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Neuropsychology In the public domain

2014, Vol. 28, No. 6, 973983 http://dx.doi.org/10.1037/neu0000112

Repetition Priming of Words and Nonwords in Alzheimers Disease and


Normal Aging
Beth A. Ober and Gregory K. Shenaut
University of California, Davis and Veterans Affairs Northern California Health Care System, Martinez, CA

Objective: This study examines the magnitude and direction of nonword and word lexical decision
repetition priming effects in Alzheimers disease (AD) and normal aging, focusing specifically on the
negative priming effect sometimes observed with repeated nonwords. Method: Probable AD patients
(30), elderly normal controls (34), and young normal controls (49) participated in a repetition priming
experiment using low-frequency words and word-like nonwords with a letter-level orthographic orienting
task at study followed by a lexical decision test phase. Results: Although participants reaction times
(RTs) were longer in AD compared with elderly normal, and elderly normal compared with young
normal, the repetition priming effect and the degree to which the repetition priming effect was reversed
for nonwords compared to words was unaffected by AD or normal aging. Conclusion: AD patients, like
young and elderly normal participants, are able to modify (in the case of words) and create (in the case
of nonwords) long-term memory traces for lexical stimuli, based on a single orthographic processing
trial. The nonword repetition results are discussed from the perspective of new vocabulary learning
commencing with a provisional lexical memory trace created after orthographic encoding of a novel
word-like letter string.

Keywords: memory, implicit memory, lexical decision, reaction time (RT), nonword familiarity

There has been considerable interest in repetition priming to make yes/no recognition judgments for previously seen and
defined as faster or more accurate processing of a repeated stim- foil items; these paradigms are explicit tests of memory. Dissoci-
ulus due to its prior processingin elderly normal (EN) and ations between repetition priming and episodic/event memory per-
probable Alzheimers disease (AD) individuals. In repetition prim- formance have often been found in AD and normal aging, with
ing paradigms, participants are generally not told about any pos- deficits on episodic memory tasks (to a much greater extent for AD
sible relationship between the initial and later occurrences of than for EN groups), in the face of normal performance on repe-
stimulus items; thus, these paradigms are implicit tests of memory. tition priming tasks (Craik & Rose, 2012; Zacks & Hasher, 2006).
This is in contrast to episodic memory paradigms in which specific A particularly interesting aspect of lexical decision repetition is
mention is usually made of previous experience with the stimulus that nonwords can be repeated; in this case, a performance decre-
items, and participants are asked to recall previously seen items or ment is sometimes found for word-like nonwords, presumably
because they become more difficult to distinguish from real words
in some way (e.g., McKoon & Ratcliff, 1979, Experiment 2).
Prior to describing the design features and specific rationale for
This article was published Online First July 7, 2014. the current study of repetition priming in AD, we will provide a
Beth A. Ober and Gregory K. Shenaut, Human Development Unit, brief overview of repetition priming in AD and normal aging,
Department of Human Ecology, University of California, Davis and Re- discuss the advantages of utilizing lexical decision as a repetition
search Service, Veterans Affairs Northern California Healthcare System, priming task, and review models of lexical decision and repetition
Martinez, CA. priming.
This research was supported in part by grants to the first author from the
Department of Veterans Affairs Medical Research Service and from the
National Institutes of Health (R29-AG10848) as well as by funding pro- Brief Overview of the Repetition Priming Literature
vided to the University of California Alzheimers Disease Research Center,
including Grants AG10129 and AG10220 from the National Institute on Repetition priming has been assessed extensively in AD and
Aging, and grants from the California State Department of Public Health normal aging with riddle-like tasks involving word generation or
Alzheimers disease Program. The contents reported within do not repre- retrieval such as word-stem completion or word-fragment comple-
sent the views of the Department of Veterans Affairs or the United States tion, and to a lesser degree with simpler, more passive tasks,
Government. We thank the staff of the University of California, Davis, usually involving reaction time (RT) measures and relatively more
Alzheimers Disease Clinical Center, Martinez and Sacramento clinics, for
shallow access to lexical-semantic memory. Such tasks (e.g., word
their referrals of research participants to our memory and language studies,
and we are grateful to the participants for their time and effort.
identification, word pronunciation, and lexical decision) produce
Correspondence concerning this article should be addressed to Beth A. smaller, less consistent deficits in repetition priming due to AD or
Ober, Human Development Unit, Department of Human Ecology, One aging, and sometimes no deficit at all. EN individuals showed
Shields Avenue, University of California, Davis, CA, 95616. E-mail: repetition priming in RT-based pronunciation or lexical decision
baober@ucdavis.edu tasks equivalent to that of young normal (YN) individuals in, for

