H.M.'s Language Production Deficits: Implications for Relations between Memory, Semantic Binding, and the Hippocampal System ☆ ☆☆ ★

Abstract To test the claim that H.M. exhibits a “pure memory deficit” that has left his language production intact, we compared the language production of H.M. and controls in three studies. In Study 1, participants described the two meanings of visually presented sentences that they knew were ambiguous, and H.M.'s descriptions suggested a semantic-level production deficit: Relative to controls of comparable age, intelligence, and education, H.M.'s descriptions were significantly less effective, less clear, less concise, and more repetitious at lexical, phrase, and sentence levels of language production. In Study 2, naive judges rated H.M.'s descriptions as less grammatical, less comprehensible, and less coherent than descriptions of controls. Study 3 replicated these results for conversational speech about childhood events that occurred long before H.M.'s operation, his epilepsy, and his epilepsy treatments. Present results contradict stages of processing theories that localize H.M.'s deficit to a storage stage that is independent of processes for retrieving and producing verbal materials, and instead support a distributed-memory theory in which memory storage and retrieval involving verbal materials are inherent aspects of normal language production.

[1]  W. Bechtel,et al.  A companion to cognitive science , 1999 .

[2]  Donald G. MacKay,et al.  H.M. Revisited: Relations between Language Comprehension, Memory, and the Hippocampal System , 1998, Journal of Cognitive Neuroscience.

[3]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[4]  Heinz Er,et al.  The clinical syndrome of early‐life bilateral hippocampal sclerosis , 1997 .

[5]  E. Heinz,et al.  The clinical syndrome of early‐life bilateral hippocampal sclerosis , 1997, Annals of neurology.

[6]  B T Hyman,et al.  H. M.’s Medial Temporal Lobe Lesion: Findings from Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[7]  K Bock,et al.  Language production: Methods and methodologies , 1996, Psychonomic bulletin & review.

[8]  D. Poeppel A Critical Review of PET Studies of Phonological Processing , 1996, Brain and Language.

[9]  Donald G. MacKay,et al.  Relations Between Language and Memory: The Case of Repetition Deafness , 1996 .

[10]  D. Amaral,et al.  Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation , 1996, The Journal of Neuroscience.

[11]  N. Woolf Global and serial neurons form a hierarchically arranged interface proposed to underlie memory and cognition , 1996, Neuroscience.

[12]  Michelle D. Miller,et al.  Can cognitive aging contribute to fundamental psychological theory? Repetition deafness as a test case , 1996 .

[13]  D. G. MacKay,et al.  Repetition Blindness Interacts with Syntactic Grouping in Rapidly Presented Sentences , 1996 .

[14]  G. Bower Reactivating a Reactivation Theory of Implicit Memory , 1996, Consciousness and Cognition.

[15]  Gurindar S. Sohi,et al.  Memory systems , 1996, CSUR.

[16]  Harold Pashler,et al.  Structures, Processes, and the Flow of Information , 1996 .

[17]  Timothy A. Salthouse,et al.  Handbook of the psychology of aging, 4th ed. , 1996 .

[18]  Neal J. Cohen,et al.  Erratum: The hippocampal memory system and its functional components: Further explication and clarification (Behavioral and Brain Sciences (1994) 17:3 (500)) , 1996 .

[19]  Basic and applied memory: Theory in context , 1996 .

[20]  Donald G. MacKay,et al.  Language, memory, and aging: Distributed deficits and the structure of new-versus-old connections. , 1996 .

[21]  D. Zaidel,et al.  The Interpretation of Sentence Ambiguity in Patients with Unilateral Focal Brain Surgery , 1995, Brain and Language.

[22]  J D Gabrieli,et al.  Double dissociation of memory capacities after bilateral occipital-lobe or medial temporal-lobe lesions. , 1995, Brain : a journal of neurology.

[23]  Philip J. Hilts,et al.  Memory's ghost : the strange tale of Mr. M and the nature of memory , 1995 .

[24]  I. Whishaw,et al.  Fundamentals of Human Neuropsychology , 1995 .

[25]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[26]  Wolfgang Klimesch,et al.  The Structure of Long-term Memory: A Connectivity Model of Semantic Processing , 1996 .

[27]  Richard S. J. Frackowiak,et al.  Brain activity during reading. The effects of exposure duration and task. , 1994, Brain : a journal of neurology.

[28]  A. Berthoz,et al.  Neurons responding to whole-body motion in the primate hippocampus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  F. Wilson Hippocampal neuronal activity in rat and primate: Memory and movement , 1994, Behavioral and Brain Sciences.

[30]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[31]  E. Tulving,et al.  Memory Systems 1994 , 1994 .

[32]  D. G. MacKay,et al.  Repetition blindness and aging: evidence for a binding deficit involving a single, theoretically specified connection. , 1994, Psychology and aging.

