Neural activity differs between explicit and implicit learning of artificial grammar strings: An fMRI study

Psychobiology - Tập 28 Số 3 - Trang 283-292 - 2000
Seger, Carol A.1, Prabhakaran, Vivek2, Poldrack, Russell A.2, Gabrieli, John D. E.2
1Department of Psychology, Colorado State University, Fort Collins, USA
2Stanford University, Stanford, USA

Tóm tắt

Functional magnetic resonance imaging was used to investigate the neural areas underlying retrieval of implicit and explicit knowledge about letter strings. Participants studied strings formed according to an artificial grammar, then performed implicit-learning-based judgments (judging the grammatical status of the string) or explicit-learning-based judgments (recognition) on novel grammatical strings. In comparison with a baseline task, recognition and grammatical judgments led to different patterns of neural activation: Recognition activated the right frontal cortex, whereas grammatical judgment activated the left frontal cortex. Recognition led to higher activity in the precuneus and medial occipital cortex, whereas grammatical judgments led to suppression of activity in the precuneus and activation in the lateral occipital cortex. When the surface structure of the strings was changed, grammatical judgments led to bilateral frontal activity and bilateral but left-lateralized activity in the occipital and parietal lobes. These results provide further evidence for a dissociation between the neural bases of implicit and explicit learning.

Tài liệu tham khảo

citation_journal_title=Journal of Experimental Psychology: Learning, Memory, & Cognition; citation_title=Modality independence of implicitly learned grammatical knowledge; citation_author=G T M Altmann, Z Dienes, A Goode; citation_volume=21; citation_publication_date=1995; citation_pages=899-912; citation_doi=10.1037/0278-7393.21.4.899; citation_id=CR1 citation_title=Implicit learning: Theoretical and practical issues; citation_publication_date=1993; citation_id=CR2; citation_author=D C Berry; citation_author=Z Dienes; citation_publisher=Erlbaum citation_title=Human cerebral asymmetry; citation_publication_date=1983; citation_id=CR3; citation_author=J Bradshaw; citation_author=N Nettleton; citation_publisher=Prentice-Hall citation_journal_title=NeuroImage; citation_title=Functional-anatomic study of episodic retrieval: II. Selective averaging of event-related fMRI trials to test the retrieval success hypothesis; citation_author=R L Buckner, W Koutstaal, D L Schacter, A M Dale, M Rotte, B R Rosen; citation_volume=7; citation_publication_date=1998; citation_pages=163-175; citation_doi=10.1006/nimg.1998.0328; citation_id=CR4 citation_journal_title=NeuroImage; citation_title=Functional-anatomic study of episodic retrieval using fMRI; citation_author=R L Buckner, W Koutstaal, D L Schacter, A D Wagner, B R Rosen; citation_volume=7; citation_publication_date=1998; citation_pages=151-162; citation_doi=10.1006/nimg.1998.0327; citation_id=CR5 citation_journal_title=Memory; citation_title=Memory for items and memory for relations in the procedural/declarative memory framework; citation_author=N J Cohen, R A Poldrack, H Eichenbaum; citation_volume=5; citation_publication_date=1997; citation_pages=131-178; citation_doi=10.1080/741941149; citation_id=CR6 citation_journal_title=Neuropsychologia; citation_title=Acquisition of motor skill after bilateral medial temporal-lobe excision; citation_author=S Corkin; citation_volume=6; citation_publication_date=1968; citation_pages=255-265; citation_doi=10.1016/0028-3932(68)90024-9; citation_id=CR7 citation_journal_title=Cognitive Science; citation_title=Mapping across domains without feedback: A neural network model of transfer of implicit