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Table 1. Quantitative Comparison of Activated Cerebral Regions (Brodmann s Areas) under Implicit and Explicit Memory Retrieval Tasks Location Implicit memory Explicit memory Act. index Act. pixels Act. ration Lat. index Act. pixels Act. ration Lat. index (AveSD) (%) (%) (AveSD) (%) (%) (%) PrCeG-4 7.013.5 42.9 79.6 28.650.0 42.9 9.0 60.6 PrCeG/PoCeG-43 22.139.7 42.9 0.6 25.939.2 42.9 60.2 7.7 SFG-6, 8 473.1361.2 100.0 28.3 401.7440.4 100.0 42.8 8.2 Frontal lobe SFG/MFG-10 62.4137.5 57.1 23.1 23.747.0 42.9 72.3 44.9 MFG-9, 46 172.6166.8 85.7 7.6 169.0200.0 71.4 15.1 1.0 IFG-44, 45 428.6158.4 100.0 27.0 342.1190.3 100.0 49.1 11.2 OrbG-11, 47 389.1549.6 85.7 1.1 317.4456.2 100.0 39.9 10.1 SCA-25 65.3166.6 28.6 30.4 11.121.2 42.9 53.8 70.8 STG-22 157.734.8 42.9 54.5 59.6129.4 57.1 32.9 58.3 STG/MTG-38 48.667.7 85.7 30.0 48.458.8 100.0 31.6 0.1 MTG-21 40.770.5 42.9 86.0 48.0114.1 42.9 29.2 8.2 Temporal Lobe ITG-20, 37 76.1104.5 71.4 12.6 142.7130.6 71.4 19.9 30.4 Temporal-28, 34, 36, 42 9.423.6 42.9 93.9 36.748.6 71.4 31.5 59.1 RhS-35 0.00.0 0.0 10.1 28.6 100.0 100.0 AnTG-41 22.628,7 42.9 17.7 48.970.4 42.9 8.2 36.8 PoCeG-1, 2, 3 53.061.1 71.4 59.0 69.9111.3 42.9 73.4 13.7 Parietal lobe Parietal-7 285.1181.9 100.0 18.7 420.0263.8 100.0 26.1 19.1 AG-39 133.1132.4 85.7 29.0 278.4144.2 100.0 7.1 35.3 SMG-40 218.3207.7 85.7 27.0 268.3206.0 100.0 11.7 10.3 Occlipital lobe Occipital-17, 18, 19 586.3319.3 100.0 15.7 753.4312.1 100.0 26.7 12.5 AnCiG-24, 32 243.4238.4 85.7 22.3 242.1245.0 100.0 23.2 0.3 Cingulate gyrus PoCiG-23 0.00.0 0.0 44.9 42.9 7.5 100.0 ICiG-26, 30 0.00.0 0.0 35.4 28.6 1.6 100.0 Act. pixel: nember of activated pixel, Act. ratio: activation ratio, Lat. index: lateralization index, Act. index: Activation index, Ave: average, SD: standard deviation PrCeG: precentral gyrus, PoCeG: postcentral gyrus, SFG: superior frontal gyrus, MFG: middle frontal gyrus, IFG: inferior frontal gyrus, OrbG: orbital gyrus, SCA: subcallosal area, STG: superior temporal gyrus, MTG: middle temporal gyrus, ITG: inferior temporal gyrus, Temporal: temporal lobe, Rhs: rhinal sulcus, AnTG: anterior transverse temporal gyrus, Parietal: parietal lobe, AG: angular gyrus, SMG: supramarginal gyrus, Occipital: occipital lobe, AnCiG: anterior cingulate gyrus, PoCiG: posterior cingulate gyrus, ICiG: isthmus of cingulate gyrus 203
Fig. 1. BOLD-MR images from 6 contiguous axial slices: (A) implicit vs. (B) explicit retrieval of previously learned words under the level with conceptual processing. Color-coded pixels on the activation maps were scaled to the range between the cutoff-threshold and the highest t-score (p<0.05). A B 204
Fig. 2. BOLD-MR images from 6 contiguous coronal slices: (A) implicit vs. (B) explicit retrieval of previously learned words under the level with conceptual processing. Color-coded pixels on the activation maps were scaled to the range between the cutoffthreshold and the highest t-score (p<0.05). A B 205
Implicit Explicit Fig. 3. Comparison of the activation ratios (%) of the volunteers corresponding to the cerebral regions (Brodmann s areas) activated during the performance of both implicit and explicit retrieval of previously encoded words under the level with conceptual processing. indicates the brain regions that were not activated. Fig. 4. Bar graph showing the activation indices (%) corresponding to the cerebral regions during implicit and explicit memory retrieval tasks under the level with conceptual processing. 206
