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Mitlibraries Email: Docs@Mit.Edu Document Services Room 14-0551 77 Massachusetts Avenue Cambridge, MA 02139 Ph: 617.253.5668 Fax: 617.253.1690 MITLibraries Email: [email protected] Document Services http://libraries.mit.edu/docs DISCLAIMER OF QUALITY Due to the condition of the original material, there are unavoidable flaws in this reproduction. We have made every effort possible to provide you with the best copy available. If you are dissatisfied with this product and find it unusable, please contact Document Services as soon as possible. Thank you. Some pages in the original document contain pictures, graphics, or text that is illegible. SCHERING- PLOUGH LBRARY MEMORY SYSTEMS OF THE HUMAN BRAIN: DISSOCIATIONS AMONG LEARING CAPACITIES IN AMNESIA Vc. t by John D. E. Gabrieli B.A. Yale University (1978) SUBMITTED TO THE DEPARTMENT OF BRAIN AND CCGITIVE SCIENCES IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN BEHAVIORAL NEUROSCIENCE at the MASSACHUSETTS INSTITUTE OF TECHNOLOGY February, 1987 @Massachusetts. Institute of Technology, 1986 Signature of Author........... ........ .... ......................... Department of Brain and Cognitive Sciences September 10, 1986 Certified by............ ... ... ............ Professor Suzanne Corkin / Thesis Supervisor Accepted by........... ...................................................... Professor Emilio Bizzi, Chairman Department of Brain and Cognitive Sciences 4iL, j :Lr'.: ./?'- Memory Systems of the Human Brain: Dissociations Among Learning Capacities in Amnesia John D. E. Gabrieli Abstract This thesis aimed to characterize different kinds of memory that are believed to reflect the functioning of distinct memory systems of the human brain. Accordingly, the experiments sought to dissociate spared from compromised learning capacities in patients with global amnesia, a neurological syndrome associated with bilateral limbic lesions and marked by a deficit in fact learning (recall and recognition of events and materials). In contrast, such patients can learn some skills and can demonstrate some verbal priming effects. These findings suggest that fact learning depends upon cortico-limbic pathways, whereas some kinds of skill learning and priming are mediated by structures of the cerebral cortex, cerebellum, or basal ganglia. The main subject of study was H.M., whose amnesia followed bilateral resection of medial temporal-lobe structures. His case has contributed substantially to the modern definition of the amnesic syndrome, and provided the first documentation of preserved learning despite amnesia. Patients with other etiologies of global amnesia, such as Korsakoff's syndrome, and with memory impairment due to Alzheimer's disease, were also examined in some experiments. The experiments probed the applicability of current theories about the neural organization of human memory to the amnesia following bilateral resection of the hippocampus and amygdala. One series of experiments indicated that semantic learning was not spared as proposed by the semantic/episodic model of memory. A second series of experiments found no support for the hypothesis that amnesia reflects the disruption of automatic mnemonic processes that record contextual memories. Other experiments confirmed and extended demonstrations of preserved learning of motor, perceptual, and problem-solving skills, and demonstrated, for the first time in H.M., preserved verbal priming. Also, the first example of preserved nonverbal priming in amnesia was documented with H.M. The main current theory about spared learning, the procedural/declarative distinction, provided little insight into the mechanism of spared capacities, and incorrectly predicted normal lexical-decision repetition-priming in H.M. Finally patients with Alzheimer's disease were impaired in stem-completion priming (a result also incompatible with the procedural/declarative distinction), but some of those patients were normal in their ability to learn a motor skill. This was the first dissociation between two kinds of learning spared in global amnesia. The results are discussed in terms of prospects for further advances in discovering the computational properties and neural substrates underlying dissociable human memory systems. Thesis Supervisor: Professor Suzanne Corkin Title: Associate Professor, Behavioral Neuroscience Department of Brain- and Cognitive Sciences TABLE OF CONTENTS Page Acknowledgments 5 Biographical Note 7 /1I. Introduction 9 ,The Amnesic Syndrome 9 Preserved Learning in Amnesia 11 Memory Systems: A Definition 17 ,/II. Background 19 Memory as a Unitary Engram 19 The Case of H.M. 20 Dissociations in the Amnesic Syndrome 24 Dissociations in the Neurological Foundations 27 of Memory Preserved Learning Capacities Despite Amnesia 30 Preserved Learning in H.M. 32 Current Theories About Memory Systems 35 III. Research Plan 44 Issues in Positing a Memory System 44 Strategy of the Present Research 49 IV. Anterograde Acquisition of Semantic Knowledge 53 -.