BRAIN AND COGNITION 7, 1.

57-177(1988)

The Impaired Learning of Semantic Knowledge following

Bilateral Medial Temporal-Lobe Resection

JOHN D. E. GABRIELI, NEAL J. COHEN, AND SUZANNE CORKIN

Department of Brain and Cognitive Sciences and Clinical Research Center,

Massachusetts Institute of Technology

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. 0 1988 Academic PESS. h.

A major source of evidence about the neural and cognitive organization

of human memory comes from studies of patients with global amnesia,
a neurological syndrome characterized by a relatively circumscribed deficit
in learning and memory. Such patients have a marked deficit in remembering
events or materials experienced subsequent to the onset of their amnesia
(anterograde amnesia). Despite the fact-learning impairment of these pa-
tients, a number of studies have demonstrated that amnesic patients can

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, RROO088,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. Neal Cohen’s current address is Cognitive Neuropsychology
Laboratory, Departments of Psychology and Neurology, Johns Hopkins University and
School of Medicine. Send correspondence and reprint requests to John Gabrieli, MIT,
EIO-003, Cambridge, MA, 02139.
157
0278-2626188$3.00
Copyright 0 1988 by Academic Press, Inc.
All rights of reproduction in any form reserved.
158 GABRIELI, COHEN, AND CORKIN

show substantial and even normal new learning of some skills, and can
exhibit a normal influence of prior experience with an item upon later
performance with that item (i.e., repetition priming) (e.g., Milner, 1962;
Warrington & Weiskrantz, 1968, 1970; Corkin, 1968; Milner, Corkin, &
Teuber, 1968; Cermak, Lewis, Butters, & Goodglass, 1973; Brooks &
Baddeley, 1976; Cohen & Squire, 1980; Cohen & Corkin, 1981; Jacoby
& Witherspoon, 1982; Mat-tone, Butters, Payne, Becker, & Sax, 1984;
Graf, Squire, & Mandler, 1984; Cermak, Talbot, Chandler, & Wolbarst,
1985; Graf, Shimamura, & Squire, 1985). The pattern of spared and
compromised learning capacities in amnesic patients has been interpreted
by a number of investigators as suggesting that separable neural circuits
mediate the learning of different forms of knowledge; these circuits con-
stitute memory systems of the human brain (Gabrieli, 1986).
Several characterizations have been offered concerning the different
forms of knowledge that may or may not be acquired in global amnesia.
One characterization derives from Tulving’s proposal (1972) that human
memory may be divided into episodic and semantic components. Episodic
memory contains autobiographical records of personal experiences that
occurred at a particular time and place (temporal-spatial context). Semantic
memory consists of generic knowledge of the world organized in a context-
free fashion, including language, concepts, history, and the rules, as-
sociations, and principles governing such knowledge. Tulving and Schacter
(Tulving, 1983, 1984, 1985; Schacter & Tulving, 1982a, 1982b) noted that
some instances of preserved and impaired learning in amnesia are consistent
with the episodic/semantic distinction, and thus constitute a biological
source of evidence in favor of an episodic/semantic division of normal
human memory. Further, Kinsbourne and Wood (1975) proposed that
amnesic patients have neurological damage to brain structures that support
the acquisition and recall of episodic memories but not to those structures
mediating the acquisition and recall of semantic memories. Another char-
acterization of the division between impaired and spared learning in
amnesia is the declarative/procedural dichotomy (Cohen and Squire,
1980). By this view, episodic and semantic memory are seen as components
of declarative memory, and are both impaired in amnesia (Zola-Morgan,
Cohen, & Squire, 1983; Cohen, 1984; Cermak et al., 1985; Squire, 1986).
Despite this theoretical interest in the status of semantic memory in
amnesia, most studies of new fact-learning in such patients have focused
upon their failure to learn episodic information. Because few studies
have addressed the ability of amnesic patients to acquire new semantic
memories, the present experiments were designed to examine the ac-
quisition of semantic memories in the patient H.M., whose amnesia
followed bilateral resection of medial temporal-lobe structures, including
the amygdala and hippocampus (Scoville & Milner, 1957).
The few studies that considered semantic knowledge in amnesia have
 IMPAIRED SEMANTIC LEARNING 159

mainly tested explicit knowledge about public events, television programs,

and public figures (e.g., Marslen-Wilson & Teuber, 1975; Albert, Butters,
& Levin, 1979; Cohen & Squire, 1981; Cermak & O’Connor, 1983). These
studies reported uniformly that amnesic patients had impaired knowledge
about events, programs, and public figures that were experienced post-
morbidly. Thus, these results speak against a preservation of semantic
learning in global amnesia. Three caveats about these results ought to
be noted. First, most of the amnesic patients had extensive impairment
in their memory of premorbidly experienced semantic information. This
retrograde deficit obscures a straightforward interpretation of any an-
terograde impairment. Second, patients may have failed to demonstrate
acquired semantic knowledge because that knowledge was assessed ex-
plicitly by recall and recognition tests. It appears that amnesic patients
demonstrate preserved learning only when that learning is measured
implicitly via changes in performance, such as changes in sensorimotor,
perceptual, and problem-solving efficiency, or in verbal production (Cohen,
1984;Moscovitch, 1984;Gabrieli, 1986; Schacter, 1987).Third, the domains
of semantic information that were examined were not selected to provide
as pure a measure of semantic memory as possible. Tulving and Kinsboume
suggestedthat language-related knowledge is the purest example of semantic
memory. Tulving (1972) summarized semantic knowledge as “the memory
necessary for the use of language” (p. 386). Accordingly, Wood, Ebert,
and Kinsbourne (1982) proposed that, “the ultimate test [of the
semantic/episodic theory] would be to abandon an amnesic in a for-
eign country and see if he learns the language (as a child would, slowly)
but forgets having been there” (pp. 171-172).
The present experiments were designed to examine H.M.‘s anterograde
acquisition of semantic knowledge in ways that would enhance the detection
of any significant learning. The tests were chosen so that relatively intact
premorbid semantic memory could be contrasted directly with the status
of postmorbidly encountered semantic information. H.M.‘s semantic
memory was assessed, to the extent possible, by implicit measures of
performance; in no experiment was he asked explicitly to recall or recognize
any prior experiences or study-list items. The experiments were organized
to provide a broad examination of semantic knowledge, and included
the first language-related tests of semantic learning in anterograde amnesia.
Thus, examination of H.M.‘s ability to acquire several kinds of semantic
knowledge, as assessed by implicit performance measures, was intended
to discover what sort of semantic learning, if any, could be accomplished
in the face of impaired episodic learning.
EXPERIMENT 1
The tasks in Experiment 1 were designed in order to teach subjects
the meanings of eight words that are known by few people. The tasks
160 GABRIELI, COHEN, AND CORKIN