973
974 OBER AND SHENAUT

example, Balota and Duchek (1991), Balota and Ferraro (1996), Models of Lexical Decision and Repetition Priming
Light and Kennison (1996), and Ober, Shenaut, Jagust, and Still-
man (1991). Contrasting studies in which EN participants showed The most pervasive element in models of lexical decision is
reduced repetition priming relative to YNs in relatively more some notion of familiarity. For example, in the two-stage model of
conceptually based tasks are plentiful; for reviews, see Light Balota and Chumbley (1984), the initial stage involved rapid
(2012), Fleischman and Gabrieli (1998), and Fleischman (2007). computation of familiarity, with relatively high familiarity biasing
Examples of AD participants showing repetition priming not dif- toward a fast yes (word) response and relatively low familiarity
fering from that of EN in RT-based pronunciation and/or lexical biasing toward a fast no (nonword) response; a second stage
decision tasks include Balota and Ferraro (1996), Carlesimo, occurred whenever the familiarity fell between the participants
Mauri, Fadda, Turriziani, and Caltagirone (2001), and Ober et al. criteria for a word compared with nonword response, and this stage
(1991); however, a study utilizing very long delays between re- involved more analytic processing of the lexical/semantic proper-
peated stimuli showed significantly less repetition priming of ties of the stimulus before a (necessarily slower) response was
lexical decision for AD compared with EN (Schnyer, Allen, made. Familiarity has long been thought to be incorporated into the
Kaszniak, & Forster, 1999). Examples of AD participants showing representation of lexemes in some way that lowers their activation
reduced repetition priming compared with EN in relatively more threshold (Forster, 1978; Morton, 1969), either absolutely as part
conceptual-level and/or word-retrieval-based tasks, include of the permanent lexical structure due to the frequency of access
Fleischman et al. (2005) and Mitchell and Schmitt (2006); for over a long period of time, or perhaps also relatively as the
reviews, see Fleischman and Gabrieli (1998) and Fleischman result of recent access (Coane, Balota, Dolan, & Jacoby, 2011).
(2007). Several within-subject studies provide evidence for a dis- Models of lexical decision that are focused more directly on
sociation such that AD patients show less-than-normal repetition repetition priming of lexical decision, however, have empha-
priming effects when the test task requires word production, but sized the levels at which the stimuli are processed during the
normal priming when it does not (Fleischman & Gabrieli, 1998; study and test phases (Duchek & Neely, 1989), or the degree to
Fleischman et al., 2001; but see Lazzara, Yonelinas, & Ober, which identical cognitive processes are used for the study and
2001). test tasks (e.g., Franks, Bilbrey, Lien, & McNamara, 2000). For
example, in experiments focusing directly on nonword priming,
Zeelenberg, Wagenmakers, and Shiffrin (2004) demonstrated
Lexical Decision: Advantages as a Repetition that lexical-decision priming for nonwords was inhibitory when
Priming Task a letter-height task was used at study, but facilitatory when a
RT-based lexical decision, in contrast to word-stem or word- lexical-decision task was used at study. Their explanation was
fragment completion, is an ideal task for the assessment of lexical based on a two-process model, with a relatively fast familiarity
repetition priming in neuropsychological populations with word- assessment followed by a slower episodic retrieval of the mem-
finding problems (such as AD and EN) because no word retrieval ory of making either a word or nonword response during
is required. There is ample evidence that AD patients perform at the study phase. Their study also included a second experiment
comparable-to-normal levels of accuracy on two-choice (word using lexical decision during both study and test, which found
vs. nonword) lexical decision, even though their RTs are rela- negative nonword priming when participants were asked to
tively long (e.g., Dunabeitia, Marin, & Carreiras, 2009; Perri et al., respond very quickly, and positive nonword priming when they
2003). In fact, AD patients produced comparable-to-normal RT were asked to respond more slowly. The quick-response con-
and accuracy in a go/no-go lexical-decision task in which a dition was interpreted as having given preference to the famil-
button press was made only to real words (Ober, Shenaut, & Reed, iarity process, whereas the slow-response condition was said to
1995). Moreover, the lexical-decision task requires the use of allow the retrieval of the prior response (to the stimulus during
nonword targets as foils, so priming of both words and nonwords the study phase). It is important to note the contrast between the
can be evaluated if desired, with the standard two-choice task. nonfamiliarity component of Balota and Chumbleys two-stage
In spite of these advantages, there have been relatively few model and the nonfamiliarity process of Zeelenberg et al.s
studies of repetition priming of lexical decision in normal aging, two-process model: In the former, access to permanent lexical/
and fewer still that included AD patients. The available evidence semantic memory is assumed, and in the latter, it is access to a
suggests that both AD and EN groups have intact repetition prim- recent, episodic memory that is used. In any case, all models of
ing for both nonwords and words, although the evidence is much repetition priming of lexical decision involve the modification
more limited for nonwords than for words. This is because the or creation of long-term memory traces representing studied
majority of experiments that have used the lexical-decision task items that can affect access to those items at the time of test.
with AD patients were actually semantic priming experiments
Specific Rationale for the Current Study
focused on priming due to associative relations between words,
each critical target word being used once in a semantically related A study by Balota and Ferraro (1996) assessed repetition prim-
pair and once in a semantically unrelated pair. This systematic ing of lexical decision in AD and normal aging without embedding
repetition of target words provided the opportunity to assess rep- lexical decisions into a semantic priming task. Their studywhich
etition priming for words but not nonwords, the latter not having focused on word-frequency effects employed a rhyme decision
been repeated systematically. When (word) repetition priming has task in the study phase, in which participants indicated whether
been assessed within this type of semantic priming paradigm, it has pairs of stimuli rhymed or not (e.g., cause/laws vs. cause/raise for
generally been found to be equivalent for AD, EN, and YN groups words, spart/cart vs. spart/hurt for nonwords), with both word and
(e.g., Ober & Shenaut, 1988; Ober et al., 1991). nonword rhyme items being potential targets in a later lexical-
REPETITION PRIMING IN AD AND AGING 975

