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TheHyperprimingPhenomenoninNormalAging:AConsequenceofCognitiveSlowing?

ArticleinNeuropsychology·November2003

DOI:10.1037/0894-4105.17.4.594·Source:PubMed

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The Hyperpriming Phenomenon in Normal Aging:A Consequence of Cognitive Slowing?

Benedicte Giffard, Beatrice Desgranges, andNacer Kerrouche

Institut National de la Sante et de la RechercheMedicale E0218, Universite de Caen

Pascale Piolino and Francis EustacheInstitute National de la Sante et de la Recherche

Medicale E0218, Universite de Cane; andUniversite Rene Descartes, Paris 5

Increased semantic priming effects (hyperpriming) are sometimes observed in Alzheimer’sdisease (AD) and in normal aging. Whereas the processes underlying this phenomenon arenow well understood in AD, the interpretation is much more woolly in normal aging. Toexplore semantic priming, the authors used a lexical decision task in which the influence ofattention and cognitive slowing was controlled. To explore the semantic organization, thewords had coordinate (tiger–lion) or attribute relations (zebra–stripes). Priming scores of 21older and 20 young participants were equivalent in the 2 conditions. These results reflect theintegrity of semantic memory with normal aging and call into question some investigationsshowing hyperpriming for older participants; this may instead be an artifact of a generalslowing effect.

To assess the integrity of the semantic memory network,researchers often use the semantic priming paradigm incognitive studies evaluating healthy participants or partici-pants with brain damaged. Contrary to classical semantictasks (e.g., naming or verbal fluency), this paradigm allowsone to assess semantic memory implicitly and then to min-imize the intervention of nonsemantic cognitive processing.Semantic priming effects refer to the modification of astimulus’s processing following the presentation of a relatedstimulus. These effects depend on semantic memory (Tulv-ing, 1995) and require the semantic processing of a primestimulus and/or a semantic relation between the prime andthe target. In participants without brain damage, many stud-ies on semantic priming effects show that, in lexical deci-sion or pronunciation tasks, recognition of a target word(chair) is facilitated by the prior presentation of a relatedprime word (table) compared with an unrelated controlword (horse; Fischler, 1977; Meyer & Schvaneveldt, 1971;Neely, 1977). The participant does not make an explicitjudgement on the link between the prime and the target, andthis processing facilitation is, thus, supposed to depend onan automatic access to information. These priming effects

are commonly viewed, within the framework of the auto-matic spread of activation in the semantic network, as apreactivation of the target by a related prime (Collins &Loftus, 1975): The presentation of a prime (word or picture)automatically activates its node in memory; this activationspreads to highly related nodes, thus momentarily increas-ing their accessibility.

The semantic priming paradigm has been largely used inAlzheimer’s disease (AD) to assess the integrity of thesemantic memory network. Nevertheless, the results haveoften been conflicting, with some authors reporting less thannormal priming (Ober & Shenaut, 1988; Salmon, Shi-mamura, Butters, & Smith, 1988; Silveri, Monteleone, Bu-rani, & Tabossi, 1996) or equivalent priming for patientswith AD and controls without AD (Nebes, Martin, & Horn,1984; Ober, Shenaut, Jagust, & Stillman, 1991). Finally,some authors have observed an apparently paradoxical in-creased priming (hyperpriming) in AD (Balota, Watson,Duchek, & Ferraro, 1999, Experiment 1; Chertkow et al.,1994; Chertkow, Bub, & Seidenberg, 1989; Margolin, Pate,& Friedrich, 1996; Nebes, Brady, & Huff, 1989). Conflict-ing hypotheses have been advanced to explain this hy-perpriming effect, but recently, thanks to a longitudinalfollow-up of a group of patients with AD, we (Giffard et al.,2002) demonstrated clearly that the degree of semanticpriming varies according to the progressive semantic mem-ory deterioration in people with AD and that the hyperprim-ing effect, which occurs at the beginning of the attribute lossonly, reflects the start of semantic memory degradation. Theexplanation is that when the attributes of concepts startbeing lost—whereas superordinate information is well pre-served (e.g., the tiger and the lion are still known to be wildanimals, but knowledge about their stripes and mane, re-spectively, is lost)—the ability to distinguish between twovery similar concepts, such as tiger and lion, is impaired.More precisely, not only do priming effects exist—becausethe words are semantically related through membership in

Benedicte Giffard, Beatrice Desgranges, and Nacer Kerrouche,Institut National de la Sante et de la Recherche Medicale (Inserm)E0128, Universite de Caen, Caen, France; Pascale Piolino andFrancis Eustache, Inserm E0218, Universite de Caen, and Institutde Psychologie, Ecole Pratique des Hautes Etudes, Centre Nationalde la Recherche Scientfique (CNRS) 8581, Universite Rene Des-cartes, Paris 5, Paris, France.