involved learning by means of definitions, synonyms, and semantic context.

It is important to note how Experiment 1 (as well as Experiments 2A,
2B, and 3) met the formal criteria for showing preserved learning in
anterograde amnesia. Learning was measured implicitly by improvement
in performance with the eight words as a consequence of prior experience
with the same material. H.M. was never asked to remember whether he
had seen the eight words before, what words he had seen before, or
what sessions, if any, had occurred previously with the eight words, i.e.,
he was never asked to recall or recognize any explicit, episodic aspect
of prior experience with the eight words.
Method
Subjecrs. H.M. and seven control subjects participated in this experiment. H.M. underwent
bilateral temporal-lobe resection in 1953, at age 27, in an attempt to alleviate his otherwise
intractable epilepsy (Scoville, Dunsmore, Liberson, Henry, & Pepe, 1953). The surgical
removal was estimated to extend 8 cm back from the tips of temporal lobes, including the
prepyriform gyrus, uncus, amygdala, hippocampus, and parahippocampal gyrus. Temporal
neocortex was reported to have been spared. H.M., who had 12 years of education, was
tested twice with these materials, in 1983 (at age 57) and in 1986 (at age 60). The seven
control subjects were men with a mean age of 53.9 years (range 46-69), whose mean years
of education was 14.8 (range 10-16).
Muteri& and procedure. The stimuli used in this experiment were eight uncommon
words: quotidian, manumit, hegira, anchorite, minatory, egress, welkin, and tyro. The test
was presented on an amber Comrex CR-5600 video screen controlled by an Apple He
microcomputer. For each word, a definition, a common single-word synonym, and a
semantically related sentence frame were developed. Testing consisted of three phases.
In Phase 1, each uncommon word was presented individually with a single definition. The
subject was asked to read each word and definition aloud, and was warned that he would
be tested on the material. Then, the uncommon words were presented individually at the
bottom of the screen, below the eight definitions. The subject had to select the correct
definition. If the subject made a correct choice, that definition was removed from the
display, and the next uncommon word appeared. If the subject made an incorrect choice,
the examiner pointed out the error and the subject had to select another definition. This
procedure continued for each word until the correct definition had been selected. If the
subject made any error in the set of eight word-definition selections, another set of eight
word-definition selections occurred. The subject had to meet a criterion of matching all
eight words in a set to their correct definitions before going on to Phase 2. In Phase 2,
the subject was presented with the same eight words, one at a time, and with a common,
single-word synonym. Again, he was warned that he would be tested on the synonyms.
Then he saw one test word appear below a display of the eight synonyms, and had to
select the correct synonym. As in the definitions test, correct answers were removed from
the choice list, and the examiner informed the subject of all incorrect responses. The
subject had to match all eight words with their synonyms within a single set in order to
complete the synonym-test phase. In Phase 3, the subject saw all eight uncommon words
in a display appearing above a single sentence in which a word was missing. The semantic
content of the sentence frame indicated which word would best complete the sentence. If
the subject selected the correct word, that word was removed from the set. If the subject
selected an incorrect word, he was informed of the error and asked to select another word.
He had to select all eight words in a set correctly for testing to end; an error in a set led
to another set of sentence completions.
 IMPAIRED SEMANTIC LEARNING 161

Results
For each phase of the test, performance was analyzed in three ways:
trials-to-criterion, total errors, and mean errors per trial (Table 1). H.M.
did not reach criterion on any phase; testing was aborted after 20 trials
in each phase. H.M. showed some meager learning, with his errors and
errors per trial decreasing across the phases. The minor learning shown
by this amnesic patient, however, should not obscure the major deficit
that he had in learning the meanings of the eight words. The magnitude
of H.M.‘s deficit is underestimated, because testing was aborted in each
phase.
For further analyses, the 1986 results were scrutinized because only
the summary numbers were saved from the 1983 sessions. It is clear
that H.M.‘s extensive training in 1983 provided no benefit in 1986. In
1986, if H.M. had continued to reduce his errors per trial at a consistent
rate, his estimated number of trials to achieve the criterion reached by
normal subjects in 7.3 trials would have been 335.
The possibility that H.M. learned some words but not others was
considered. H.M. apparently knew the meaning of “tyro,” because he
selected the correct definition and synonym every time, and the correct
sentence on 18 of 20 trials. However, he never mastered the meaning
of any other word and his errors per word on the final phase ranged
from 20 for “egress” to 50 for “anchorite,” averaging at least one error
for each presentation of every word except “tyro.”
A second source of failure was considered, namely that H.M. was
confused by the large number of choices (eight) at the beginning of each
trial. If H.M. had been affected by the sheer number of choices, he
should have performed more accurately, relative to chance, as the selections
were removed after each correct answer and chance moved from .I25
(one of eight choices) to .50 (one of two choices). In fact, the ratio of
errors to chance performance did not change as a function of reduced
multiple choices, holding nearly steady at .68 (eight-choice) to .65 (two-
choice) in the definition phase, .61 to .57 in the synonym phase, and .68
to .65 in the sentence phase. Thus the probability of H.M.‘s selecting a
correct answer was not affected by the number of choices.
Discussion
The results provided unequivocal evidence that H.M. could not learn,
in a laboratory setting, the meaning of any word that he did not already
know. H.M.‘s failure to learn the meaning of a word after an average
of 106 training trails per word (in 1986) is reminiscent of his inability to
learn a seven-digit series despite 25 consecutive presentations (Drachman
& Arbit, 1966), a visual stylus maze after 215 trials (Milner, 1965), or a
tactual stylus maze after 80 trials (Corkin, 1965). The earlier experiments
involved recall for nonmeaningful material, and the present experiment
162 GABRIELI, COHEN, AND CORKIN

