Abstract
To understand human memory, it is important to determine why some experiences are remembered whereas others are forgotten. Until recently, insights into the neural bases of human memory encoding, the processes by which information is transformed into an enduring memory trace, have primarily been derived from neuropsychological studies of humans with select brain lesions. The advent of functional neuroimaging methods, such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), has provided a new opportunity to gain additional understanding of how the brain supports memory formation. Importantly, the recent development of event-related fMRI methods now allows for examination of trial-by-trial differences in neural activity during encoding and of the consequences of these differences for later remembering. In this review, we consider the contributions of PET and fMRI studies to the understanding of memory encoding, placing a particular emphasis on recent event-related fMRI studies of the Dm effect: that is, differences in neural activity during encoding that are related to differences in subsequent memory. We then turn our attention to the rich literature on the Dm effect that has emerged from studies using event-related potentials (ERPs). It is hoped that the integration of findings from ERP studies, which offer higher temporal resolution, with those from event-related fMRI studies, which offer higher spatial resolution, will shed new light on when and why encoding yields subsequent remembering.
Full Text
The Full Text of this article is available as a PDF (296.6 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Besson M., Kutas M. The many facets of repetition: a cued-recall and event-related potential analysis of repeating words in same versus different sentence contexts. J Exp Psychol Learn Mem Cogn. 1993 Sep;19(5):1115–1133. doi: 10.1037//0278-7393.19.5.1115. [DOI] [PubMed] [Google Scholar]
- Brewer J. B., Zhao Z., Desmond J. E., Glover G. H., Gabrieli J. D. Making memories: brain activity that predicts how well visual experience will be remembered. Science. 1998 Aug 21;281(5380):1185–1187. doi: 10.1126/science.281.5380.1185. [DOI] [PubMed] [Google Scholar]
- Buckner R. L., Koutstaal W. Functional neuroimaging studies of encoding, priming, and explicit memory retrieval. Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):891–898. doi: 10.1073/pnas.95.3.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chapman R. M., McCrary J. W., Chapman J. A. Short-term memory: the "storage" component of human brain responses predicts recall. Science. 1978 Dec 15;202(4373):1211–1214. doi: 10.1126/science.725596. [DOI] [PubMed] [Google Scholar]
- D'Esposito M., Aguirre G. K., Zarahn E., Ballard D., Shin R. K., Lease J. Functional MRI studies of spatial and nonspatial working memory. Brain Res Cogn Brain Res. 1998 Jul;7(1):1–13. doi: 10.1016/s0926-6410(98)00004-4. [DOI] [PubMed] [Google Scholar]
- Demb J. B., Desmond J. E., Wagner A. D., Vaidya C. J., Glover G. H., Gabrieli J. D. Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity. J Neurosci. 1995 Sep;15(9):5870–5878. doi: 10.1523/JNEUROSCI.15-09-05870.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dolan R. J., Fletcher P. C. Dissociating prefrontal and hippocampal function in episodic memory encoding. Nature. 1997 Aug 7;388(6642):582–585. doi: 10.1038/41561. [DOI] [PubMed] [Google Scholar]
- Donchin E. Presidential address, 1980. Surprise!...Surprise? Psychophysiology. 1981 Sep;18(5):493–513. doi: 10.1111/j.1469-8986.1981.tb01815.x. [DOI] [PubMed] [Google Scholar]
- Elger C. E., Grunwald T., Lehnertz K., Kutas M., Helmstaedter C., Brockhaus A., Van Roost D., Heinze H. J. Human temporal lobe potentials in verbal learning and memory processes. Neuropsychologia. 1997 May;35(5):657–667. doi: 10.1016/s0028-3932(96)00110-8. [DOI] [PubMed] [Google Scholar]
- Fabiani M., Donchin E. Encoding processes and memory organization: a model of the von Restorff effect. J Exp Psychol Learn Mem Cogn. 1995 Jan;21(1):224–240. doi: 10.1037//0278-7393.21.1.224. [DOI] [PubMed] [Google Scholar]