decision task. The repetition priming effect, as assessed by lexical letter-height task, but did not require participants to hold a differ-
decision RT, was positive for words and negative for nonwords ent version of the presented stimulus in working memory.
(slower lexical decision RTs for repeated nonwords is more likely
when the study task does not involve lexical decision, as will be Nonword Characteristics
discussed later). Most importantly, the study found that the mag-
nitudes of (negative) nonword and (positive) word repetition prim- Nonwords that closely resemble words tend to show repetition
ing did not differ across AD, EN, and YN participants, providing priming effects of greater magnitude than those that do not (Stone
evidence that neither normal aging nor AD impairs the ability to & Orden, 1993; Wagenmakers, Zeelenberg, Steyvers, Shiffrin, &
create the necessary memory traces for nonwords. Raaijmakers, 2004), keeping in mind that, depending on experi-
Given that episodic memory is significantly impaired in AD, mental parameters, the nonword repetition priming effect may
whereas semantic memory and implicit memory are relatively sometimes manifest as facilitation and sometimes as inhibition
preserved, we can assume that the memory processes underlying (Zeelenberg et al., 2004). The usual method of generating word-
preserved repetition priming of lexical decision are unlikely to like nonwords has been to modify real words by replacing one or
depend on episodic memory; on the other hand, the relative pres- two letters, as was done in Balota and Ferraro (1996), but this
ervation of lexical/semantic knowledge would allow it to be used approach produces nonwords that may violate standard English
normally. The previously published study most similar to ours is letter-sequence frequencies, and presentation of such nonwords
that of Balota and Ferraro (1996). However, our study differed has been shown to activate, under some circumstances, the source
from theirs in two principal areas: the lexicality of the study task words from which they were derived (Deacon, Dynowska, Ritter,
and the overall similarity of word versus nonword stimuli. Instead & Grose-Fifer, 2004). To avoid these problems in the current
of rhyme decision, which is relatively likely to involve lexical study, we used obsolete English words, that is, words that once
access, our study task involved matching substrings within word were active in the language, but which have been considered
obsolete for 100 years or more; this results in words that feel
and nonword strings in order to minimize word-level processing of
much more like low-frequency words than many nonwords pro-
the stimuli by focusing the participants on letter-by-letter (ortho-
duced by altering current words. They are generally more likely to
graphic) processing. Our nonword stimuli were obsolete English
contain familiar morphology and perhaps a few participants may
words, and our words were all of low familiarity/low frequency,
have seen one or more of them in an historical text or dictionary,
our intention being to maximize the similarity of words and
or as a cognate word in a foreign language. In any case, previous
nonwords in form and in familiarity. Moreover, unfamiliar, low-
testing has shown that participants have little or no trouble clas-
frequency words show significantly longer lexical decision RTs
sifying them correctly as nonwords, at least on first presentation
and significantly greater repetition priming effectsthan high-
(Ober et al., 1991).
frequency words in YNs (e.g., Balota & Spieler, 1999;
Scarborough, Cortese, & Scarborough, 1977), ENs (Balota &
Ferraro, 1996), and very mild AD patients (but not mild-to- Word Frequency
moderate AD, per Balota & Ferraro, 1996). These experimental Low-frequency words benefit more from repetition than high-
design features were intended to provide a strong test of whether frequency words (Balota & Ferraro, 1996; Duchek & Neely,
AD and EN individuals differ from YN individuals in their ability 1989). This effect has usually been interpreted as indicating that
to modify (in the case of words) or create (in the case of nonwords) high-frequency words are already quite familiar, and therefore do
long-term memory traces, on the basis of only relatively shallow not become more familiar from recent presentation. In order to
orthographic processing of lexical stimuli, such that these traces maximize the potential amount of word priming in the current
would facilitate later processing of these stimuli. study, we used only low-frequency words, whereas Balota and
Ferraro used half high-frequency and half low-frequency words,
because word frequency was a critical variable in their study. Also,
Study Task
the use of only unfamiliar, low-frequency words further reduced
In contrast to the phonological, word-level study task was used the difference in familiarity between words and nonwords in our
by Balota and Ferraro, we were interested in using a subword level study compared with theirs.
orthographic study task comparable with the letter-height study
task used by Zeelenberg et al. (2004) with YN participants, in Method
which the letter string was simply scanned with no requirement of
any processing at the lexical level. Eliminating the requirement for
Participants
word-level processing at study would provide a test of whether
participants form new lexical/semantic memory traces for non- A total of 113 native speakers of English participated in this
words when there is unlikely to have been any prior conscious study: 30 who had been diagnosed with probable AD, 34 EN, and
lexical processing of them. Unfortunately, the letter-height task, 49 YN. Demographic and other information about the participant
which requires participants to ascertain whether a mentally gener- groups is presented in Table 1. The AD individuals were recruited
ated, lower-case version of an upper-case (presented) stimulus has from the University of California, Davis, Alzheimers Disease
more ascending letters (e.g., h, t) or descending letters (e.g., j, q), Clinical Centers (Martinez and Sacramento sites). All met the
could be difficult for AD patients due to their deficiencies in NINCDS-ADRDA (McKhann et al., 1984) criteria for probable
working memory. The study task we decided to use here, substring AD. None of the AD participants had a history of psychiatric
matching, had the same orthographic-scanning characteristic as the treatment, drug or alcohol abuse, heart disease, uncontrolled high
976 OBER AND SHENAUT

Table 1 Stimulus Materials


Mean (SD in Parentheses) Age, Education, MMSE, and NAART
for Each Participant Group A set of 50 low-familiarity, low-frequency word stimuli were
collected from the MRC Psycholinguistics Data Base: Machine
N Agea Educ. MMSE NAARTb Usable Dictionary, Version 2 (Wilson, 1988). The words ranged
from 217 to 448 (median 411) in the MRC composite familiarity
YN 49 19.3 (1.6) 13.1 (1.2) 26.41 (8.31)
EN 34 71.5 (6.5) 15.4 (2.4) 29.5 (0.7) 16.41 (8.66) norm, and ranged from 4 to 15 (median 5) in the MRC Francis and
AD 30 78.4 (6.1) 13.3 (2.4) 22.2 (3.9) 27.31 (10.28) Kucera (1982) frequency norm. Examples of word stimuli are
ardent, kerosene, sonata, and tweed. In addition, 50 pronounceable
Note. YN young normal; EN elderly normal; AD Alzheimers
disease; MMSE Mini-Mental Status Exam (number correct out of 30); nonwords were collected from a list of obsolete words (Ober et al.,
NAART North American Adult Reading Test (number of errors, i.e., 1991). No nonword appeared either in the familiarity norm or in
incorrectly pronounced words, out of 61). the Francis and Kucera norm. They were marked as obsolete in the
a
A smaller sample of EN participants that was more closely age-matched Oxford English Dictionary (1971) and were found neither in
to the AD group was utilized in a re-analyses of the EN and AD experi-
mental data; details are included in the Results section. b The NAART
Websters Modern (1902) or New Collegiate (1981) dictionaries.
was unavailable for one AD participant, due to experimenter error. Examples of the nonwords are: chalon, famble, jocant, and san-
glier. Both word and nonword stimuli had from five to eight letters
and from one to four syllables.
blood pressure, stroke, or head injury; none were taking any Items were divided into two counterbalance sets such that each
medications known to affect cognition (including cholinesterase stimulus was used equally often as a studied and an unstudied item
inhibitors). The AD participants were mildly-to-moderately de- (see Table 2). Six words and nonwords were randomly selected to
mented, with scores on the Mini-Mental State Examination (Fol- be used as fillers, two words and two nonwords in each of the three
stein, Folstein, & McHugh, 1975) ranging from 1228. phases, the same filler items being used in both counterbalancing
The EN participants were recruited from the community, via sets. The remaining 44 words and 44 nonwords were divided
advertisements posted in senior centers and placed in community equally and randomly between the two sets for the study phase,
newspapers. All of the EN individuals met the same exclusionary resulting in 22 words and 22 nonwords for each set. Three-letter
criteria as the AD participants and none had any complaints about matching substrings of each item were selected randomly (e.g.,
memory or other cognitive functions; they all had scores on the sonata: nat), then modified by random letter substitution to pro-
MMSE in the range of 2730. The YN participants were recruited duce three-letter substrings that did not match the item by only one
from among research subject pools in Psychology and Human letter (e.g., nat: nbt). Of the 22 studied words and 22 studied
Development at the University of California, Davis. These nonwords in Set 1, 10 words and 10 nonwords were randomly
younger participants met the same exclusionary criteria as the EN assigned to become studied items in the practice phase of Set 1 and
participants. All participants were given the North American Adult the unstudied items in the practice phase of Set 2; 12 words and 12
Reading Test (NAART; Spreen & Strauss, 1991), which involves nonwords were randomly assigned to become the studied items in
the pronunciation of irregularly spelled words, and which is the test phase of Set 1 and the unstudied items in the test phase of
strongly correlated with verbal IQ. The AD and EN participants Set 2. The same procedure was used in the opposite direction for
received a nominal fee, whereas the YN participants received the 22 words and 22 nonwords in the study phase of Set 2. Subjects
course credit for their participation. The study was approved by the were assigned sequentially to Set 1 or Set 2, and items within the
Institutional Review Boards of the VA Northern California Health lists were shuffled randomly for each participant, except for filler
Care System and the University of California, Davis. items, which always came first.