TABLE 1
H.M.‘s IMPAIRED PERFORMANCEON WORD LEARNING TEST

Experimental Error
Subjects phase Trials-to-criterion Errors per Trial
Control Definitions 3.1 (2.3) 3.1 (4.2) 0.7 (0.8)
Synonyms 1.6 (2.2) 0.9 (1.9) 0.3 (0.5)
Sentences 2.6 (1.3) 2.4 (2.1) 0.7 (0.5)
Total 7.3 (4.0) 7.0 (7.1) 0.7 (0.6)
H.M. (1983) Definitions 20 252 12.6
Synonyms 20 253 12.7
Sentences 20 213 10.7
Total 60 718 12.0
H.M. (1986) Definitions 20 287 14.4
Synonyms 20 227 11.4
Sentences 20 224 11.2
Total 60 738 12.3

” Standard deviation.

multiple-choice recognition for meaningful material. H.M. benefitted neither

from the change in method of testing nor from the greater meaningfulness
of the stimuli. Amnesic patients, including H.M., have shown good learning
on tasks involving multiple repetitions of mirror-tracing, rotary pursuit,
and hard-to-perceive figures and words (e.g., Milner, 1962; Corkin, 1968;
Mimer et al., 1968; Warrington & Weiskrantz, 1968, 1970; Cermak et
al., 1973; Brooks & Baddeley, 1976; Cohen & Squire, 1980). Because
H.M. did not benefit from the multiple repetitions of the digit series,
maze routes, or word meanings, the conclusion is that multiple repetitions
per se do not underlie preserved learning for motor and perceptual skills
in amnesia, as pointed out by Cohen (1984). Rather, there is something
qualitatively different between the classes of knowledge that an amnesic
patient can and cannot learn, and rote learning of a word’s meaning falls
into the impaired class of knowledge. Finally, H.M.‘s failure to learn
the meaning of even one word despite such extensive training may be
contrasted with the language acquisition skills of children: Between the
ages of 2 and 5, the average child learns the equivalent of nine new
words a day (Carey, 1978).
The poor vocabulary learning by H.M. may appear to contradict results
reported by Glisky, Schacter, and Tulving (1986). They found that four
amnesic patients (three of whom developed amnesia after closed-head
injuries and one after viral encephalitis) could acquire computer-related
vocabulary. Although these patients did learn the meanings of computer
terms, they did so at a significantly impaired rate. Glisky et al. pointed
out that their vocabulary training procedure optimized learning because
 IMPAIRED SEMANTIC LEARNING 163

the terms were already familiar to the patients (e.g., save, run, boot),
the terms related to their meaning (e.g., catalog-a disk’s table of contents),
and there were multiple relations among terms and meanings taken from
the same domain of computer terminology. Despite the optimal learning
conditions, those patients were still impaired relative to normal control
subjects. Thus, no matter how favorable the circumstances for learning
word meanings, patients who are impaired at acquiring episodic knowledge
are still impaired at learning the meanings of words. Furthermore, another
amnesic patient with Korsakoff’s syndrome participated in Experiment
1, and she too performed far worse than any control subject (although
somewhat better than H.M.) (Gabrieli, 1986). Consequently, failure to
learn the meaning of obscure words seems to be linked inextricably to
impaired episodic learning, irrespective of the etiology of the amnesia.
To the extent that learning word meanings constitutes an example of
semantic learning, the results of the present experiment and those reported
by Glisky et al. indicate that impaired semantic learning is an obligatory
concomitant of impaired episodic learning. Rote teaming of word definitions,
however, may be viewed as an example of paired-associate episodic
learning. Experiments 2A, 2B, and 3 were conducted in order to probe
more fully H.M.‘s semantic memory.
EXPERIMENT 2A
The strength of Experiment 1 was that exhaustive presentation and
testing of semantic knowledge was conducted in a strictly controlled
fashion. It was possible, however, that H.M.‘s semantic acquisition abilities
might not have been engaged ecologically in the experimental paradigm
and thus might have been intact but unexpressed. People normally learn
the meaning of new words in their language in entirely different circum-
stances from those present in the laboratory. The circumstances often
include exposure to an initially unknown word in a variety of meaningful
contexts, in a number of separated episodes, and in the course of motivated
experiences, i.e., people see or hear the word in pursuit of a goal. In
fact, several studies have shown that the powerful mechanisms subserving
language acquisition in children are not engaged if children are drilled
so as to learn semantic values of nonsense words (reviewed in Carey,
1978). It therefore became important to discover whether H.M. had
acquired some knowledge of words that were new to the English language
since his operation in 1953, and that he may have encountered in daily
life. Furthermore, it was of interest to probe H.M.‘s knowledge of new
words at various levels. H.M.‘s semantic knowledge was examined in
tests of recall and recognition of word definitions; the latter permitted
him to demonstrate an existent but impoverished knowledge of the meaning
of new words. Also assessedwas H.M.‘s lexical knowledge (the knowledge
that a string of letters consititutes a real word in the English language)
164 GABRIELI, COHEN, AND CORKIN