- Fabiani M., Karis D., Donchin E. Effects of mnemonic strategy manipulation in a Von Restorff paradigm. Electroencephalogr Clin Neurophysiol. 1990 Feb;75(2):22–35. doi: 10.1016/0013-4694(90)90149-e. [DOI] [PubMed] [Google Scholar]
- Fabiani M., Karis D., Donchin E. P300 and recall in an incidental memory paradigm. Psychophysiology. 1986 May;23(3):298–308. doi: 10.1111/j.1469-8986.1986.tb00636.x. [DOI] [PubMed] [Google Scholar]
- Fernández G., Brewer J. B., Zhao Z., Glover G. H., Gabrieli J. D. Level of sustained entorhinal activity at study correlates with subsequent cued-recall performance: a functional magnetic resonance imaging study with high acquisition rate. Hippocampus. 1999;9(1):35–44. doi: 10.1002/(SICI)1098-1063(1999)9:1<35::AID-HIPO4>3.0.CO;2-Z. [DOI] [PubMed] [Google Scholar]
- Fernández G., Weyerts H., Schrader-Bölsche M., Tendolkar I., Smid H. G., Tempelmann C., Hinrichs H., Scheich H., Elger C. E., Mangun G. R. Successful verbal encoding into episodic memory engages the posterior hippocampus: a parametrically analyzed functional magnetic resonance imaging study. J Neurosci. 1998 Mar 1;18(5):1841–1847. doi: 10.1523/JNEUROSCI.18-05-01841.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fiez J. A., Raichle M. E., Balota D. A., Tallal P., Petersen S. E. PET activation of posterior temporal regions during auditory word presentation and verb generation. Cereb Cortex. 1996 Jan-Feb;6(1):1–10. doi: 10.1093/cercor/6.1.1. [DOI] [PubMed] [Google Scholar]
- Friedman D. Cognitive event-related potential components during continuous recognition memory for pictures. Psychophysiology. 1990 Mar;27(2):136–148. doi: 10.1111/j.1469-8986.1990.tb00365.x. [DOI] [PubMed] [Google Scholar]
- Friedman D. ERPs during continuous recognition memory for words. Biol Psychol. 1990 Feb;30(1):61–87. doi: 10.1016/0301-0511(90)90091-a. [DOI] [PubMed] [Google Scholar]
- Friedman D. Event-related potential investigations of cognitive development and aging. Ann N Y Acad Sci. 1992 Jul 1;658:33–64. doi: 10.1111/j.1749-6632.1992.tb22838.x. [DOI] [PubMed] [Google Scholar]
- Friedman D., Ritter W., Snodgrass J. G. ERPs during study as a function of subsequent direct and indirect memory testing in young and old adults. Brain Res Cogn Brain Res. 1996 Jul;4(1):1–13. doi: 10.1016/0926-6410(95)00041-0. [DOI] [PubMed] [Google Scholar]
- Friedman D., Sutton S. Event-related potentials during continuous recognition memory. Electroencephalogr Clin Neurophysiol Suppl. 1987;40:316–321. [PubMed] [Google Scholar]
- Gabrieli J. D., Brewer J. B., Desmond J. E., Glover G. H. Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science. 1997 Apr 11;276(5310):264–266. doi: 10.1126/science.276.5310.264. [DOI] [PubMed] [Google Scholar]
- Gabrieli J. D. Cognitive neuroscience of human memory. Annu Rev Psychol. 1998;49:87–115. doi: 10.1146/annurev.psych.49.1.87. [DOI] [PubMed] [Google Scholar]
- Halgren E., Smith M. E. Cognitive evoked potentials as modulatory processes in human memory formation and retrieval. Hum Neurobiol. 1987;6(2):129–139. [PubMed] [Google Scholar]
- Haxby J. V., Ungerleider L. G., Horwitz B., Maisog J. M., Rapoport S. I., Grady C. L. Face encoding and recognition in the human brain. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):922–927. doi: 10.1073/pnas.93.2.922. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heinze H. J., Mangun G. R., Burchert W., Hinrichs H., Scholz M., Münte T. F., Gös A., Scherg M., Johannes S., Hundeshagen H. Combined spatial and temporal imaging of brain activity during visual selective attention in humans. Nature. 1994 Dec 8;372(6506):543–546. doi: 10.1038/372543a0. [DOI] [PubMed] [Google Scholar]
- Johnson M. K., Hashtroudi S., Lindsay D. S. Source monitoring. Psychol Bull. 1993 Jul;114(1):3–28. doi: 10.1037/0033-2909.114.1.3. [DOI] [PubMed] [Google Scholar]
- Johnson R., Jr, Pfefferbaum A., Kopell B. S. P300 and long-term memory: latency predicts recognition performance. Psychophysiology. 1985 Sep;22(5):497–507. doi: 10.1111/j.1469-8986.1985.tb01639.x. [DOI] [PubMed] [Google Scholar]