[33]  J L Ringo,et al.  Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons. , 1994, Journal of neurophysiology.

[34]  D. Norman Memory and attention: An introduction to human information processing. , 1994 .

[35]  David S. Olton,et al.  Hippocampal function and interference , 1994 .

[36]  Endel Tulving,et al.  The Role of Repetition and Associative Interference in New Semantic Learning in Amnesia: A Case Experiment , 1993, Journal of Cognitive Neuroscience.

[37]  T. Arbuckle,et al.  Aging, inhibition, and verbosity. , 1993, Journal of gerontology.

[38]  S. Grossberg,et al.  Normal and amnesic learning, recognition and memory by a neural model of cortico-hippocampal interactions , 1993, Trends in Neurosciences.

[39]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

[40]  Peter Graf,et al.  Implicit Memory : New Directions in Cognition, Development, and Neuropsychology , 1993 .

[41]  Jerome Engel,et al.  Surgical treatment of the epilepsies , 1993 .

[42]  Mary C. Potter,et al.  The regeneration of syntax in short term memory , 1992 .

[43]  D. G. MacKay Awareness and error detection: New theories and research paradigms , 1992, Consciousness and Cognition.

[44]  Lynn Nadel,et al.  Multiple Memory Systems: What and Why , 1992, Journal of Cognitive Neuroscience.

[45]  G. Cottrell,et al.  Cognitive Binding: A Computational-Modeling Analysis of a Distinction between Implicit and Explicit Memory , 1992, Journal of Cognitive Neuroscience.

[46]  E. Metter,et al.  Grammatical comprehension, aphasic syndromes and neuroimaging , 1991, Journal of Neurolinguistics.

[47]  Donald G. MacKay,et al.  On the tip of the tongue: What causes word finding failures in young and older adults? , 1991 .

[48]  E Halgren,et al.  Firing of human hippocampal units in relation to voluntary movements , 1991, Hippocampus.

[49]  Tim Shallice,et al.  Neuropsychological impairments of short-term memory , 1992 .

[50]  M. Corballis,et al.  Memory Mechanisms: A Tribute To G.v. Goddard , 1990 .

[51]  D. Schacter Perceptual Representation Systems and Implicit Memory , 1990, Annals of the New York Academy of Sciences.

[52]  M. W. Brown,et al.  Hippocampus and medial temporal cortex: Neuronal activity related to behavioural responses during the performance of memory tasks by primates , 1990, Behavioural Brain Research.

[53]  Lawrence Freedman,et al.  Fluent identification of repeated words. , 1990 .

[54]  W. Prinz,et al.  Relationships Between Perception and Action: Current Approaches , 1990 .

[55]  Walter Kintsch,et al.  Sentence memory: A theoretical analysis ☆ , 1990 .

[56]  A. Caramazza Cognitive Neuropsychology and Neurolinguistics: Advances in Models of Cognitive Function and Impairment , 1990 .

[57]  Thomas M. Hess,et al.  Aging and cognition : knowledge organization and utilization , 1990 .

[58]  D. G. MacKay,et al.  Chapter Five Cognition and Aging: A Theory of New Learning and the Use of Old Connections , 1990 .

[59]  D. Mackay,et al.  Perception, Action, and Awareness: A Three-Body Problem , 1990 .

[60]  W. Levelt,et al.  Speaking: From Intention to Articulation , 1990 .

[61]  R. Muller,et al.  The firing of hippocampal place cells predicts the future position of freely moving rats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  S. Keele,et al.  Timing Functions of The Cerebellum , 1989, Journal of Cognitive Neuroscience.

[63]  S. Corkin,et al.  Rate of forgetting in H.M.: 6-month recognition. , 1988, Behavioral neuroscience.

[64]  E. Metter,et al.  Subcortical structures in aphasia. An analysis based on (F-18)-fluorodeoxyglucose, positron emission tomography, and computed tomography. , 1988, Archives of neurology.

[65]  M. Garrett Processes in language production , 1988 .

[66]  N. Cohen,et al.  The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection , 1988, Brain and Cognition.

[67]  Fred Plum,et al.  Language, communication, and the brain. , 1988, Research publications - Association for Research in Nervous and Mental Disease.

[68]  Cortical-subcortical differences in aphasia. , 1988, Research publications - Association for Research in Nervous and Mental Disease.

[69]  N. Cohen,et al.  Forgetting in H.M.: A second look , 1987, Neuropsychologia.

[70]  Gerard Kempen,et al.  An Incremental Procedural Grammar for Sentence Formulation , 1987, Cogn. Sci..

[71]  L. Squire CHAPTER 7 – Memory and the Brain* , 1986 .

[72]  G S Dell,et al.  A spreading-activation theory of retrieval in sentence production. , 1986, Psychological review.