of words that came into the language after 1953. It was possible that
H.M. knew that a new word was a real word without knowing the
meaning of that word; this experience occurs in healthy people. Thus,
H.M.‘s lexical knowledge could have grown independently of his semantic
knowledge for the same material. In addition, H.M.‘s ability to perceive
and pronounce new words was examined.
Method
Subjects. H.M. and seven male normal control subjects took the recall and recognition
vocabulary tests. The control subjects’ mean age (53.4 years, range 46-63 years) and years
of education (mean 13.0, range 10-16) were comparable to H.M.‘s (age 57, and 12 years
of education). H.M. and four of the control subjects (mean age, 56.7; mean years of
education, 12.0) also took the lexical decision test.

Materials and Procedure

The lexical decision test was given on a Comrex CR-5600 amber video screen controlled
by an Apple Be microcomputer. The recall and recognition tests were administered in
paper-and-pencil format.The critical test stimuli were 45 words (new words) added to the
Merriam-Webster Dictionary in supplements published in 1954 (17 words), 1959 (1 word),
1966 (5 words), 1971 (8 words), 1976 (9 words), and 1981 (5 words). Examples of new
words were charisma, psychedelic, granola, jacuzzi, and palimony. These words were
chosen so as to be suitable for lexical decision and definition tests according to two criteria:
(a) that each was sufficiently common that normal control subjects with a high school
education could demonstrate lexical and semantic knowledge of the words in the performance
tests; and (b) that neither the meanings of the words nor the fact that they were real words
in the English language could have been deduced logically by analysis of the apparent root
or components of the word. The 45 words that met these criteria were used in the lexical
decision, recall, and recognition phases of the experiment, in that order. In addition, H.M.
was given recall and recognition tests of definitions of words and phrases not suitable for
lexical decision, e.g., angel dust, closet queen, cut-offs.
Lexical decision. For every one of the 45 new words (new to the dictionary since 1953),
4 old words of equal letter length were selected. Two of the old words were high frequency
@O/million or higher) and 2 were low frequency (l/million) (Kucera & Francis, 1%7). For
every such set of 4 old words, 1 of the high-frequency and 1 of the low-frequency words
were converted into pronounceable pseudowords (nonwords) by replacing one vowel and
one consonant with another vowel and consonant. Thus, five sets of 45 items were sys-
tematically generated: new words, old words of high frequency, old words of low frequency,
pseudowords derived from old high-frequency words, and pseudowords derived from old
low-frequency words. The items were then assigned pseudorandomly to positions in five
blocks with the following constraints: All blocks contained the same number of items from
each of five sets, the blocks contained the same average word length, there were never
more than 5 words or nonwords in a row, and there were never more than 3 items from
the same set in a row. A practice set of 24 items preceded the test. It comprised old
words, including 6 high-frequency and 6 low-frequency words, and 12 pseudowords generated
as above. At the beginning of the experimental session, the subject was instructed to decide
as quickly and accurately as possible whether a string of letters constituted a real English-
language word. He was told that this test was not meant to be a diicult spelling test and
to treat slang words as words. The response was a two-choice reaction time measure: The
subject pressed a button on the keyboard with his right hand if the answer for a probe
was yes, and another button with the left hand for no. Two cards, with the words “Yes”
and “No” on them, remained above the appropriate keys throughout the testing session.
 IMPAIRED SEMANTIC LEARNING 165

On every trial, the subjects heard a warning signal. One second later, the following display
appeared in the center of the video screen: IS THE FOLLOWING A REAL WORD?
After 500 msec, the probe item appeared in the center of the screen in capital letters. The
probe remained on the screen until the subject responded, and then it disappeared. Three
seconds intervened between the disappearance of the probe and the succeeding warning
signal. A I-min rest period followed after every 45 probes. The entire testing session lasted
about 40 min.
Recall of word definitions. Two tests demanding recall of word meanings were given.
The Vocabulary subtest of the Wechsler Adult Intelligence Scale-Revised (WAIS-R) was
administered in the standard fashion (Wechsler, 1981), whereby the examiner said each
word aloud and asked the subject to provide a definition orally. All of the 35 words had
been in the language well before 1953. A recall test for the 45 new words seen in the
lexical decision test was given in an identical fashion, except that the subject saw and
heard every word.
Recognition of word de$nitions. The subject received a recognition test for the same 45
new words seen in the lexical decision and recall tests. For each new word, the subject
had to select the correct definition from among four multiple choices. The test words and
multiple choices were presented in a booklet; prior to selecting each answer, the subject
heard each word read aloud.

Results
It is likely that some or all of the words that entered the dictionary
during the 1950s were in common usage prior to H.M.‘s operation. Thus,
for all analyses, the 45 new words were divided into two sets: words
that entered the dictionary during the 1950s (around the time of H.M.‘s
operation) and words that entered the dictionary after 1960 (well after
H.M.‘s operation in 19.53).H.M.‘s scores were designated “normal” if
they were within one standard deviation of the mean score of the normal
control subjects; “borderline” if they were more than one but less than
two standard deviations below the mean of the normal control subjects;
and “markedly impaired” if they were inferior by more than two standard
deviations (Table 2).