Fig. 5. Lateralization of the implicit and explicit memory retrieval tasks of the encoded words under the level with conceptual processing. Fig. 6. Comparison of the lateralization indices (%) between implicit and explicit memory retrieval tasks in the frontal lobe. 207
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1. Atkinson RC, Shiffrin RM. A proposed system and its control processes: Psychol Learn Motiv. New York, Academic Press, 1968;2:89-195 2. Craik FIM, Lockhart RS. Levels of processing: a framework for memory research. J Verb Learn Behav 1972;11:671-684 3. Tulving E. How many memory systems are there? Am Psychol 1985;40;385-398 4. Schacter DL, Tulving E. What are the memory systems of 1994? In Schacter DL, Tulving E(Eds.), Memory Systems 1994. Cambridge, MA: The MIT Press, 1994;165 5. Schacter DL. Implicit memory: History and current status. J Exp Psychol Learn Mem Cogn 1987;13:501-518 6. Tulving E, Schacter DL. Priming and human memory systems. Science 1990;247:301-306 209
7. Jacoby LL. A process dissociation framework: separating automatic from intentional uses of memory. J Mem Lang 1991;30:513-541 8. Roediger HL 3rd, Blaxton TA. Effects of varying modality, surface features, and retention interval on priming in word-fragment completion. Mem Cogn 1987;15:379-388 9. Jacoby LL, Dallas M. On the relationship between autobiographical memory and perceptual learning. J Exp Phyghol Gen 1981;110: 306-340 10. Jacoby LL. Perceptual enhancement: Persistent efferts of an experience. J Exp Psychol Learn Mem Cogn 1983;9:21-38 11. Squire LR. Declarative memory and undeclarative memory: multiple brain systems supporting learning and memory. J Cogn Neurosci 1992;99:195-231 12. Pakin AJ. Memory: Phenomena, experiment, and theory. Oxford, Blackwell Publishers 1993 13. Zola-Morgan S, Squire LR. Neuroanatomy of memory. Annu Rev Neurosci 1993;16:547-563 14. Schacter DL. Introduction to Implicit memory: Multiple perspectives. Bull Psycho Soc 1990;28:338-340 15. Squire LR. Mem Brain. New York: Oxford University Press 1987 16. Michael W, Eysenck, Mark T. Keane. Cognitive psychology. Lawrence, Erlbaum Associates: Publishers Hove Press 1995 17. Kirchhoff BA, Wagner AD, Maril A, Stern CE. Prefrontal-temporal circuitry for episodic encoding and subsequent memory. J Neurosci 2000;20:6173-6180 18. Kavcic V, Zhong J, Yoshiura T, Doty RW. Commonality of fmri for retrieval but not for encoding of words versus nonverbalizable images. Neuroimage 1999;6:part2 of 2 parts 19. Buckner RL, Koutstaal W. Functional neuroimaging studies of encoding, priming, and explicit memory retrieval. Proc Natl Acad Sci 1998;95:891-898 20. Schacter DL, Wagner AD. Medial temporal lobe activations in fmri and PET studies of episodic encoding and retrieval. Hippocampus 1999;9:7-24 21. Nyberg L, Cabeza R, Tulving E. Asymmetric frontal activation during episodic memory: what kind of specificity? Trends Cogn Sci 1998;2:419-420 22. Desmond JE, Sum JM, Wagner AD, et al. Functional MRI measurement of language lateralization in Wada-tested patients. A neuropsychological and magnetic resonance study. Brain 1995;118: 1411-1419 23. Kapur N, Ellison D, Smith MP, McLellan DL, Burrows EH. Focal retrograde amnesia following bilateral temporal lobe pathology-a neuropsychological and magnetic resonance study. Brain 1992; 115:73-85 24. Zola-Morgan S, Squire LR. Neuroanatomy of memory. Annu Rev Neurosci 1993;16:547-563 25. Squire LR, Knowlton BJ. Memory, hippocampus, and brain systems. In M. Gazzanga (Ed), Cogn Neurosci. Cambridge: MIT, 1994; 825-838 26. Fazio F, Perani D, Gilardi MC, et al. Metabolic impairment in human amnesia: a PET study of memory networks. J Cereb Blood Flow Metab 1992;12:353-358 27. Buckner RL, Raichle ME, Miezin FM, Petersen SE. Functional anatomic studies of memory retrieval for auditory words and visual pictures. J Neurosci 1996;16:6219-6235 210