knowledge; citation_author=Z Dienes, G T M Altmann, S-J Gao; citation_volume=23; citation_publication_date=1999; citation_pages=53-82; citation_doi=10.1207/s15516709cog2301_3; citation_id=CR8 citation_journal_title=Hippocampus; citation_title=Encoding and retrieval in the human medial temporal lobes: An empirical investigation using functional magnetic resonance imaging; citation_author=R J Dolan, P F Fletcher; citation_volume=9; citation_publication_date=1999; citation_pages=25-34; citation_doi=10.1002/(SICI)1098-1063(1999)9:1<25::AID-HIPO3>3.0.CO;2-4; citation_id=CR9 citation_journal_title=Cerebral Cortex; citation_title=Learning-related neuronal responses in prefrontal cortex studied with functional neuroimaging; citation_author=P Fletcher, C Buchel, O Josephs, K Friston, R Dolan; citation_volume=9; citation_publication_date=1999; citation_pages=168-178; citation_doi=10.1093/cercor/9.2.168; citation_id=CR10 citation_journal_title=Brain; citation_title=Brain activity during memory retrieval: The influence of imagery and semantic cueing; citation_author=P Fletcher, T Shallice, C D Frith, R S J Frackowiak, R J Dolan; citation_volume=119; citation_publication_date=1996; citation_pages=1587-1596; citation_doi=10.1093/brain/119.5.1587; citation_id=CR11 citation_journal_title=Brain; citation_title=The functional roles of prefrontal cortex in episodic memory: II. Retrieval; citation_author=P Fletcher, T Shallice, C D Frith, R S J Frackowiak, R Dolan; citation_volume=121; citation_publication_date=1998; citation_pages=1249-1256; citation_doi=10.1093/brain/121.7.1249; citation_id=CR12 citation_journal_title=NeuroImage; citation_title=Characterizing evoked hemodynamics with fMRI; citation_author=K J Friston, C D Frith, R D Turner, R S J Frackowiak; citation_volume=2; citation_publication_date=1995; citation_pages=157-165; citation_doi=10.1006/nimg.1995.1018; citation_id=CR13 citation_journal_title=Human Brain Mapping; citation_title=Statistical parametric maps in functional imaging: A general linear approach; citation_author=K J Friston, A P Holmes, K J Worsley, J P Poline, C D Frith, R S J Frackowiak; citation_volume=2; citation_publication_date=1995; citation_pages=189-210; citation_doi=10.1002/hbm.460020402; citation_id=CR14 citation_journal_title=Brain & Language; citation_title=Hemisphere differences in the acquisition and use of descriptive systems; citation_author=E Goldberg, L D Costa; citation_volume=14; citation_publication_date=1981; citation_pages=144-173; citation_doi=10.1016/0093-934X(81)90072-9; citation_id=CR15 citation_journal_title=Cognitive Psychology; citation_title=Transfer and complexity in artificial grammar learning; citation_author=R L Gomez; citation_volume=33; citation_publication_date=1997; citation_pages=154-207; citation_doi=10.1006/cogp.1997.0654; citation_id=CR16 citation_journal_title=Journal of Experimental Psychology: Learning, Memory, & Cognition; citation_title=What is learned from artificial grammars? Transfer tests of simple association; citation_author=R L Gomez, R W Schvaneveldt; citation_volume=20; citation_publication_date=1994; citation_pages=392-410; citation_doi=10.1037/0278-7393.20.2.396; citation_id=CR17 citation_journal_title=Journal of Experimental Psychology: Learning, Memory, & Cognition; citation_title=The information that amnesic patients do not forget; citation_author=P Graf, L R Squire, G Mandler; citation_volume=10; citation_publication_date=1984; citation_pages=164-178; citation_doi=10.1037/0278-7393.10.1.164; citation_id=CR18 citation_journal_title=Journal of Neuroscience; citation_title=Recollection and familiarity in recognition memory: An event-related functional magnetic resonance imaging study; citation_author=R N A