-Experiment 1: Learning the meanings of words 58 Experiment 2a: Lexical and semantic 69 knowledge for words entering the language after H.M.'s operation -Experiment 2b: Identification of incomplete words 79 entering the language after H.M.'s operation Experiment 3: Lexical knowledge for names of 82 people who became famous after H.M.'s operation \, V. Anterograde Acquisition of Knowledge for Content 96 and Context Experiment 1: Verbal temporal ordering 96 Experiment 2: Recall for spatial location 109 'VI. Anterograde Acquisition of Motor Knowledge 119 Experiment 1: Mirror tracing 121 ,.-VII. Anterograde Acquisition of Perceptual Knowledge 138 Experiment 1:Identification of mirror-reversed 140 text Experiment 2: Identification of incomplete 163 words and nonwords Experiment 3: Specific learning in general skill 184 acquisition 4 ,v'VIII. Anterograde Acquisition of Problem-solving Knowledge 189 Experiment 1: Number series 190 Experiment 2: Sugar production 199 Experiment 3: Missionaries and cannibals 209 IX. Expression of Anterograde Verbal Experience on Verbal 217 Performance (Priming) -- Experiment 1: Stem-completion priming in H.M. 219 Experiment 2: Latency of stem-completion priming 227 Experiment 3: Stem-completion priming in amnesia 236 and in Alzheimer's disease .-Experiment 4: Nonverbal pattern priming 257 -- Experiments 5a & 5b: Lexical decision repetition 262 priming in H.M. X. Conclusions 275 The Semantic/Episodic Distinction 275 The Content/Context Distinction 277 The Procedural/Declarative Distinction 278 Dichotomies in the Amnesic Syndrome 283 The Neural Basis of Multiple Memory Systems 289 Future Research 292 XI. References 295 Appendices 326 ACKNOWLEDGMENTS Professional The experiments in this thesis were performed under the guidance and supervision, and with the collaboration, of Suzanne Corkin. Collaborators on particular experiments included Neal Cohen (Chapter IV; Chapter IX, Experiment 1), Edith Sullivan (V-1), Harvey Sagar (V-1), Chris Darnell and Mark Snow (V-2), Margaret Keane (V-2; IX-4), Susan Mickel (VI), Frank Merrill (VII), Mary Minn (VIII-3), Ben Stanger (IX-2 and -3), Bill Milberg (IX-4), and George Xixis (IX-5a). Experiments related to but not reported in this thesis were done with Alice Cronin-Golomb, Jim Hodgson, Janell Schweickert, and J. Tim Soley. The analyses and interpretation of results benefited tremendously from discussions with my collaborators, but the ones in the thesis are my own and do not necessarily reflect the views of my coworkers. Also, the members of my thesis committee, Laird Cermak, Mary Potter, and Gerald Schneider provided valuable comments that are already reflected in the thesis and will be even more evident as parts of the thesis are revised and submitted for publication. I have also been fortunate to receive outstanding support in the execution and reporting of these experiments. Rae Ann Clegg was especially helpful in a number of the experiments, as were Kate Banks, Gena Desclos, Allison Feeley, Denise McDermott, Jill Merves, and Marguerite Randolph. Frank Merrill and Mark Snow did the computer programming for most of the experiments and aided in the analysis of the results. Dave Shea helped in programming some of the statistical analysis. Beverly Chew and John Rosen provided assistance on questions of statistics. A number of undergraduates assisted in gathering pilot data, most of them through the Undergraduate Research Opportunities Program (UROP): Yashi Ahmed, Avrim Blum, Pauline Fisher, Ira Haimowitz, Diane Ho, Jill Gaulding, Matt Kaplan, Ellen Maker, and David Small. Stephanie Biggs, Aliyah Baruchin, and Marie Wininger have been most gracious in preparing this long manuscript. Gena Desclos provided much assistance in preparing the figures. I am grateful to Brenda Milner for the opportunity to work with H.M., and to John Growdon for referral of the patients with Alzheimer's disease and Parkinson's disease to the MIT Clinical Research Center. I should also like to acknowledge my appreciation for the work done and ideas generated by researchers in the field of the study of amnesia who are cited throughout this thesis. The scientific and imaginative qualities of their work excited me about the experimental study of amnesia, and my own thoughts and experiments drew heavily upon theirs. Harold Bloom (1973) wrote that each generation of writers (such as the Romantic poets Shelley and Keats) misreads their predecessors (in their case Milton) in an unconscious but willful urge to find some mistaken theme or view left open for them to develop correctly. With this
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