The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection

doi:10.1016/0278-2626(88)90027-9

Brain and Cognition

Volume 7, Issue 2, April 1988, Pages 157-177

https://doi.org/10.1016/0278-2626(88)90027-9 Get rights and content

Abstract

The integrity of several aspects of semantic memory (including knowledge of the meaning, lexical status, perception, and pronunciation of words and famous names) was examined in H.M., a patient with anterograde amnesia following bilateral medial temporal-lobe excision. Despite normal memory for such semantic knowledge acquired prior to the onset of his amnesia in 1953, H.M. showed a severe deficit in memory for semantic information encountered subsequently. In combination with the previously reported impairments in new learning shown by H.M., the deficits observed here point to an association between semantic and episodic memory, and do not lend support to a distinction between them. The acquisition of semantic and episodic information, therefore, appears to depend upon a common memory system that requires the intact functioning of medial temporal-lobe structures.

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Evidence of some new, but imperfect, semantic knowledge over multiple exposures was reported in both K.C (Hayman et al., 1993; Tulving et al., 1991; Tulving, 1993; Westmacott et al., 2001; Westmacott and Moscovitch, 2001, 2002). and H.M. (Freed et al., 1987; Gabrieli et al., 1988; O’Kane et al., 2004; James & MacKay, 2001; MacKay et al., 1998). In contrast, E.P. was said not to exhibit any form of declarative learning (Reed et al., 1997); findings suggestive of limited learning of household items in E.P. were interpreted as reflecting premorbidly established preferences of certain items over others (Bayley et al., 2008).
Kent Cochrane (K.C.) has been investigated by researchers for nearly three decades after intracranial trauma from a motorcycle accident at age 30 resulted in a striking profile of amnesia. K.C. suffered severe anterograde amnesia in both verbal and non-verbal domains which was accompanied by selective retrograde amnesia for personal events experienced prior to the time of his injury (episodic memory), with relative preservation of memory for personal and world facts (semantic memory), and of implicit memory. This pattern of spared and impaired memory extended to spatial memory for large-scale environments and beyond memory to future imagining and decision-making. Post-mortem brain findings at age 62 included moderate diffuse atrophy, left orbitofrontal contusion, left posterior cerebral artery infarct, and left anterior frontal watershed infarct. Notably, there was severe neuronal loss and gliosis of the hippocampi bilaterally. The left hippocampus was severely affected anteriorly and posteriorly, but CA2, CA4, and the dentate gyrus (DG) were focally spared. There was associated degeneration of the left fornix. The right hippocampus showed near complete destruction anteriorly, with relative preservation posteriorly, mainly of CA4 and DG. Bilateral parahippocampal gyri and left anterior thalamus also showed neuron loss and gliosis. There was no evidence of co-existing neurodegenerative phenomena on beta-amyloid, phosphorylated tau, or TDP-43 immunostaining. The extent of damage to medial temporal lobe structures is in keeping with K.C.'s profound anterograde and retrograde amnesia, with the exception of the unexpected finding of preserved CA2/CA4 and DG. K.C.'s case demonstrates that relatively clean functional dissociations are still possible following widespread brain damage, with structurally compromised brain regions unlikely to be critical to cognitive functions found to be intact. In this way, the findings presented here add to K.C.'s significant contributions to our understanding of clinical-anatomical relationships in memory.

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^☆: Presented in part at the Society for Neuroscience meeting in Boston, November 1983, and in the first author's doctoral thesis submitted to the Massachusetts Institute of Technology. Supported by Grants MH24433, RR00088, and 2T32GM07478. This research was done with the valuable assistance of Rae Ann Clegg, Maryann Martone, Edith Sullivan, Allison Feeley, Frank Merrill, Mark Snow, Mary Minn, and George Xixis. Frederick C. Mish of Merriam-Webster Dictionary, Inc., kindly provided the dictionary supplements. William Milberg, Margaret Keane, Laird Cermak, and Mary Potter provided helpful comments on prior versions of this paper.

¹: Neal Cohen's current address is Cognitive Neuropsychology Laboratory, Departments of Psychology and Neurology, Johns Hopkins University and School of Medicine.

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The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection☆

Abstract

Neuropsychologia

Neuropsychologia

Neuropsychologia

Neuropsychologia

Neuropsychologia

Neuropsychologia

Neuropsychologia

Temporal gradients in the retrograde amnesia of patients with alcoholic Korsakoff's disease

Archives of Neurology

The child as word learner

The episodic-semantic distinction in amnesia

Role of verbal mediation in performance of motor tasks by Korsakoff patients

Perceptual and Motor Skills

Preserved learning capacity in amnesia: Evidence for multiple memory systems

The amnesic patient H.M.: Learning and retention of a cognitive skill

Society for Neuroscience Abstracts

Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that

Science

Acquisition of motor skill after bilateral medial temporal-lobe excision

Neuropsychologia

Lasting consequences of bilateral medial temporal lobectomy: Clinical course and experimental findings in H.M.

Memory for remote personal and public events after bilateral medial temporal lobectomy

Society for Neuroscience Abstracts

Memory and the hippocampal complex

Archives of Neurology

Memory systems of the human brain: Dissociations among learning capacities in amnesia

Consequences of recent experience with forgotten words in amnesia

Society for Neuroscience Abstracts

Acquisition of perceptual skills in amnesia due to medial temporal-lobe (H.M.) and diencephalic lesions

Society for Neuroscience Abstracts

Learning and retention of computer-related vocabulary in amnesic patients: Method of vanishing cues

Journal of Clinical and Experimental Neuropsychology

Priming across modalities and priming across category levels: Extending the domain of preserved function in amnesia

Journal of Experimental Psychology: Learning, Memory and Cognition

The information that amnesic patients do not forget

Journal of Experimental Psychology: Learning, Memory, and Cognition