Table 2
Counterbalancing Scheme for Study, Practice, and Test Phases

Set 1 Set 2

Study phase Fillers for study phase (2 words, 2 nonwords)


P1: Studied items for practice phase, P2: Studied items for practice phase, Set 2
Set 1 (10 words, 10 nonwords) (10 words, 10 nonwords)
T1: Studied items for test phase, Set 1 T2: Studied items for test phase, Set 2
(12 words, 12 nonwords) (12 words, 12 nonwords)

Practice phase Fillers for practice phase (2 words, 2 nonwords)


Studied P1 (10 words, 10 nonwords) P2 (10 words, 10 nonwords)
Unstudied P2 (10 words, 10 nonwords) P1 (10 words, 10 nonwords)

Test phase Fillers for test phase (2 words, 2 nonwords)


Studied T1 (12 words, 12 nonwords) T2 (12 words, 12 nonwords)
Unstudied T2 (12 words, 12 nonwords) T1 (12 words, 12 nonwords)
Note. The same filler items are used in both sets; all other items are used in one set as a studied item and in
the other as an unstudied item, as indicated by the labels P1, P2, T1, and T2. Studied and unstudied items within
a phase were shuffled together before each run.
REPETITION PRIMING IN AD AND AGING 977

Design and Procedure


100
A 3 Group (AD, EN, and YN) 2 Lexicality (word vs.
nonword) 2 Repetition (studied vs. unstudied) design was em-

Priming Effect (Milliseconds)


ployed, with lexicality and repetition being manipulated within
subjects. The experimental procedure involved three phases, with
a brief pause (about 1 min) between them (see above and Table 2 0
for details on stimulus selection and counterbalancing). In the first
(study) phase the participants performed a substring matching task.
Each of the study phase stimuli was presented on a computer
screen with a three letter string beneath it. Participants were
-100
instructed to press a large green button (yes) if the lower string was
contained in the longer string above it, and to press a large red
button (no) if the lower string was not contained in the longer
string. For half of these trials yes was the correct answer (e.g.,
flyer - yer, brike - rik); for the other half, no was the correct -200
answer (e.g., mutton - dut, drazel - drx). The second and third
AD EN YN
phases consisted of two-choice lexical decision trials, in which
subjects were instructed to respond yes or no depending on
whether a stimulus was a word. The second session was a practice
Word
session for the third, which was the critical test phase. One half of
Nonword
the studied words and one half of the studied nonwords had been
presented with a matching substring, and the other half had been
presented with a nonmatching substring during the study phase. Figure 1. Word and nonword RT priming effect means (SE) for AD
None of the test phase stimuli had been utilized in the practice (Alzheimers disease, N 30), EN (elderly normal, N 34), and YN
phase. Participants were not given any information about the (young normal, N 49) participants.
relationship between the substring and lexical decision tasks.
suggested that d .20, .50, and .80, be interpreted as small,
Results medium, and large effects, respectively (Cohen, 1988; pp. 24 27).

The 113 participants that were included in the data analyses had
Analysis of Differences Due to Age
all achieved accuracy levels of 75% or more on the critical word
and nonword trials. Additional participants were tested who did The RT means are presented in Table 3. A 2 Group (YN, EN)
not meet the predetermined accuracy criteria; these included five 2 Lexicality (word, nonword) 2 Repetition (studied, unstudied)
YN, one EN, and seven AD participants. In order to reduce RT ANOVA revealed the expected overall longer RT for the EN
variance due to outliers in the data for the final 113 participants, a compared with YN groups, F(1, 81) 12.2, p .001, d .78,
data trimming procedure was employed in which the trials with the and the expected longer RTs for nonwords versus words, F(1,
highest and the lowest RT in each cell of the experimental design 81) 68.7, p .001, d 1.8. The overall effect of repetition was
were eliminated for each participant, as suggested by Bush, Hess, negligible, F(1, 81) 1, due to the positive repetition effect for
and Wolford (1993). words canceling out the negative repetition effect for nonwords.
The mean RT priming effects (unstudiedstudied) for the three The Lexicality Repetition interaction effect was quite robust,
groups across all experimental conditions are displayed in Figure F(1, 81) 20.1, p .001, d 1.0, and reflects the opposite
1. As can be seen in the figure, the pattern of results for RT effects of repetition on words versus nonwords. All of the remain-
priming is that all three groups showed evidence of a numerically ing interactions were insignificant, including Group Lexicality,
positive priming effect for words (i.e., shorter RT for studied and Group Lexicality Repetition, both with F(1, 81) 1. In
words than for unstudied words) and a negative priming effect for sum, the increase in RT for nonwords versus words was propor-
nonwords (i.e., longer RT for studied nonwords compared with tionate for the YN and EN groups, and the degree to which the
unstudied nonwords). In order to address the primary question as repetition priming effect was reversed for nonwords (negative
to whether word and nonword repetition priming of lexical deci- priming) versus words (positive priming) was not modulated by
sion RTs is modulated either by age or by dementia, the AD and age group.
EN groups were included in a first set of ANOVAs (dementia- Of secondary interest were the error data, which are also pre-
related effects), whereas the EN and YN groups were included in sented in Table 3. The error rate was low, ranging from 3% to 11%
a second set of ANOVAs (age-related effects). Secondary analyses across experimental conditions. A Group Lexicality Repeti-
included: an analysis of lexical decision errors, a test of the effect tion ANOVA showed that EN were more accurate than YNs, F(1,
of the 7-year mean age difference between our EN and AD groups, 81) 28.3, p .001, d 1.2; a marginal two-way interaction of
a test of the effect of general slowing due to aging and dementia, Lexicality Repetition, due to repeated words showing overall
and a test to determine the extent to which individual groups fewer errors than nonrepeated words, in contrast to equivalent
manifested RT priming effects for words and nonwords. All effect levels of accuracy for repeated versus nonrepeated nonwords, F(1,
sizes are expressed in terms of Cohens d statistic; Cohen has 81) 3.79, p .052, d .43; and a robust three-way interaction
978 OBER AND SHENAUT