Recall of Word Dejinitions

For both the WARS-R Vocabulary subtests and the 45 new words, a
definition received two points if it was a good definition, and one point
if it was a poor definition that nevertheless revealed some sense of the
word’s meaning. Recall for the WAIS-R Vocabulary subtest was scored
as a percentage of the perfect score of 70, and for the 45 new words as
a percentage of the perfect scores of 36 for the 1950s words, and of 54
for the post-1950s (P&OS, 197Os,1980s)words. H.M. demonstrated normal
recall of definitions for the pre-1950 words, a borderline deficit for recall
of the 1950s words, and a marked impairment for recall of the post-1950s
words (Table 2).
166 GABRIELI, COHEN, AND CORKIN

TABLE 2
DIFFERENTIAL WORD KNOWLEDGE AT THREETIME PERIODS

Time period

Task Pre- I 950s 1950s Post-1950s

Recall of definitions
NCS 67.1 (15.3)” 70.6 (18.3) 57.2 (14.0)
H.M. 61.4 38.9 13.9
Recognition of definitions
NCS - 92.8 (7.6) 83.1 (10.4)
H.M. - 55.6 37.0
Lexical decision on words
NCS 92.2 (3.0) 82.0 (10.6) 76.5 (10.8)
H.M. 93.0 70.6 50.0

” Standard deviation.

Recognition of Word Definitions

The results for the recognition test with the definitions of the 45 new
words were calculated as a percentage of perfect scores of 18 for the
1950swords and 27 for the post-1950swords. Chance performance consisted
of a 25% score. H.M. showed markedly impaired recognition for the
meaning of words that entered the dictionary after his operation (Table
2).

Lexical Decision Test

The lexical decision data were scored as percentage correct responses,
i.e., “yes” responses for words and “no” responses for nonwords.
H.M.‘s ability to categorize nonwords as nonwords was borderline; he
scored 87.7% as compared to the control group’s mean score of 94%
(SD = 3.1). For identification of pre-1950s words as words, H.M.‘s score
was normal. H.M.‘s ability to recognize a word that entered the dictionary
after his operation as a word per se was borderline for the 1950s and
markedly impaired from 1960 onward (Table 2).

EXPERIMENT 28
H.M. showed normal learning when asked to reread words aloud that
were presented in a perceptually difficult condition (Gabrieli, Merrill, &
Corkin, 1986). That same perceptually difficult condition was used for
presentation of the new words, old words, and nonwords shown in the
lexical decision experiment. H.M. was asked to read the words aloud
as soon as he could perceive them. His knowledge of the new words
was measured by contrasting his speed of perceiving and reading the
new words versus the nonwords.
 IMPAIRED SEMANTIC LEARNING 167

Method
Subjects. H.M. and one normal control subject, matched by sex, age (59 years to H.M.‘s
60 years), and education (12 years for both subjects).
Materials and procedure. The stimuli were those used in the lexical decision task of
Experiment 2A, presented in the same order as before. An additional block with 9 new
words, 9 high-frequency words, 9 low-frequency words, and 18 nonwords was added; this
block had the same structure as the earlier blocks (Experiment 2A). The stimuli were
presented in large, J-in. graphic letters. A stimulus appeared initially such that 70% of the
display was obscured by a field, or blanket, of randomly placed dots (or noise). Pilot
studies had shown that no subject could read the stimulus correctly with 70% noise. The
noise was removed slowly in 60 equal steps of 1.2% per step so that after 15 set the word
appeared without any noise. The subject was seated 1 m from the monitor and was asked
to read aloud the word or nonword as soon as he could. Upon a correct reading, the
examiner pressed a key that recorded the time to read correctly. Each stimulus stayed on
until the subject read it. Answers were recorded to the nearest second.

Results
The mean times to read sets of words correctly were calculated; the
sets were (a) high-frequency words, (b) low-frequency words, (c) nonwords,
(d) 1950s words, and (e) post-1950s words. The normal control subject
averaged 5.4 set for the high-frequency words to H.M.‘s 5.1 set, 6.1
set to 9.2 set for low-frequency words, 7.8 set to 13.6 set for nonwords,
6.7 set to 11.4 set for 1950s words, and 6.5 set to 14.8 set for post-
1950s words. The control subject was 17% faster in reading new words
(6.5 set) than nonwords (7.8 set), but H.M.‘s speed of identification of
the new words (13.7 set) and nonwords (13.6 set) was almost equal.
Thus, by this measure of semantic knowledge of new words, a measure
that included perceptual identification and pronunciation, H.M. showed
no knowledge whatsoever of the new words.
EXPERIMENT 3
A second realm of semantic memory that could have been spared in
H.M. is knowledge of the names of famous people. Knowledge of this
sort is partially linguistic (names) and partially dependent upon experience
with world events. A minimal expression of knowledge for the names
of famous people would be the ability to recognize a famous name as
such. This capacity is somewhat analogous to recognition of a word as
a word (lexical decision). The participants in Experiment 3 were asked
to decide whether a name they saw was that of a famous person; half
of the names were those of famous people and half were those of nonfamous
people.
A reason to hypothesize that H.M. would do well on such a test was
his ability to recognize public figures from news photographs (Marslen-
Wilson & Teuber, 1975). H.M. and control subjects were tested for their
unprompted and prompted recognition of public figures who had become
famous in each decade from the 1920s through the 1960s. The subjects
168 GABRIELI, COHEN, AND CORKIN

were asked first to identify the faces of famous people without prompts.
H.M. correctly identified people who came to fame prior to the onset
of his amnesia (in the 192Os, 193Os,and 1940s) with normal accuracy.
He was impaired, however, in identifying the faces of people who became
famous after his operation, in the 1950s and 1960s. Subjects were also
provided semantic and phonemic prompts for the public figures whom
they had been unable to identify. With these cues, H.M.‘s performance
improved so that he identified correctly 80% of the figures who became
prominent after the onset of his amnesia. Tulving (1984) and Weiskrantz
(1985) have pointed out that H.M.‘s good performance is suggestive of
preserved acquisition of postmorbidly experienced semantic knowledge.