Henson, M D Rugg, T Shallice, O Josephs, R J Dolan; citation_volume=19; citation_publication_date=1999; citation_pages=3962-3972; citation_id=CR19 citation_journal_title=Psychological Science; citation_title=Intact artificial grammar learning in amnesia: Dissociation of classification learning and explicit memory for specific instances; citation_author=B J Knowlton, S J Ramus, L R Squire; citation_volume=3; citation_publication_date=1992; citation_pages=172-179; citation_doi=10.1111/j.1467-9280.1992.tb00021.x; citation_id=CR20 citation_journal_title=Journal of Experimental Psychology: Learning, Memory, & Cognition; citation_title=The information acquired in artificial grammar learning; citation_author=B J Knowlton, L R Squire; citation_volume=20; citation_publication_date=1994; citation_pages=79-91; citation_doi=10.1037/0278-7393.20.1.79; citation_id=CR21 citation_journal_title=Journal of Experimental Psychology: Learning, Memory, & Cognition; citation_title=Artificial grammar learning depends on implicit acquisition of both abstract and exemplar-specific information; citation_author=B J Knowlton, L R Squire; citation_volume=22; citation_publication_date=1996; citation_pages=169-181; citation_doi=10.1037/0278-7393.22.1.169; citation_id=CR22 citation_journal_title=Neuropsychology; citation_title=Dissociations within nondeclarative memory in Huntington’s disease; citation_author=B J Knowlton, L R Squire, J S Paulsen, N R Swerdlow, M Swenson, N Butters; citation_volume=10; citation_publication_date=1996; citation_pages=538-548; citation_doi=10.1037/0894-4105.10.4.538; citation_id=CR23 citation_journal_title=Brain; citation_title=Episodic retrieval activates the precuneus irrespective of the imagery content of work pair associates: A PET study; citation_author=B J Krause, D Schmidt, F M Mottaghy, J Taylor, U Halsband, H Herzog, L Tellmann, H-W Muller-Gartner; citation_volume=122; citation_publication_date=1999; citation_pages=255-263; citation_doi=10.1093/brain/122.2.255; citation_id=CR24 citation_journal_title=NeuroImage; citation_title=Right anterior prefrontal cortex activation during semantic monitoring and working memory; citation_author=A K MacLeod, R L Buckner, F M Miezin, S E Petersen, M E Raichle; citation_volume=7; citation_publication_date=1998; citation_pages=41-48; citation_doi=10.1006/nimg.1997.0308; citation_id=CR25 citation_title=Representing artificial grammars: Transfer across stimulus forms and modalities; citation_inbook_title=How implicit is implicit learning?; citation_publication_date=1997; citation_pages=73-106; citation_id=CR26; citation_author=L Manza; citation_author=A S Reber; citation_publisher=Oxford University Press citation_journal_title=Journal of Experimental Psychology: Human Perception & Performance; citation_title=Abstract visual-form representations in the left cerebral hemisphere; citation_author=C J Marsolek; citation_volume=21; citation_publication_date=1995; citation_pages=375-386; citation_doi=10.1037/0096-1523.21.2.375; citation_id=CR27 citation_journal_title=Neuropsychology; citation_title=Form-specific explicit and implicit memory in the right cerebral hemisphere; citation_author=C J Marsolek, L R Squire, S M Kosslyn, M E Lulenski; citation_volume=8; citation_publication_date=1994; citation_pages=588-597; citation_doi=10.1037/0894-4105.8.4.588; citation_id=CR28 citation_journal_title=Journal of Experimental Psychology: Learning, Memory, & Cognition; citation_title=Role of implicit and explicit processes in learning from examples: A synergistic effect; citation_author=R C Mathews, R R Buss, W B Stanley, F Blanchard-Fields, J R Cho, B Druhan; citation_volume=15; citation_publication_date=1989; citation_pages=1083-1100; citation_doi=10.1037/0278-7393.15.6.1083; citation_id=CR29 