Table 3 the AD group made disproportionately more errors on nonwords


Mean RT and Error Rate (SD) Across Groups and than words, compared with the EN group, F(1, 62) 3.69, p
Repetition Conditions .056, d .49, for Group Lexicality. The three-way interaction
was insignificant, F(1, 62) 2.61, p .107, d .41, but at a level
Words Nonwords that did not completely exclude the possibility that the EN groups
Repeated Not repeated Repeated Not repeated greater accuracy for studied than for unstudied nonwords differed
from the AD groups pattern in the opposite direction. This would
RT (ms)
YN 680 (114) 719 (109) 852 (239) 821 (201)
be parallel to the same interaction found for EN compared with
EN 824 (183) 867 (216) 1,006 (295) 971 (319) YN. All remaining main effects and interactions were insignificant
AD 1,140 (363) 1,205 (395) 1,797 (1091) 1,686 (870) (Fs 1).
Errors (%)
YN 6 (7) 11 (10) 10 (9) 8 (9)
EN 3 (5) 3 (5) 3 (5) 6 (9) Possible Effects of an Age Difference Between the
AD 4 (7) 6 (7) 11 (11) 9 (12) EN and AD Groups
Note. YN young normal; EN elderly normal; AD Alzheimers Given the almost 7-year age difference between our AD and EN
disease.
samples (see Table 1), we reanalyzed the RT data with a smaller
sample of EN participants more closely matched on years of age to
of Group Lexicality Repetition (absent in the analysis of the the AD group. The youngest of the EN participants were dropped
RT data), F(1, 81) 10.3, p .002, d .71. The three-way until we ended up with a group of 21 ENs with a mean age of 75.7
interaction was due to YN participants showing the same pattern of (SD 4.1), which resulted in t(49) 1.73, p .086, for the age
positive repetition priming for words versus negative priming for difference (2.7 years) between AD and ENs, in contrast to t(62)
nonwords as they showed for the RT data, although EN partici- 4.34, p .001, for the age difference (6.9 years) between the full
pants showed no priming for words and positive priming for sample of 34 ENs and the AD group. The pattern of results was
nonwordsa pattern different from that exhibited in the RT data. nearly identical for this as compared with the full-sample analyses.
There was a marginal indication of a repetition effect, with re- The only differences were that the F values were somewhat
peated items showing greater accuracy than nonrepeated items, decreased (and corresponding p values were somewhat increased),
F(1, 81) 2.80, p .094, d .37; all remaining Fs 1. presumably due to a decrease in power with the smaller sample.
A parallel ANOVA was performed on the error rate date with
the smaller sample of 21 EN participants who were matched more
Analysis of Differences Due to Dementia
closely in age with the AD; the results were virtually identical to
We now turn to the RT data for the EN versus AD groups (see those using the full sample of EN participants, including the
the relevant rows of Table 3). As expected, the AD group re- direction of the EN groups accuracy difference for studied versus
sponded more slowly than the EN group across all experimental unstudied nonwords, except for a minor reduction of F values and
conditions, F(1, 62) 22.0, p .001, d 1.2, and there were slightly increased p values.
longer RTs for nonwords compared with words, F(1, 62) 26.6,
p .001, d 1.3. The overall effect of repetition was negligible, Possible Effects of Age- and Dementia-Related
F(1, 62) 1, due to the positive effect of repetition for words
General Slowing
canceling out the negative effect of repetition for nonwords. As
was the case for the YN and EN groups combined data, the To examine possible effects of general slowing on the between-
analysis on the EN and AD groups combined data showed a group RT priming results, we applied a method suggested by
significant Lexicality Repetition effect, F(1, 62) 5.75, p Madden, Nebes, and Allen (1992). First, in order to get the best
.018, d .61, due to the opposite effects of repetition on words possible estimate of the task-complexity function of the YN and
versus nonwords. The AD group showed a disproportionate overall AD groups relative to the EN group using the data available in this
increase in RT for nonwords versus words (563 ms, a 45% in- experiment, we computed the group means of eight different types
crease) as compared with the EN group (142 ms, a 17% increase), of correct trials: For the study phase task (substring matching, not
which was reflected in a significant Group Lexicality interaction semantic), we computed the mean RT for word/match, word/no-
effect, F(1, 62) 10.3, p .002, d .81. The remaining match, nonword/match, and nonword/no-match; for lexical deci-
interaction effects, including the important Group Lexicality sion (semantic), we included both the practice block and the
Repetition effect, produced Fs 1. In summary, the AD group experimental block, and computed the means for studied/word,
exhibited greater slowing for nonwords compared with words than studied/nonword, unstudied/word, and unstudied/nonword. Then,
did the EN group, and most importantly, the degree to which the using those eight variables, we computed linear regression equa-
repetition priming effect was reversed for nonwords (negative tions for EN and AD: AD 69.3 1.68 (EN), r2 .974, and
priming) versus words (positive priming) did not differ for the AD for EN and YN: YN 287 0.543 (EN), r2 .987. We then
compared to EN participants. transformed the YN and AD lexical decision data by reversing the
The error rate ranged from 3% to 11% across experimental equations (i.e., subtracting the mean and dividing by the coeffi-
conditions. The Group Lexicality Repetition ANOVA indi- cient), and repeated the analyses described earlier on aging and
cated that the AD group showed lower accuracy than the EN dementia. For overall RT, neither the AD group nor the YN group
group, F(1, 62) 9.09, p .004, d .77; words showed higher differed from the EN group, Fs 1. For all other factors and
accuracy than nonwords, F(1, 62) 10.9, p .002, d .84; and interactions, the pattern of results was identical to that of the
REPETITION PRIMING IN AD AND AGING 979