Method
Subjects. H.M., aged 57, and four male normal control subjects (mean age, 51.O years,
mean years of education, 14.1) participated in this experiment.
Mzferials and procedure. The stimuli were names of people who had come to fame
between 1930 and 1983. Four names were selected in each of five career categories (movie
stars, athletes, American politicians, foreign leaders, and writers) for each of six decades
(193Os, 194Os,195Os, 1960s 197Os,and 198Os),giving a total of 120 famous names. Some
of the criteria used in assigning the decade in which a person came to fame were as follows:
movie stars were assigned to the decade in which they first received an Academy Award
(Oscar) nomination; authors to the decade in which they first received a Pulitzer Prize;
baseball players to the decade in which they first won any sort of batting title or most
valuable player award; football players to the decade in which they received a Heisman
Trophy as the outstanding collegiate player; tennis players to the decade in which they
first won a Grand Slam tournament; and boxers to the decade in which they won a title.
For each famous name, a nonfamous name was selected from the Boston area telephone
book that matched the ethnic quality of the famous name. The famous and nonfamous
names were randomly assigned to four blocks of trials with the following constraints: Each
block contained an equal number of famous and nonfamous names; there were never more
than 3 famous names from the same category or decade in a row; and within each set of
30 there was one famous name from each category and decade. A practice set given prior
to the test consisted of the names of 12 people who were famous before 1920 and 12
nonfamous names. The subject was instructed to decide as quickly and as accurately as
possible whether the name he saw was that of a famous person. It was also explained
that the task was not to decide whether a familiar name was well known enough to qualify
as famous, but rather to rate any familiar name as famous so long as it was not the name
of a personal acquaintance. If the name was that of a famous person, the subject pressed
a key with his right hand; above the key was a card with the word “Yes.” If the name
was not that of a famous person, the subject pressed another key with his left hand: above
that key was a card with the word “No.” An auditory warning signal preceded each trial.
One second later, the following display appeared at the top of the computer screen: IS
OR WAS THE FOLLOWING A FAMOUS PERSON? After 500 msec, a name appeared
in capita1 letters in the center of the screen. After the subject’s response, the name
disappeared and 3 set elapsed before a warning signal initiated the next trial.

Results
H.M.‘s ability to reject nonfamous names (72.3% correct) was com-
parable to the performance of the normal control group (mean = 81.4%,
 IMPAIRED SEMANTIC LEARNING 169

SD = 13.7). Identification of famous names was scored by decade.

H.M.‘s identification of people who came to fame in the 1930sand 1940s
(premorbidly) was normal (87.5% versus control group mean score of
84.2%, SD = 14.7). For people who came to fame during the 195Os,
however, H.M.‘s score of 70% was one standard deviation (13.8) below
the 81.3% mean percentage correct of the control group. Finally, for
people who came to fame in the 1960s 1970s and 1980s and who were
almost certainly unknown to H.M. premorbidly, his 53.3% performance
was about two standard deviations (14.1) below the 80% mean percentage
correct of the normal control group.
Discussion
There appears to be some contradiction between H.M.‘s impaired
recognition of names of people who became famous after his operation
and his ability to provide the names of famous people when prompted
(Marslen-Wilson & Teuber, 1975). Both tests probed for the maximal
expression of minimal knowledge of the names of public figures. In order
to reconcile this apparent paradox, we examined retrospectively H.M.‘s
performance on two later administrations (1977 and 1980) of Marslen-
Wilson and Teuber’s test involving recognition of public figures from
news photographs (Sullivan & Corkin, unpublished data); this test also
included 14 new photographs of people who became well known in the
1970s (Moon & Corkin, unpublished data). We also examined the scores
of three normal subjects (mean age, 48 years) tested in the same time
period. H.M.‘s percentages of correct identification (without prompts)
on the two later test administrations were similar to his percentages from
the two administrations reported earlier by Marslen-Wilson and Teuber:
64% (earlier) versus 53% (later) for the 1920s 1930s and 1940s; 8%
versus 8% for the 1950s and 1960s; and 0% for the 1970s (not previously
shown to H.M.). The pattern of intact memory of public figures from
his premorbid period and impaired memory for such figures from his
postmorbid period was again evident. As in the Marslen-Wilson and
Teuber procedure, the subjects attempted to identify the famous people
without prompts, then received semantic prompts for people not identified,
and then phonemic prompts for people not identified with semantic prompts.
The semantic prompts provided a number of facts about the unidentified
famous person (e.g., for Alfred Landon “He was the Republican pres-
idential nominee in 1936; he ran against Roosevelt and lost; he was also
governor of Kansas.“) The phonemic prompts provided an increasing
number of letters in the first and then last names of the public figures,
moving from initials and ending with almost the whole name provided
until the subject could produce the correct name. For Alfred Landon
the phonemic cues were “A.L., Alf. L, Alfred L., Alfred Lan., Alfred
Land.”
170 GABRIELI, COHEN, AND CORKIN