- Kapur S., Craik F. I., Tulving E., Wilson A. A., Houle S., Brown G. M. Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2008–2011. doi: 10.1073/pnas.91.6.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kapur S., Tulving E., Cabeza R., McIntosh A. R., Houle S., Craik F. I. The neural correlates of intentional learning of verbal materials: a PET study in humans. Brain Res Cogn Brain Res. 1996 Nov;4(4):243–249. doi: 10.1016/s0926-6410(96)00058-4. [DOI] [PubMed] [Google Scholar]
- Kelley W. M., Miezin F. M., McDermott K. B., Buckner R. L., Raichle M. E., Cohen N. J., Ollinger J. M., Akbudak E., Conturo T. E., Snyder A. Z. Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron. 1998 May;20(5):927–936. doi: 10.1016/s0896-6273(00)80474-2. [DOI] [PubMed] [Google Scholar]
- Klein D., Milner B., Zatorre R. J., Meyer E., Evans A. C. The neural substrates underlying word generation: a bilingual functional-imaging study. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2899–2903. doi: 10.1073/pnas.92.7.2899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Konishi S., Yoneyama R., Itagaki H., Uchida I., Nakajima K., Kato H., Okajima K., Koizumi H., Miyashita Y. Transient brain activity used in magnetic resonance imaging to detect functional areas. Neuroreport. 1996 Dec 20;8(1):19–23. doi: 10.1097/00001756-199612200-00005. [DOI] [PubMed] [Google Scholar]
- Lepage M., Habib R., Tulving E. Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus. 1998;8(4):313–322. doi: 10.1002/(SICI)1098-1063(1998)8:4<313::AID-HIPO1>3.0.CO;2-I. [DOI] [PubMed] [Google Scholar]
- Liu A. K., Belliveau J. W., Dale A. M. Spatiotemporal imaging of human brain activity using functional MRI constrained magnetoencephalography data: Monte Carlo simulations. Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8945–8950. doi: 10.1073/pnas.95.15.8945. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mangun G. R., Buonocore M. H., Girelli M., Jha A. P. ERP and fMRI measures of visual spatial selective attention. Hum Brain Mapp. 1998;6(5-6):383–389. doi: 10.1002/(SICI)1097-0193(1998)6:5/6<383::AID-HBM10>3.0.CO;2-Z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martin A., Wiggs C. L., Weisberg J. Modulation of human medial temporal lobe activity by form, meaning, and experience. Hippocampus. 1997;7(6):587–593. doi: 10.1002/(SICI)1098-1063(1997)7:6<587::AID-HIPO1>3.0.CO;2-C. [DOI] [PubMed] [Google Scholar]
- McCarthy G., Blamire A. M., Rothman D. L., Gruetter R., Shulman R. G. Echo-planar magnetic resonance imaging studies of frontal cortex activation during word generation in humans. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):4952–4956. doi: 10.1073/pnas.90.11.4952. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Musen G., Treisman A. Implicit and explicit memory for visual patterns. J Exp Psychol Learn Mem Cogn. 1990 Jan;16(1):127–137. doi: 10.1037//0278-7393.16.1.127. [DOI] [PubMed] [Google Scholar]
- Münte T. F., Heinze H. J., Scholz M., Künkel H. Effects of a cholinergic nootropic (WEB 1881 FU) on event-related potentials recorded in incidental and intentional memory tasks. Neuropsychobiology. 1988;19(3):158–168. doi: 10.1159/000118453. [DOI] [PubMed] [Google Scholar]
- Nyberg L. Mapping episodic memory. Behav Brain Res. 1998 Feb;90(2):107–114. doi: 10.1016/s0166-4328(97)00094-6. [DOI] [PubMed] [Google Scholar]
- Paller K. A., Kutas M., Mayes A. R. Neural correlates of encoding in an incidental learning paradigm. Electroencephalogr Clin Neurophysiol. 1987 Oct;67(4):360–371. doi: 10.1016/0013-4694(87)90124-6. [DOI] [PubMed] [Google Scholar]
- Paller K. A., McCarthy G., Wood C. C. ERPs predictive of subsequent recall and recognition performance. Biol Psychol. 1988 Jun;26(1-3):269–276. doi: 10.1016/0301-0511(88)90023-3. [DOI] [PubMed] [Google Scholar]
- Paller K. A. Recall and stem-completion priming have different electrophysiological correlates and are modified differentially by directed forgetting. J Exp Psychol Learn Mem Cogn. 1990 Nov;16(6):1021–1032. doi: 10.1037//0278-7393.16.6.1021. [DOI] [PubMed] [Google Scholar]