original analysis, suggesting that general slowing had little if any closer to that of targets requiring a no decision, than was the case for
impact on the results. Balota and Ferraro, who changed one or two letters in real words to
produce their nonwords, and used both high- and low-frequency
Priming in All Groups Combined and Within words. The combination of the orthography-based study task and the
Individual Groups lexicality-based test task minimized the role of strategies based on
explicit memory for the encoding context, because different levels of
In spite of the pattern of effects reported above, it is still of processing as well as different responses were required during the
interest to determine whether individual groups produced positive study versus test phase. In spite of these changes, the results of our
RT priming for words and negative priming for nonwords. As a study are quite similar to those of Balota and Ferraro as pertains
preliminary, we looked at word and nonword RT priming for all specifically to the pattern of word and nonword repetition priming in
three groups combined in a pair of 3 Group (AD, EN, YN) 2 aging and dementia; note, however, that Balota and Ferraro did not
Repetition (studied, unstudied) ANOVAs, using just word or just report on priming within individual groups nor provide per-group
nonword data. There was a significant overall positive priming standard errors. Moreover, it is of interest that the absolute magnitude
effect for words, F(1, 110) 15.9, p .001, d 0.76, and also of priming in our study was greater than in theirs for every group and
a significant (but less robust) overall negative priming effect for for both words and nonwords (our EN group being compared with
nonwords, F(1, 110) 4.75, p .029, d 0.42. both of theirs, and our AD group to both of theirs). This suggests that
Next, we performed a series of t tests on priming within each the methodological differences in our studya much shallower study
individual group (means and standard errors are displayed in task and much lower frequency words and more word-like non-
Figure 1). YN participants showed significant priming for words, wordsmay have enhanced both positive priming for words and
t(48) 2.86, p .006, but insignificant priming for nonwords, negative priming for nonwords in every group, at least to some
t(48) 1.49, p .138; EN participants showed significant prim- degree.
ing for words, t(33) 3.24, p .003, and marginal priming for
nonwords, t(33) 1.81, p .076; and AD patients showed a
marginal priming effect for words, t(29) 1.83, p .074, and
Word Repetition Priming
insignificant priming for nonwords, t(29) 1.33, p .191. The invariance of the positive word-repetition priming effect with
Although all of these results are in the predicted direction, and all AD and EN, in spite of the slower overall RTs obtained with these
three groups showed priming for words (if only marginally for participant groups on the lexical-decision task relative to YN, and in
AD), only the EN group showed a (marginal) priming effect for spite of the well-documented deficits in explicit memory tests asso-
nonwords. ciated with AD and normal aging (Fleischman & Gabrieli, 1999; Old
& Naveh-Benjamin, 2008), is another indication of its robustness. The
Discussion present findings for words are consistent with findings of preserved
repetition priming in normal aging and AD across several types of
Summary of Findings verbal tasks, when the tasks are relatively more perceptual than
conceptual in nature and when word retrieval is not required (as
The RT data from this lexical decision, repetition priming experi- reviewed by Fleischman, 2007). Nonetheless, the present AD study is
ment showed that the pattern of priming was not modulated by age one of very few that have focused on repetition priming of lexical
(YN vs. EN) or by dementia (AD vs. EN), and that there was overall decision; the majority of experiments on lexically based repetition
significant positive priming for words as well as overall significant priming in AD have utilized tasks such as threshold word-
negative priming for nonwords. A caveat is that although each of the identification, and word-stem or word-fragment completion (e.g.,
three individual groups showed at least marginal priming for words, Arroyo-Anllo, Ingrand, Neau, Aireault, & Gil, 2004; Karlsson,
only the EN group showed marginal priming for nonwords, indicating Borjesson, Adolfson, & Nilsson, 2002; La Voie & Faulkner, 2008).
that there may have been insufficient power relative to within-group
variability to test for these priming effects in the individual groups.
Nonword Repetition Priming
The accuracy data generally resembled the RT data, with the follow-
ing caveats: The overall accuracy was high, with rather small differ- The use of a two-choice lexical decision paradigm to assess repe-
ences among conditions; and, unlike the AD and YN groups, the EN tition priming has the benefit of allowing the researcher to evaluate
group did not show the expected increase in accuracy with repeated nonword repetition priming effects. We were particularly interested in
words, or the expected decrease in accuracy with repeated nonwords. the nonword priming effect because it provides a test of the intactness
There did not appear to be any effect of a slight age difference of the memory processes which underlie repetition priming for novel
between the AD and EN groups, nor did there appear to be any effect (i.e., never before encountered) stimuli. The design of the present
of general slowing, due either to age or to dementia. experiment, with different study- versus test-phase tasks, very low-
The current study differed from an earlier one by Balota and frequency words (i.e., very unfamiliar words), and very word-like
Ferraro (1996) in several ways. Our study task, substring matching, nonwords (i.e., obsolete English words) was meant to ensure a robust
was intended to maximize the role of orthographic, letter-by-letter nonword familiarity effect (i.e., negative priming for nonwords),
processing, in contrast to the test task (lexical decision), which in- which we could then compare across participant groups. We did,
volved lexical, word-level processing, whereas their study task, rhyme indeed, obtain a negative priming effect for nonwords, which was
decision, was at the lexical level. Moreover, the use of low-frequency equivalent between the AD and EN groups, as well as between the EN
word targets and obsolete English nonword targets resulted in the a and YN groups. Negative priming effects for nonwords have been
priori familiarity of the targets requiring a yes decision being much obtained with YNs (Bowers, 1994; McKoon & Ratcliff, 1979;
980 OBER AND SHENAUT