We acknowledge A. Hirtt and C. Le Stanc for the recruitment ofparticipants and A. R. Young and A. Viard for revising the Englishstyle.

Correspondence concerning this article should be addressed toFrancis Eustache, Laboratoire de Neuropsychologie, InsermE0218, Universite de Caen, CHU Cote de Nacre, 14033 CaenCedex, France. E-mail: neuropsycho@chu-caen.fr

Neuropsychology Copyright 2003 by the American Psychological Association, Inc.2003, Vol. 17, No. 4, 000–000 0894-4105/03/$12.00 DOI: 10.1037/0894-4105.17.4.000

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their preserved superordinate class—but they are greaterthan in a control group (i.e., hyperpriming occurs). Specificattributes that characterize each concept are lost; hence, aconfusion, an overlapping between the two coordinate con-cepts (both are wild animals and also both have fur and aredangerous) occurs. Therefore, as suggested by Martin(1992), the semantic priming (tiger–lion) would be treatedby the patient as repetition priming (wild animal–wild ani-mal), the magnitude of the latter being greater than theformer.

The majority of normal aging studies have shown equiv-alent semantic priming effects in comparing older withyoung participants (Bowles & Poon, 1988; Burke, White, &Diaz, 1987; Chiarello, Church, & Hoyer, 1985; Howard,McAndrews, & Lasaga, 1981; Linnville, 1995). However,as in AD studies, several investigators have shown signifi-cantly greater semantic priming effects for older relative toyounger adults (Laver, 2000; Laver & Burke, 1993; Myer-son, Hale, Chen, & Lawrence, 1997). This hyperprimingeffect in normal aging could be due to several factors. ForLaver and Burke (1993), who undertook a meta-analysisof 15 studies, the increased priming effect is due to the morenumerous connections among related words in older adults’memory because of their greater experience during 60 ormore years of language compared with 18-year-old adults.More precisely, the authors explained this increased prim-ing by the fact that “in semantic memory, transmission ofpriming is aided by the many indirect connections that linkrelated concepts. . . . Summation of priming over multipleconnections rapidly increases priming levels at target nodesnear levels required for onset of the activation mechanism”(Laver & Burke, 1993 p. 41). Other hypotheses are alsoconceivable. Contrary to the proposal of Laver and Burke, ifthe processing underlying the increased performance is thesame as that described previously in AD, it could mean thatthe semantic network of the older participants with hy-perpriming is no more intact, specifically at the attributelevel.

Aside from those two diametrically opposed hypothesesbased on modifications in semantic processing with age,there exist more methodological explanations (Myerson etal., 1997). It is well-known that the older population ischaracterized by a slowing of nearly every cognitive pro-cess. Factors that slow processing of words (e.g., age) areexpected to increase the facilitation of semantic context,because when the processing time is long, the semanticcontext has more chance to have an effect. According to thisassertion, the increase of semantic priming effects wouldsimply reflect an artifact of a general slowing in normalaging: the slower the participant is, the larger the primingeffects are. A participant with very long response times(RTs) in the control condition (tiger–hammer) has morechance of showing a larger decrease in RT when the targetis preceded by a related prime (tiger–lion), in comparisonwith a participant already fast in the control condition.Moreover, Lyons, Kellas, and Martin (1995), using a lexicaldecision task, observed equivalent priming effects between

a “fast” older group and a young group and increasedpriming for a “slow” older group compared with the younggroup.