Unlike Marslen-Wilson and Teuber, we scored the semantically and

phonemically prompted identifications separately, each as a percentage
of possible figures identified by that type of cue. H.M. used the semantic
prompts as effectively as did the normal subjects for his premorbid period
(1920-1940s): He correctly identified 28% of the public figures versus a
mean of 35% (SD = 12) for the normal subjects. His successful use of
semantic prompts for figures in the 195Os-1970sfell to 2%, whereas the
normal subjects scored a higher 21% (SD = 8). Thus, H.M.‘s semantic
knowledge of the faces and names of public figures from the time after
his operation was as impaired as the results of Experiment 3 suggested.
Indeed, H.M.‘s use of semantic prompts was almost totally impaired for
post-1950s public figures: On the two later test occasions, he identified
only 2 of 95 public figures from the 195Os-1970s period with the aid of
semantic prompts. These two were Mao Tse Tung, a 1960s figure in the
test who became the leader of China in 1947 (the first semantic prompt),
and Lyndon Baines Johnson, who had been active in national politics
since the late 1940s. It is difficult, therefore, upon close retrospective
examination of these data, to conclude that H.M. successfully encoded
and stored semantic information. The result of this reanalysis corresponds
closely with a detailed study that demonstrated H.M.‘s severely impaired
knowledge of postmorbid public events (Corkin, Cohen, & Sagar, 1983).
GENERAL DISCUSSION
The main results of Experiments 2A, 2B, and 3 were that H.M. was
normal on several measures of premorbid semantic knowledge, moderately
impaired on semantic knowledge from the 1950s and severely impaired
on semantic knowledge from 1960 onward. On four separate measures,
H.M.‘s scores declined steeply across time periods relative to the mean
scores of the control subjects (Fig. 1). The more moderate impairment
in knowledge from the 1950s may have resulted from the prevalence of
some of that knowledge in the 1940s. Because this possibility is difficult
to evaluate, this discussion will focus on the contrast between H.M.‘s
memory for permorbidly known words and names and the post-1950s
words and names, which he probably encountered only after the onset
of his anterograde amnesia.
H.M. demonstrated impaired knowledge of semantic information that
entered society’s knowledge after 1960, i.e., after the onset of his an-
terograde amnesia. The question remains as to whether H.M.‘s semantic
memory reflects having experienced the last 32 years at all. There are
several items of evidence that argue against such an absolute amnesia.
First, H.M.‘s recall and recognition of word definitions for post-1950s
words were better than chance. Second, his performance on the lexical
decision and name categorization tasks demonstrated some knowledge
of post-1950s words and names. If H.M. treated post-1950s words as
 IMPAIRED SEMANTIC LEARNING 171

0 ’ I I I
prel9505 1950s pos119505
Time Period

FIG. 1. H.M.‘s scores on four tests of semantic knowledge from three time periods;
the scores are calculated as percentages of the mean scores of the normal control subjects
(NCS) in Experiments 2A and 3.

nonwords, he should have categorized only 12% of post-1950s words as

words (his false positive rate for nonwords), whereas his actual rate of
correct verification was over four times that (50%). The same logic applies
to the name categorization task, in which H.M.‘s correct response rate
(53%) was about twice his rate of falsely categorizing nonfamous names
as famous (28%). It should be noted, however, that some of H.M.‘s
relatively good performance on those two tasks may have been due to
the nature of the nonwords and nonfamous names. Although the nonwords
were constructed to be pronounceable, the orthographic character of the
nonwords was almost certainly less like that of true English than were
the new, actually English, words. Consequently, cues may have been
provided that bolstered H.M.‘s performance on the new words. Similarly,
the nonfamous names could not be randomly generated, and they may
also have provided subtle clues. The effect of these possible problems
in controlling stimuli was likely to be small, however, so that H.M.‘s
better than chance scores ought not to be dismissed as artifactual. Thus,
the results indicate some changes in H.M.‘s semantic knowledge since
1953; these changes are, however, small relative to normal subjects.
It is likely that the limitations placed upon his daily life by his amnesic
condition reduced H .M’s exposure to new, common knowledge, but there
is reason to doubt this explanation of H.M.‘s impaired scores. H.M. has
spent considerable time watching television, a major source of such
information. Because he has been unable to work since his operation,
it is likely that H.M. was exposed to more television than the age-matched
control subjects. One would therefore have expected him to know the
names of popular public figures whom he has seen and heard about often
on television. Yet, H.M. classified such names as John Travolta, Sylvester
172 GABRIELI, COHEN, AND CORKIN

Stallone, Ivan Lendl, Bjorn Borg, Roger Maris, and Roger Staubach as
nonfamous names. These actors and sport figures have appeared frequently
on television over a number of years. Furthermore, H.M. is usually
unable to name the current President of the United States, probably the
most frequently mentioned name on the airwaves. Another variable that
may have affected H.M.‘s performance is a mild difficulty with language
that has become apparent in recent years (Corkin, 1984). This difficulty
has remained small relative to his memory disorders, did not appear to
affect his facility with verbal premorbid semantic knowledge in the present
experiments, and has not precluded him from demonstrating preserved
learning abilities on verbal tasks (Gabrieli, 1986). In sum, H.M.‘s sheltered
life and mild language difficulties may have contributed somewhat to his
impaired performance, but it appears unlikely that these factors could
account for the steep gradient of impaired semantic knowledge shown
in Fig. 1.
The interpretation of H.M.‘s impaired but above-chance scores could
follow two divergent paths. The first path would lead to the conclusion
that the above-chance scores indicated significantly, but not completely,
preserved anterograde semantic learning in H.M. The second path would
arrive at the opposite conclusion, arguing that although H.M. showed
some postmorbidly acquired semantic knowledge, his consistent impairment
indicates that the ability to acquire semantic and episodic knowledge
were both disrupted by the surgical resection in 1953. This conclusion
would suggest an association between semantic and episodic learning,
rather than a dissociation. H.M.‘s better-than-chance postmorbid scores,
then, reflected frequent and rich exposures to postmorbid semantic
knowledge, via television, radio, and magazines, rather than a preserved
learning capacity. Despite the relative ecological validity of the stimuli,
H.M. was impaired and was as likely to call a new word a nonword as
he was to call it a word, and as likely to categorize a famous name as
a nonfamous name as he was to call it a famous name. Finally, when
H.M. had to combine two tests with new words (Experiment 2B), per-
ception and pronunciation, he actually showed no advantage whatsoever
for new words over nonwords. Thus, the more semantic knowledge a
task demanded, the less likely H.M. was to score above chance. H.M.‘s
meager postmorbid learning of semantic knowledge contrasts with the
substantial and sometimes normal learning he has exhibited on other
tasks (e.g., Corkin, 1968; Milner et al., 1968; Cohen & Corkin, 1981;
Nissen, Cohen, & Corkin, 1981; Gabrieli, Cohen, Huff, Hodgson, &
Corkin, 1984; Gabrieli et al., 1986; Keane, Milberg, Cronin-Golomb,
Gabrieli, & Corkin, 1986).
The conclusion of the present study is in agreement with prior studies
with other patients (e.g., Albert et al., 1979; Cohen & Squire, 1981;
Cermak & O’Connor, 1983) that found a deficit in amnesic patients’
 IMPAIRED SEMANTIC LEARNING 173