Neural Mechanism of Implicit and Explicit Memory Retrieval: Functional MR Imaging 1 Heoung-Keun Kang, M.D., Gwang-Woo Jeong, Ph.D., Tae-Jin Park, Ph.D. 2 Jeong-Jin Seo, M.D., Hyung-Joong Kim, Sung-Jong Eun, Tae-Woong Chung, M.D. 1 Department of Radiology, Chonnam National University Medical School 2 Department of Psychology, Chonnam National University Purpose: To identify, using functional MR imaging, distinct cerebral centers and to evaluate the neural mechanism associated with implicit and explicit retrieval of words during conceptual processing. Materials and Methods: Seven healthy volunteers aged 2125 (mean, 22) years underwent BOLD-based fmr imaging using a 1.5T Signa Horizon Echospeed MR system. To activate the cerebral cortices, a series of tasks was performed as follows: the encoding of two-syllable words, and implicit and explicit retrieval of previously learned words during conceptual processing. The activation paradigm consisted of a cycle of alternating periods of 30 seconds of stimulation and 30 seconds of rest. Stimulation was accomplished by encoding eight twosyllable words and the retrieval of previously presented words, while the control condition was a white screen with a small fixed cross. During the tasks we acquired ten slices (6 mm slice thickness, 1 mm gap) parallel to the AC-PC line, and the resulting functional activation maps were reconstructed using a statistical parametric mapping program (SPM 99). Results: A comparison of activation ratios (percentages), based on the number of volunteers, showed that activation of Rhs-35, PoCiG-23 and ICiG-2630 was associated with explicit retrieval only; other brain areas were activated during the performance of both implicit and explicit retrieval tasks. Activation ratios were higher for explicit tasks than for implicit; in the cingulate gyrus and temporal lobe they were 30% and 10% greater, respectively. During explicit retrieval, a distinct brain activation index (percentage) was seen in the temporal, parietal, and occipital lobe and cingulate gyrus, and PrCeG-4, Pr/PoCeG-43 in the frontal lobe. During implicit retrieval, on the other hand, activity was greater in the frontal lobe, including the areas of SCA-25, SFG/MFG- 10, IFG-4445, OrbG-1147, SFG-68, and MFG-946. Overall, activation was lateralized mainly in the left hemisphere during both implicit and explicit retrieval tasks. For explicit retrieval, the lateralization index was more than twice as high as for implicit retrieval. Conclusion: Our findings indicate that there is neuro-anatomical dissociation between implicit and explicit retrieval of words during conceptual processing, suggesting, on the basis of cognitive neuroscience, that the performance of implicit and explicit memory-related tasks involves different mechanisms. Index words : Encoding and retrieval Explicit and implicit retrieval Functional magnetic resonance imaging, fmri Address reprint requests to : Gwang-Woo Jeong, Ph.D., Department of Radiology, Chonnam National University Medical School, 8 Hack-dong, Dong-gu, Gwangju 501-757, Korea. Tel. 82-62-220-5881 Fax. 82-62-226-4380 E-mail: gwjeong@chonnam.ac.kr 211