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10(2):180–186

    Article  CAS  PubMed  Google Scholar 

  • Tambini A, Ketz N, Davachi L (2010) Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 65(2):280–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tulving E (1999) Memory, consciousness and the brain: the Tallinn conference. Psychology Press, Philadelphia

    Google Scholar 

  • Uncapher MR, Rugg MD (2009) Selecting for memory? The influence of selective attention on the mnemonic binding of contextual information. J Neurosci 29(25):8270–8279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner AD, Schacter DL, Rotte M, Koutstaal W, Maril A, Dale AM, Rosen BR, Buckner RL (1998) Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281(5380):1188–1191

    Article  CAS  PubMed  Google Scholar 

  • Wagner AD, Shannon BJ, Kahn I, Buckner RL (2005) Parietal lobe contributions to episodic memory retrieval. Trends Cogn Sci 9(9):445–453

    Article  PubMed  Google Scholar 

  • Weissman DH, Roberts KC, Visscher KM, Woldorff MG (2006) The neural bases of momentary lapses in attention. Nat Neurosci 9(7):971–978

    Article  CAS  PubMed  Google Scholar 

  • Wheeler ME, Buckner RL (2004) Functional-anatomic correlates of remembering and knowing. NeuroImage 21(4):1337–1349

    Article  PubMed  Google Scholar 

  • Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265(5172):676–679

    Article  CAS  PubMed  Google Scholar 

  • Yamashita K, Hirose S, Kunimatsu A, Aoki S, Chikazoe J, Jimura K, Masutani Y, Abe O, Ohtomo K, Miyashita Y, Konishi S (2009) Formation of long-term memory representation in human temporal cortex related to pictorial paired associates. J Neurosci 29(33):10335–10340

    Article  CAS  PubMed  Google Scholar 

  • Yonelinas AP (2002) The nature of recollection and familiarity: a review of 30 years of research. J Mem Lang 46(3):441–517

    Article  Google Scholar 

  • Yoo JJ, Hinds O, Ofen N, Thompson TW, Whitfield-Gabrieli S, Triantafyllou C, Gabrieli JD (2012) When the brain is prepared to learn: enhancing human learning using real-time fMRI. NeuroImage 59(1):846–852

    Article  PubMed  Google Scholar 

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Correspondence to Junichi Chikazoe .

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Chikazoe, J., Konishi, S. (2017). Functional Neuroimaging Approaches to Human Memory. In: Tsukiura, T., Umeda, S. (eds) Memory in a Social Context. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56591-8_2

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