Zeelenberg et al., 2004), and with AD and EN participants (Balota & There is considerable similarity between encountering an un-
Ferraro, 1996). We have provided a replication and extension of known word while reading a text, and encountering a word-like
equal-to-normal, negative, nonword priming for AD patients, utilizing nonword in an experimental context. In a textual context, it is
a different type of study task (requiring a focus on sublexical orthog- reasonable to assume that the string is processed as a word that was
raphy) and a more challenging lexical-decision task (in terms of the previously unknown, with fragments of meaning, grammatical
similarity of the nonwords to the words) than employed in previous function, and pronunciation stored in a rudimentary, provisional
research. Our findings provide increased support for the ability of lexical entry. When the same string is encountered later, additional
mild-to-moderate AD patients (like ENs and YNs) to create long-term meaning is added to the previously created entry from the later
memory traces for novel, word-like letter strings. context; this is repeated as part of the normal process of word
There is evidence for two opposing processes in making a lexical acquisition. Obviously, the textual context provides considerable
decision to a repeated nonword: a relatively fast, familiarity-based information that can be stored in the new lexical entry, even if
process, which inhibits the correct response to a repeated nonword there is not enough to provide a complete understanding of the
(i.e., it is biased toward a word response) and results in a negative word. In an experimental context, particularly one such as in the
nonword priming effect; and a relatively slow, instance-based process, present experiment where the initial encoding of the items was
which facilitates the correct response to a repeated nonword (i.e., it is quite shallow, there is much less information available for storage
biased toward a nonword response) and results in a positive non- in a provisional lexical entry. However, even in such a case there
word priming effect. This opposing-process evidence was obtained by may be at least some information available, including when and
the manipulation of speed-stress (Wagenmakers, Zeelenberg, et al., where the item was encountered, what the readers mental state
2004) and similarity of the study and test tasks (Zeelenberg et al., was at the time, what the response was, and hypotheses as to
2004), in lexical-decision experiments with YN participants. In their possible morphological, phonological, and semantic attributes
discussions of the nature of nonword memory representations, based on the items orthography. If such provisional lexical entries
Wagenmakers, Zeelenberg et al. (2004), Zeelenberg et al. (2004), and resulted from single study-phase exposures to word-like nonword
Wagenmakers, Steyvers et al. (2004) assume that the initial presen- letter strings, then during the test phase of a repetition-priming
tation of a nonword does not result in a lexical-semantic memory trace experiment the entry would be activated when the previously
for that nonword. Instead, their assumption is that in addition to an viewed letter string was presented again, along with any attributes
instance (context-based) trace being created, the presentation of a stored there, including item familiarity. Incidentally, if such pro-
nonword triggers activation of (actual) words in lexical-semantic visional lexical entries are created as the result of an exposure as
memory that are orthographically and/or phonologically similar to the shallow as that involved in our experiments study task, it is most
presented nonwords. These types of neighborhood activation ef- likely that the process is an automatic one, as opposed to one
fects have, in fact, been demonstrated for nonwords (Siakaluk, Sears, requiring specific effort or explicit processing of the item.
& Lupker, 2002) as well as for words (Sears, Hino, & Lupker, 1995; The concept of a provisional lexical entry is compatible with
Yates, Locker, & Simpson, 2004). Repeated presentation of a non- both the Tenpenny (1995) weakly episodic and the Bowers
word results in at least some of these neighborhood words being (2000) weakly abstractionist view of repetition priming. Both
reactivated, thus increasing the feeling of familiarity to the nonword views allow for the contribution of episodic and abstract memory
stimulus. In any case, it is assumed by Wagenmakers, Zeelenberg, and traces to repetition priming, albeit with one type of trace playing a
colleagues (e.g., Zeelenberg et al., 2004) that the familiarity-based more important role in each view. Moreover, this type of approach
process underlying negative nonword priming does not entail lexical- is compatible either with a multiple-systems view in which lexical
semantic representations for the nonwords per se. In the next section, and semantic processing are supported by separate memory sys-
we argue that such representations may indeed be involved in the tems (Coltheart, Rastle, Perry, Langdon, & Ziegler, 2001), or with
processing of repeated word-like nonwords. a single-system view in which lexical and semantic processing are
served by the same memory system (e.g., Dilkina, McClelland, &
Plaut, 2010).
A Theoretical Conjecture: Nonword Repetition Coane et al. (2011) results, which differentiated a long-lasting
Priming and Novel Word Learning absolute familiarity (resulting from experience with the item
across the life span) from an episode-specific relative familiarity
It is not unusual to encounter word-like nonwords when reading. (a change in familiarity caused by recent access), provides an
A well-known example is in Chapter 1 of J. K. Rowlings (1997) interesting nuance to the idea of a provisional lexical entry for
Harry Potter and the Philosophers Stone: nonwords. Their dual-familiarity model suggests that words with
Even Muggles like yourself should be celebrating, this happy, happy
high absolute familiarity have little potential to accrue relative
day! familiarity, whereas words with low absolute familiarity have high
potential; this duality can explain certain aspects of the word
And the old man hugged Mr. Dursley around the middle and walked frequency effect. Because a newly created nonword lexeme
off. would have near-zero absolute familiarity, then it would have
maximum potential to attain high relative familiarity, making such
Mr. Dursley stood rooted to the spot. He had been hugged by a
complete stranger. He also thought he had been called a Muggle, lexemes subjectively more similar to unfamiliar words in terms of
whatever that was (p. 10). overall familiarity, and perhaps accounting for the negative non-
word repetition effect such as we report here.
This word-like nonword is used a few more times later in the In order to account for positive nonword priming based on a
same chapter, but is not defined explicitly until Chapter 4. memory of making a previous no response in experiments using
REPETITION PRIMING IN AD AND AGING 981