citation_journal_title=Psychological Science; citation_title=Right-hemisphere memory superiority: Studies of a split-brain patient; citation_author=J Metcalfe, M Funnell, M S Gazzaniga; citation_volume=6; citation_publication_date=1995; citation_pages=157-164; citation_doi=10.1111/j.1467-9280.1995.tb00325.x; citation_id=CR30 citation_journal_title=Cognitive Psychology; citation_title=Attentional requirements of learning: Evidence from performance measures; citation_author=M J Nissen, P Bullemer; citation_volume=19; citation_publication_date=1987; citation_pages=1-32; citation_doi=10.1016/0010-0285(87)90002-8; citation_id=CR31 citation_journal_title=Trends in Cognitive Sciences; citation_title=The role of prefrontal cortex during tests of episodic memory; citation_author=S F Nolde, M K Johnson, C L Raye; citation_volume=2; citation_publication_date=1998; citation_pages=399-406; citation_doi=10.1016/S1364-6613(98)01233-9; citation_id=CR32 citation_journal_title=Psychonomic Bulletin & Review; citation_title=PET studies of encoding and retrieval: The HERA model; citation_author=L Nyberg, R Cabeza, E Tulving; citation_volume=3; citation_publication_date=1996; citation_pages=135-148; citation_doi=10.3758/BF03212412; citation_id=CR33 citation_journal_title=Science; citation_title=Activation of extrastriate and frontal cortical areas by visual words and word-like stimuli; citation_author=S E Petersen, P T Fox, A Z Snyder, M E Raichle; citation_volume=249; citation_publication_date=1990; citation_pages=1041-1044; citation_doi=10.1126/science.2396097; citation_id=CR34 citation_journal_title=Neuropsychology; citation_title=Striatal activation during cognitive skill learning; citation_author=R A Poldrack, V Prabhakaran, C A Seger, J D E Gabrieli; citation_volume=13; citation_publication_date=1999; citation_pages=564-574; citation_doi=10.1037/0894-4105.13.4.564; citation_id=CR35 Prabhakaran, V., Rypma, B., & Gabrieli, J. D. E. (in press). Neural substrates of mathematical reasoning: An fMRI study of neocortical activation during performance of the necessary arithmetic operations test. Neuropsychology. citation_journal_title=Cognitive Psychology; citation_title=Neural substrates of fluid reasoning: An fMRI study of neocortical activation during performance of the Raven’s Progressive Matrices test; citation_author=V Prabhakaran, J A L Smith, J E Desmond, G H Glover, J D E Gabrieli; citation_volume=33; citation_publication_date=1997; citation_pages=43-63; citation_doi=10.1006/cogp.1997.0659; citation_id=CR37 citation_journal_title=Brain; citation_title=Brain activity during reading: The effects of exposure duration and task; citation_author=C J Price, R J S Wise, J D G Watson, K Patterson, D Howard, R S J Frackowiak; citation_volume=117; citation_publication_date=1994; citation_pages=1255-1269; citation_doi=10.1093/brain/117.6.1255; citation_id=CR38 citation_journal_title=Journal of Neuroscience; citation_title=Differential sensitivity of human visual cortex to faces, letter-strings, and textures: A functional magnetic resonance imaging study; citation_author=A Puce, T Allison, M Asgari, J C Gore, G McCarthy; citation_volume=16; citation_publication_date=1996; citation_pages=5205-5215; citation_id=CR39 citation_journal_title=Brain; citation_title=Cerebral organization of component processes in reading; citation_author=K R Pugh, B A Shaywitz, S E Shaywitz, R T Constable, P Skudlarski, R K Fulbright, R A Bronen, D P Shankweiler, L Katz, J M Fletcher, J C Gore; citation_volume=119; citation_publication_date=1996; citation_pages=1221-1238; citation_doi=10.1093/brain/119.4.1221; citation_id=CR40 citation_journal_title=Journal of Verbal Learning & Verbal