postmorbid semantic knowledge. The consistency of this finding raises

the question of how studies with amnesic patients pertain to Tulving’s
suggestion that normal memory is divisible into episodic and semantic
components. In theory, amnesic patients could have shown a clear dis-
sociation between the two kinds of memory: preservation of semantic
learning together with an impairment in episodic learning. In fact, such
patients have shown a deficit in learning both kinds of information.
Impaired semantic and episodic learning are correlated in anterograde
amnesia, and studies with amnesic patients provide no evidence that the
two kinds of learning are dissociable. The presence of meager semantic
learning in H.M. is also difficult to evaluate in relation to the epi-
sodic/semantic dichotomy. That learning could be accounted for either
by the relative frequency and richness of episodes in which semantic
information is encountered, or by the hypothesized fundamental difference
between the two kinds of memory. This difficulty in interpretation is the
same one faced by those examining the episodic/semantic distinction in
normal human memory. Thus, studies with amnesic patients have not
offered clarifying evidence vis-a-vis the episodic/semantic dichotomy,
and certainly do not constitute a neurological validation of the dichotomy.
At the same time, the studies of amnesic patients do not necessarily
contradict an episodic/semantic distinction in normal human memory.
Episodic and semantic memory could be different kinds of memory that
share one common component or one kind of interdependence. It may
be, for example, that episodic memory plays a role in the ontogeny of
semantic memory, and that an impairment in anterograde episodic learning
disrupts anterograde semantic learning. In such a scheme, already acquired
episodic and semantic memories could be dissociable (but see Cermak,
1984, for a different view). Because both sorts of learning are impaired
in amnesia, however, such a dissociation would not be evident in amnesic
patients.
Although studies of H.M. and other amnesic patients do not provide
evidence in favor of a division between episodic and semantic memory,
it is worth considering how current versions of the episodic/semantic
distinction map onto the pattern of impaired versus spared memory abilities
in amnesia. Tulving’s more recent formulations (1983, 1984, 1985) have
defined episodic memory as a subsystem of procedural memory. In par-
ticular, Tulving has placed skill learning and, perhaps, repetition priming
outside of semantic memory, and has considered excluding from semantic
memory knowledge of words (referred to as lexical memory). The present
results suggest that lexical memory must indeed be excluded from semantic
memory if one is to argue that the learning preserved in amnesia derives
from an intact semantic memory system. With these exclusions and the
present results, however, it is unclear what evidence remains strongly
in favor of preserved semantic learning in amnesia.
174 GABRIELI, COHEN, AND CORKIN

Kinsbourne (1987) has redefined episodic and semantic memories as

processes rather than forms of knowledge. Episodic memories, by his
current account, are the reexperiencing of a previous experience. He
has redefined semantic memory as performance modified by previous
experience, a definition that includes skill learning and repetition priming
as examples of semantic learning. Kinsbourne has greatly expanded Tulv-
ing’s original conception of semantic memory, so that it can now include
all preserved learning phenomena in amnesia. One way of viewing this
redefinition is that Kinsbourne incorporates procedural memory within
the notion of semantic memory, in contrast to Tulving who has incorporated
semantic within procedural memory, and to others who have identified
semantic memory as part of the declarative system in the declara-
tive/procedural framework (Cohen, 1984; Cermak et al., 1985; Squire,
1986). The present results, however, pose problems for Kinsbourne’s
reformulation. All of the capacities reported here as being impaired in
H.M., including defining, pronouncing, perceiving, and making lexical
decisions about words, would have to be interpreted as requiring the
reexperiencing of previous experiences by normal subjects. This possibility
seems counterintuitive and makes it difficult, if not impossible, to know
what tasks, in principle, require the reexperiencing of previous experiences.
While the present results do not contradict Tulving’s or Kinsbourne’s
current versions of the episodic/semantic distinction, the changes in
definitions of episodic and semantic make it difficult to see what empirical
results could provide confirmatory or disconfirmatory evidence about the
episodic/semantic distinction as a descriptive or explanatory theory of
preserved and impaired learning in amnesia.
Returning, finally, to the question of whether an amnesic patient, if
placed in a foreign country, would learn the language but forget having
been there (Wood et al., 1982), it appears instead that H.M.‘s impaired
acquisition of semantic knowledge has made modem-day English a partially
foreign language for him. When attempting to recall or recognize the
meanings of post-1950s words, H.M.‘s errors appeared similar to what
one would expect from a foreigner with schoolbook knowledge of English
when confronted with colloquial terms: He attempted to construe meanings
from the literal components of words and phrases. For example, H.M.
defined, spontaneously, “acid rain” as a “heavy rain,” “biodegradable”
as “two grades, ” “closet queen” as “moths,” “flower child” as “a
young person who grows flowers,” and “soul food,” as “forgiveness.”
H.M.‘s anterograde amnesia, which includes a deficit in learning semantic
knowledge, has rendered him an alien in his own land and time.
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