lexical decision at both study and test, Wagenmakers, Zeelenberg EN Error-Rate Priming
et al. (2004) posited an episodic, instance-based component in
their model of lexical-decision repetition priming, motivated in Finally, it was unexpected that the EN groups error data did not
part by their explicit assumption that nonwords have no lexical or display the pattern seen across all groups for RT priming and in the
semantic memory entries. It is unclear what the participants YN and AD group for errors, namely positive priming for words and
decision to classify a word-like letter string as not a word would negative priming for nonwords. Instead, the EN error rate showed
have on the formation of provisional lexical entries. The existence near-zero priming for words and positive priming for nonwords.
of such entries would presumably facilitate retrieval of memories Although this could be simply a fluke, there is another possibility: the
of previous responses by acting as a verbal index into episodic well-known cautiousness of elderly participants (e.g., Starns & Rat-
memory; alternatively, one could suppose that the previous lexical cliff, 2010). EN participants may have noticed during the study phase
decision is stored in the provisional lexeme itself, being activated that the items seemed to be very infrequent words, and so implicitly
along with its other attributes when the letter string is repeated. tried to find a meaning for each one (e.g., in case they were asked
Ironically, in this case part of the information stored in the lexical about them later) while they performed the substring matching task,
entry would be this is not a word. However, this is not unprec- with failure being more salient than success. In this case, I found no
edented: Consider Lewis Carrolls (1872) slithy toves and other meaning for X memory trace could have facilitated their error
more or less familiar words whose meaning is essentially that performance for studied nonwords while having little effect on words.
they are meaningless, plus some bits of source information. The Note that although in our experiment this contrary effect was visible
process whereby an initially sparse provisional lexeme can become only in EN error performance, the explanation is somewhat compat-
increasingly word-like as it accumulates meaning through subse- ible with the finding of Zeelenberg et al. (2004) of positive RT
quent experience seems similar to the Wagenmakers, Steyvers et priming for nonwords when lexical decisions are made at study.
al. (2004) account of how new information is added to an existing Perhaps if processing time were constrained during the study task,
lexical/semantic trace; the addition of the idea of provisional gratuitous lexical processing could be reduced, parallel to what was
lexemes coming into existence upon encoding of word-like letter also seen by Zeelenberg et al. for explicit lexical decisions with
strings would provide a theoretical starting point for that process. constrained study time.
Interestingly, there is evidence for implicit learning of novel
Conclusions and Future Directions
words by way of reports of successful acquisition of new words by
amnesics (e.g., Westmacott & Moscovitch, 2001) and partial ac- The results of this study extend the stimulus and task parameters
quisition (across incidental-learning exposures) and retention of a under which repetition priming of lexical decision, based mainly (if
novel verb by AD patients (Grossman et al., 2007). Both AD and not exclusively) on implicit memory processes, is preserved in AD as
amnesic patient groups have significant deficits on explicit mem- well as normal aging. Specifically, the repetition priming effect and
ory tasks; thus, the novel-word learning must be solely or mainly the degree to which the repetition priming effect was reversed for
implicit in nature. In the case of AD, these patients preserved nonwords compared with words was unaffected by AD or normal
novel-word learning is consistent with the evidence for preserved aging. Thus, AD and EN individuals, like YN individuals, are able to
lexical-decision priming, and with a general preservation of im- form new long-term memory traces based on purely orthographic
plicit learning and memory for lexical stimuli. It should be noted, encoding of novel word-like letter strings.
however, that there was evidence that the AD patients were defi- One obvious question for future research is whether significant
cient compared with controls in the acquisition of the semantic differences in priming effects would be obtained for AD compared
attributes of newly learned words in Grossman et al. (2007). An with EN groups or EN compared with YN groups with a lexical
interesting demonstration of novel word learning in YNs is pro- decision test task, if the time between the study and test phases had
vided by Tamminen and Gaskell (2013) who were able to obtain been many hours (or several days), as opposed to the approximate 10
semantic priming by preceding previously known words by newly min of the current study. A related question for future research is
learned words (after only a brief period of training); semantic whether there would be differences in the longevity of the lexical-
priming is, of course, indicative of the new words having been decision priming effects based on the nature of the study task (e.g.,
incorporated into the lexical/semantic network. orthographic, phonemic, or semantic) and/or the type of word versus
In sum, our conjecture is that an initial presentation of a non- nonword stimuli (including the similarity between the two types of
word, whether in an experimental task or in a text, may automat- stimuli), in addition to differences due to age or disease.
ically cause a provisional lexical entry to be created, storing Another direction for future research is toward clarifying the link
mainly orthographic or phonemic features (but relatively few between nonword repetition priming and the acquisition of new
semantic features). Consistent with this proposition are research vocabulary. To what extent do the abstract structures posited by
findings in the domain of novel-word learning that are suggestive Tenpenny (1995) and Bowers (2000) act like lexical entries? Com-
of changes in the lexical/semantic processing for novel words plicating this task is the lack of an accepted way to determine
occurring after just a single exposure (e.g., Nora et al., 2012; objectively when a newly encountered nonword such as Muggle
Tamminen & Gaskell, 2013). These and related findings have led enters the lexicon and what information is stored with it during the
to the complementary systems account of word learning that ongoing process of lexicalization. Given the Grossman et al. (2007)
distinguishes short- from long-term (after being repeatedly linked findings regarding novel-word learning abilities in AD (which are
to semantic information) mental representations of novel words, consistent with preserved nonword repetition priming in AD), another
with the long-term representations becoming less distinguishable interesting research avenue would be to extend that work via para-
from those of existing words with regard to behavioral and neural digms that make greater use of implicit memory tasks, on which AD
response patterns (Lindsay & Gaskell, 2010). patients perform relatively well (e.g., tasks that do not require word
982 OBER AND SHENAUT

retrieval). Such implicit tasks could involve pairings of novel words decision tasks. Memory & Cognition, 17, 148 162. doi:10.3758/
with pictures, sounds, tactile stimuli, and so forth, in addition to verbal BF03197065
material such as sentence frames. Dunabeitia, J. A., Marin, A., & Carreiras, M. (2009). Associative and
orthographic neighborhood density effects in normal aging and Alzhei-
mers disease. Neuropsychology, 23, 759 764. doi:10.1037/a0016616
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.28.3.661 Accepted May 2, 2014

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