Behavior; citation_title=Implicit learning of artificial grammars; citation_author=A S Reber; citation_volume=6; citation_publication_date=1967; citation_pages=855-863; citation_doi=10.1016/S0022-5371(67)80149-X; citation_id=CR41 citation_journal_title=Journal of Experimental Psychology; citation_title=Transfer of syntactic structure in synthetic languages; citation_author=A S Reber; citation_volume=81; citation_publication_date=1969; citation_pages=115-119; citation_doi=10.1037/h0027454; citation_id=CR42 citation_journal_title=Journal of Experimental Psychology: General; citation_title=Implicit learning and tacit knowledge; citation_author=A S Reber; citation_volume=118; citation_publication_date=1989; citation_pages=219-235; citation_doi=10.1037/0096-3445.118.3.219; citation_id=CR43 citation_journal_title=Learning & Memory; citation_title=Contrasting cortical activity associated with category memory and recognition; citation_author=P J Reber, C E L Stark, L R Squire; citation_volume=5; citation_publication_date=1998; citation_pages=420-428; citation_id=CR44 citation_journal_title=Proceedings of the National Academy of Sciences; citation_title=Cortical areas supporting category learning identified using functional MRI; citation_author=P J Reber, C E L Stark, L R Squire; citation_volume=95; citation_publication_date=1998; citation_pages=747-750; citation_doi=10.1073/pnas.95.2.747; citation_id=CR45 citation_journal_title=NeuroImage; citation_title=Neural correlates of memory retrieval during recognition memory and cued recall; citation_author=M D Rugg, P C Fletcher, K Allan, C D Frith, R S J Frackowiak, R J Dolan; citation_volume=8; citation_publication_date=1998; citation_pages=262-273; citation_doi=10.1006/nimg.1998.0363; citation_id=CR46 citation_journal_title=Brain; citation_title=Differential activation of the prefrontal cortex in successful and unsuccessful memory retrieval; citation_author=M D Rugg, P C Fletcher, C D Frith, R S Frackowiak, R J Dolan; citation_volume=119; citation_publication_date=1996; citation_pages=2073-2083; citation_doi=10.1093/brain/119.6.2073; citation_id=CR47 citation_journal_title=NeuroImage; citation_title=Late onset of anterior prefrontal activity during true and false recognition: An event-related fMRI study; citation_author=D L Schacter, R L Buckner, W Koutstaal, A M Dale, B R Rosen; citation_volume=6; citation_publication_date=1997; citation_pages=259-269; citation_doi=10.1006/nimg.1997.0305; citation_id=CR48 citation_journal_title=Psychological Bulletin; citation_title=Implicit learning; citation_author=C A Seger; citation_volume=115; citation_publication_date=1994; citation_pages=163-196; citation_doi=10.1037/0033-2909.115.2.163; citation_id=CR49 citation_journal_title=Consciousness & Cognition; citation_title=Independent judgment-linked and motor-linked mechanisms in artificial grammar learning; citation_author=C A Seger; citation_volume=7; citation_publication_date=1998; citation_pages=259-284; citation_doi=10.1006/ccog.1997.0331; citation_id=CR50 citation_journal_title=Neuropsychologia; citation_title=Hemispheric asymmetries and individual differences in visual concept learning as measured by functional MRI; citation_author=C A Seger, R A Poldrack, V Prabhakaran, Z Zhao, G Glover, J D E Gabrieli; citation_volume=38; citation_publication_date=2000; citation_pages=1316-1324; citation_doi=10.1016/S0028-3932(00)00014-2; citation_id=CR51 citation_journal_title=Cerebral Cortex; citation_title=Top-down modulation of early sensory cortex; citation_author=G L Shulman, M Corbetta, R L Buckner, M E Raichle, J A Fiez, F M Miezin, S E Petersen; citation_volume=7; citation_publication_date=1997; citation_pages=193-206; citation_doi=10.1093/cercor/7.3.193; citation_id=CR52 