- Paulesu E., Frith C. D., Frackowiak R. S. The neural correlates of the verbal component of working memory. Nature. 1993 Mar 25;362(6418):342–345. doi: 10.1038/362342a0. [DOI] [PubMed] [Google Scholar]
- Petersen S. E., Fox P. T., Posner M. I., Mintun M., Raichle M. E. Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature. 1988 Feb 18;331(6157):585–589. doi: 10.1038/331585a0. [DOI] [PubMed] [Google Scholar]
- Rombouts S. A., Machielsen W. C., Witter M. P., Barkhof F., Lindeboom J., Scheltens P. Visual association encoding activates the medial temporal lobe: a functional magnetic resonance imaging study. Hippocampus. 1997;7(6):594–601. doi: 10.1002/(SICI)1098-1063(1997)7:6<594::AID-HIPO2>3.0.CO;2-F. [DOI] [PubMed] [Google Scholar]
- Rosen B. R., Buckner R. L., Dale A. M. Event-related functional MRI: past, present, and future. Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):773–780. doi: 10.1073/pnas.95.3.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rugg M. D. Memories are made of this. Science. 1998 Aug 21;281(5380):1151–1152. doi: 10.1126/science.281.5380.1151. [DOI] [PubMed] [Google Scholar]
- Sanquist T. F., Rohrbaugh J. W., Syndulko K., Lindsley D. B. Electrocortical signs of levels of processing: perceptual analysis and recognition memory. Psychophysiology. 1980 Nov;17(6):568–576. doi: 10.1111/j.1469-8986.1980.tb02299.x. [DOI] [PubMed] [Google Scholar]
- Schacter D. L., Chiu C. Y., Ochsner K. N. Implicit memory: a selective review. Annu Rev Neurosci. 1993;16:159–182. doi: 10.1146/annurev.ne.16.030193.001111. [DOI] [PubMed] [Google Scholar]
- Schacter D. L., Wagner A. D. Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus. 1999;9(1):7–24. doi: 10.1002/(SICI)1098-1063(1999)9:1<7::AID-HIPO2>3.0.CO;2-K. [DOI] [PubMed] [Google Scholar]
- Schmidt S. R. Encoding and retrieval processes in the memory for conceptually distinctive events. J Exp Psychol Learn Mem Cogn. 1985 Jul;11(3):565–578. doi: 10.1037//0278-7393.11.3.565. [DOI] [PubMed] [Google Scholar]
- Shallice T., Fletcher P., Frith C. D., Grasby P., Frackowiak R. S., Dolan R. J. Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature. 1994 Apr 14;368(6472):633–635. doi: 10.1038/368633a0. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Tulving E., Kapur S., Craik F. I., Moscovitch M., Houle S. Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2016–2020. doi: 10.1073/pnas.91.6.2016. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tulving E., Markowitsch H. J., Craik F. E., Habib R., Houle S. Novelty and familiarity activations in PET studies of memory encoding and retrieval. Cereb Cortex. 1996 Jan-Feb;6(1):71–79. doi: 10.1093/cercor/6.1.71. [DOI] [PubMed] [Google Scholar]
- Van Petten C., Senkfor A. J. Memory for words and novel visual patterns: repetition, recognition, and encoding effects in the event-related brain potential. Psychophysiology. 1996 Sep;33(5):491–506. doi: 10.1111/j.1469-8986.1996.tb02425.x. [DOI] [PubMed] [Google Scholar]
- Wagner A. D., Poldrack R. A., Eldridge L. L., Desmond J. E., Glover G. H., Gabrieli J. D. Material-specific lateralization of prefrontal activation during episodic encoding and retrieval. Neuroreport. 1998 Nov 16;9(16):3711–3717. doi: 10.1097/00001756-199811160-00026. [DOI] [PubMed] [Google Scholar]
- Wagner A. D., Schacter D. L., Rotte M., Koutstaal W., Maril A., Dale A. M., Rosen B. R., Buckner R. L. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science. 1998 Aug 21;281(5380):1188–1191. doi: 10.1126/science.281.5380.1188. [DOI] [PubMed] [Google Scholar]
- Wagner A. D. Working memory contributions to human learning and remembering. Neuron. 1999 Jan;22(1):19–22. doi: 10.1016/s0896-6273(00)80674-1. [DOI] [PubMed] [Google Scholar]
- Weyerts H., Tendolkar I., Smid H. G., Heinze H. J. ERPs to encoding and recognition in two different inter-item association tasks. Neuroreport. 1997 May 6;8(7):1583–1588. doi: 10.1097/00001756-199705060-00007. [DOI] [PubMed] [Google Scholar]
- Zarahn E., Aguirre G., D'Esposito M. A trial-based experimental design for fMRI. Neuroimage. 1997 Aug;6(2):122–138. doi: 10.1006/nimg.1997.0279. [DOI] [PubMed] [Google Scholar]