[73]  B. Boruff,et al.  Short-term memory capacity: magic number or magic spell? , 1986, Journal of experimental psychology. Learning, memory, and cognition.

[74]  H. Eichenbaum,et al.  Diminished ability to interpret and report internal states after bilateral medial temporal resection: case H.M. , 1985, Behavioral neuroscience.

[75]  D. Schacter,et al.  Implicit and explicit memory for new associations in normal and amnesic subjects. , 1985, Journal of experimental psychology. Learning, memory, and cognition.

[76]  N. Cohen,et al.  Dissociations Among Processes in Remote Memory , 1985, Annals of the New York Academy of Sciences.

[77]  James L. McClelland,et al.  Distributed Models of Cognitive Processes: Applications to Learning and Memory a , 1985, Annals of the New York Academy of Sciences.

[78]  R. Kesner Correspondence between Humans and Animals in Coding of Temporal Attributes: Role of Hippocampus and Prefrontal Cortex , 1985, Annals of the New York Academy of Sciences.

[79]  D. Olton,et al.  Memory dysfunctions: an integration of animal and human research from preclinical and clinical perspectives. , 1985, Annals of the New York Academy of Sciences.

[80]  S. Corkin Lasting Consequences of Bilateral Medial Temporal Lobectomy: Clinical Course and Experimental Findings in H.M. , 1984 .

[81]  A. Rubens,et al.  Disturbances of long-term memory in aphasic patients. A comparison of anterior and posterior lesions. , 1984, Brain : a journal of neurology.

[82]  Giuseppe Vallar,et al.  Fractionation of working memory: Neuropsychological evidence for a phonological short-term store , 1984 .

[83]  E. Tulving Elements of episodic memory , 1983 .

[84]  J. Gray,et al.  Précis of The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system , 1982, Behavioral and Brain Sciences.

[85]  D. G. MacKay The Problems of Flexibility, Fluency, and Speed-Accuracy Trade-Off in Skilled Behavior. , 1982 .

[86]  P. Muter,et al.  Very rapid forgetting , 1980, Memory & cognition.

[87]  D. Benson,et al.  Interictal memory and language impairment in temporal lobe epilepsy , 1980, Neurology.

[88]  Wayne A. Wickelgren,et al.  Chunking and consolidation: A theoretical synthesis of semantic networks configuring in conditioning , 1979 .

[89]  E. Warrington,et al.  Further analysis of the prior learning effect in amnesic patients , 1978, Neuropsychologia.

[90]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[91]  Peter E. Morris,et al.  Aspects of Memory , 1978 .

[92]  T. Shallice,et al.  Short-term memory impairment and spontaneous speech , 1977, Neuropsychologia.

[93]  Harold Goodglass,et al.  Phonological factors in auditory comprehension in aphasia , 1977, Neuropsychologia.

[94]  William D. Marslen-Wilson,et al.  Memory for remote events in anterograde amnesia: Recognition of public figures from newsphotographs , 1975, Neuropsychologia.

[95]  B. Milner,et al.  Psychological aspects of focal epilepsy and its neurosurgical management. , 1975, Advances in neurology.

[96]  Chris L. S. Coryn,et al.  Short-term memory , 1975 .

[97]  J. Lackner Observations on the speech processing capabilities of an amnesic patient: several aspects of H.M.'s language function. , 1974, Neuropsychologia.

[98]  E. Warrington,et al.  The effect of prior learning on subsequent retention in amnesic patients. , 1974, Neuropsychologia.

[99]  Wayne A. Wickelgren,et al.  The long and the short of memory. , 1973 .

[100]  Philip M. Corsi Human memory and the medial temporal region of the brain. , 1972 .

[101]  C. Riper The Nature of Stuttering , 1971 .

[102]  B. Milner,et al.  Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.☆ , 1968 .

[103]  Wayne A. Wickelgren,et al.  Sparing of short-term memory in an amnesic patient: Implications for strength theory of memory , 1968 .

[104]  Murray Sidman,et al.  Some additional quantitative observations of immediate memory in a patient with bilateral hippocampal lesions , 1968 .

[105]  W. Scoville Amnesia after bilateral mesial temporal-lobe excision: Introduction to case H.M. , 1968 .

[106]  Suzanne Corkin,et al.  ACQUISITION OF MOTOR SKILL AFTER BILATERAL MEDIAL TEMPORAL-LOBE EXCISION , 1968 .

[107]  Richard C. Atkinson,et al.  Human Memory: A Proposed System and its Control Processes , 1968, Psychology of Learning and Motivation.

[108]  Thomas G. Bever,et al.  In search of ambiguity , 1967 .

[109]  D. Drachman,et al.  Memory and the hippocampal complex. II. Is memory a multiple process , 1966 .

[110]  B. Milner Effects of Different Brain Lesions on Card Sorting: The Role of the Frontal Lobes , 1963 .

[111]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.