citation_journal_title=Journal of Cognitive Neuroscience; citation_title=Common blood flow changes across visual tasks: II. Decreases in cerebral cortex; citation_author=G L Shulman, J A Fiez, M Corbetta, R L Buckner, F M Miezin, M E Raichle, S E Petersen; citation_volume=9; citation_publication_date=1997; citation_pages=648-663; citation_doi=10.1162/jocn.1997.9.5.648; citation_id=CR53 citation_journal_title=Cognitive Psychology; citation_title=Working memory: A view from neuroimaging; citation_author=E E Smith, J Jonides; citation_volume=33; citation_publication_date=1997; citation_pages=5-42; citation_doi=10.1006/cogp.1997.0658; citation_id=CR54 citation_journal_title=Cognition; citation_title=Alternative strategies of categorization; citation_author=E E Smith, A L Patalano, J Jonides; citation_volume=65; citation_publication_date=1998; citation_pages=167-196; citation_doi=10.1016/S0010-0277(97)00043-7; citation_id=CR55 citation_title=Declarative and nondeclarative memory: Multiple brain systems supporting learning and memory; citation_inbook_title=Memory systems 1994; citation_publication_date=1994; citation_pages=203-232; citation_id=CR56; citation_author=L R Squire; citation_publisher=MIT Press citation_journal_title=Proceedings of the National Academy of Sciences; citation_title=Activation of the hippocampus in normal humans: A functional anatomical study of memory; citation_author=L R Squire, J G Ojemann, F M Miesin, S E Petersen, T O Videen, M E Raichle; citation_volume=89; citation_publication_date=1992; citation_pages=1837-1841; citation_doi=10.1073/pnas.89.5.1837; citation_id=CR57 citation_title=Co-planar stereotactic atlas of the human brain; citation_publication_date=1988; citation_id=CR58; citation_author=J Talairach; citation_author=P Tournoux; citation_publisher=Thieme citation_journal_title=Proceedings of the National Academy of Sciences; citation_title=Hemispheric encoding/retrieval asymmetry in episodic memory: Positron emission tomography findings; citation_author=E Tulving, S Kapur, F I M Craik, M Moscovitch, S Houle; citation_volume=91; citation_publication_date=1994; citation_pages=2016-2020; citation_doi=10.1073/pnas.91.6.2016; citation_id=CR59 citation_journal_title=NeuroImage; citation_title=Activation of lateral extrastriate areas during orthographic processing of Japanese characters studied with fMRI; citation_author=I Uchida, H Kikyo, K Nakajima, S Konishi, K Sekihara, Y Miyashita; citation_volume=9; citation_publication_date=1999; citation_pages=208-215; citation_doi=10.1006/nimg.1999.0400; citation_id=CR60 citation_journal_title=Brain; citation_title=Prefrontal cortex and recognition memory Functional-MRI evidence for context-dependent retrieval processes; citation_author=A D Wagner, J E Desmond, G H Glover, J D E Gabrieli; citation_volume=121; citation_publication_date=1997; citation_pages=1985-2002; citation_doi=10.1093/brain/121.10.1985; citation_id=CR61 citation_journal_title=Nature; citation_title=The amnesic syndrome Consolidation or retrieval?; citation_author=E K Warrington, L Weiskrantz; citation_volume=228; citation_publication_date=1970; citation_pages=628-630; citation_doi=10.1038/228628a0; citation_id=CR62 Wharton, C M, Grafman, J, Filename, S K, Hansen, E K, Brainier, J, Marks, A, & Honda, M (1999). The neuroanatomy of analogical reasoning Manuscript submitted for publication. citation_journal_title=Journal of Computer Assisted Tomography; citation_title=Rapid automated algorithm for aligning and reslicing PET images; citation_author=R P Woods, S R Cherry, J C Mazziota; citation_volume=16; citation_publication_date=1992; citation_pages=620-633; citation_doi=10.1097/00004728-199207000-00024; citation_id=CR64