H.M. Revisited: Relations between Language Comprehension, Memory, and the Hippocampal System

Abstract

Three studies tested the claim that H.M. exhibits a "pure memory deficit" that has left his ability to comprehend language unimpaired relative to memory-normal controls. In Study 1, H.M. and memory-normal controls of comparable intelligence, education, and age indicated whether sentences were ambiguous or unambiguous, and H. M. detected ambiguities significantly less often than controls. In Study 2, participants identified the two meanings of visually presented sentences that they knew were ambiguous, and relative to controls, H.M. rarely discovered the ambiguities without help and had difficulty understanding the first meanings, experimenter requests, and his own output. Study 3 replicated these results and showed that they were not due to brain damage per se or to cohort effects: Unlike H.M., a patient with bilateral frontal lobe damage detected the ambiguities as readily as young and same-cohort older controls. These results bear on two general classes of theories in use within a wide range of neurosciences and cognitive sciences: The data favor "distributed-memory theories" that ascribe H.M.'s deficit to semantic-level binding processes that are inherent to both language comprehension and memory, over "stages-of-processing theories," where H.M.'s defective storage processes have no effect on language comprehension.

Semantic knowledge in patient H.M. and other patients with bilateral medial and lateral temporal lobe lesions

“…In one study, patients with HF lesions performed normally, but three MTLϩ patients were impaired . In an earlier study with similar materials, H.M. was also found to be impaired (MacKay et al, 1998b).…”

“…In contrast to these findings of preserved cognitive abilities other than memory, it was recently reported that H.M., E.P., and other patients with large medial temporal lobe lesions were impaired at detecting and explaining ambiguity in sentences (MacKay et al, 1998b;Schmolck et al, 2001;Squire et al, 2001). It is unclear how exceptional this impairment is and whether it might be part of a broader impairment in semantic knowledge.…”

“…Second, while providing definitions, he made a large number of grammatical errors. For example, he made frequent errors in the use of pronouns and referents (see also MacKay et al, 1998b). (For additional examples of difficulties unique to H.M., see Schmolck et al, 2000.…”

Neural binding mechanisms in learning and memory

“…It has been proposed that the hippocampus is specialized for processing allocentric (world centered) spatial relationships to aid flexible navigation and provides the spatiotemporal context for episodic memories (Burgess et al, 2002). Moreover, it was demonstrated that even patient H.M., thought to suffer from a pure memory deficit, had severe deficits in language comprehension as indicated by his poor ability to identify the two meanings of visually presented ambiguous sentences (MacKay et al, 1998).…”

Aging, memory, and language in amnesic H.M.

“…However, all three claims of Kensinger et al (2001) are in conflict with other evidence indicating that: (1) H.M. exhibits recent deficits in processing low-frequency (LF) words James, 2001, 2002); (2) from 1983 to 1997, H.M. exhibited exaggerated age-linked declines in processing LF words that he knew and used correctly in 1970 James, 2001, 2002); (3) H.M. exhibited syntax-level processing deficits in more than 30 sources of evidence from 1967-1973(Lackner, 1974MacKay, Burke, and Stewart, 1998a;MacKay, Stewart, and Burke, 1998b) to 1997-1999, 2002MacKay, James, Taylor, and Marian, in press).…”