Finally, a review of the literature indicates that theseincreased priming effects with age can occur in some ex-perimental conditions that incite the participant to developattentional strategies (Laver & Burke, 1993; Lyons et al.,1995; Myerson et al., 1997), such as expectancy mecha-nisms or postlexical semantic matching processes (seeNeely, 1991, for a review). These attentional processes arealtered in normal aging (Hasher & Zacks, 1979; Jennings &Jacoby, 1993). The expectancy mechanism is under thestrategic control of the participant and accounts for thepriming effects via the assumption that the participant usesthe prime to generate an expectancy set that consists ofpotential targets that are related to the prime: If the partic-ipant notices that the prime is sometimes followed by arelated word, he or she can try to guess what the target willbe. This mechanism facilitates the processing of expectedtargets and inhibits the recognition of unexpected targets.This strategic mechanism occurs with relatively high pro-portions of related pairs and with a long time intervalbetween the onset of the prime and the target (stimulus–onset asynchrony; SOA). The postlexical semantic match-ing process occurs if the participant notices that there is asemantic relationship between the prime and the target: heor she will be biased toward a response that the stimulus isa word (no relationship would be noticed if the target was anonword). Thus, the participant answers more easily that thetarget is a word when it is related to the prime. On thecontrary, inhibitory effects occur if the participant noticesno semantic relation; he or she would tend to answer that thetarget is a nonword, and this would slow down the “yes”response, especially if the nonword ratio is high (Neely,Keefe, & Ross, 1989).

The objective of the present study was, therefore, toassess semantic priming effects in normal aging and toconfirm, if we observe a hyperpriming effect, that this effectis the result of methodological weakness in the protocol.More precisely, we wanted to investigate whether slowerRT can account for hyperpriming in normal aging. Thus,this study has the fundamental aim of verifying the integrityof the content and the organization of semantic memory innormal aging using a semantic priming paradigm by com-paring the semantic priming effects of a young group and anolder group obtained from a lexical decision task. This taskwas exactly the same as that used in our previous studies(Giffard et al., 2001, 2002) in which hyperpriming effectswere observed in AD in spite of the neutralization of theattentional processes and the attenuation of the influence ofthe cognitive slowing.

In this lexical decision task, in which we investigatedwhether, and to what extent, cognitive slowing characterizesthe priming effects found in older participants, we comparedtwo conditions. First, the slowing effect was not controlled,and the priming effects were, therefore, expressed in rawscores (unrelated condition RT � related condition RT).Second, to express semantic priming effects independentlyof overall cognitive slowing, we conducted regression anal-

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yses of related RT on the unrelated RT to obtain residualscores statistically independent of unrelated RT. Buchananet al. (1994) used a similar method in a study of schizo-phrenia to control for the response slowness of the patients.Moreover, we minimized the intervention of attentionalmechanisms with the help of automaticity criteria: that is,using a low proportion of related words (� 20%), using ashort SOA (� 250 ms), emphasizing low attention to theprime (the participant just had to answer to the target), andusing the same proportion of word targets and nonwordtargets (Neely, 1991; Posner & Snyder, 1975). Finally, inorder to undertake a detailed exploration of the structure ofsemantic memory in normal aging, we used a methodologyused in studies of AD, which is specifically designed toexplore the attribute and coordinate relations in semanticmemory. In this disease, the preservation of superordinateinformation, contrasting with an impaired knowledge of thesemantic attributes, has been shown in several studies (e.g.,Desgranges, Eustache, Rioux, de la Sayette, & Lechevalier,1996; Martin & Fedio, 1983; Warrington, 1975). In thepresent study, in order to assess categorical and attributeknowledge of an older group, we used, in the lexical deci-sion task, two types of word pairs; some were relatedaccording to a coordinate condition (tiger–lion), in whichthe prime and the target belonged to the same semanticcategory and shared the same semantic level, and others,according to an attribute condition (tiger–stripe), in whichthe target was a specific attribute of the prime concept.

We make the assumption that, if the semantic network isintact in the older participants, and given that this strictmethodology (absence of attentional mechanisms, cognitiveslowing controlled) is used, the semantic priming effects inthe older and young groups should be equivalent, therebyindicating a preserved content and organization of semanticmemory. A hyperpriming effect may be observed just whenthe performances are in raw scores, that is, when the slow-ing effect is not controlled for. Moreover, similar primingeffects—expressed as residual RT independent of the cog-nitive slowing—between the two groups of participants inthe coordinate and attribute conditions should argue in favorof the integrity of the hierarchical structure of semanticmemory with aging.

Method

Participants

Twenty young and 21 older participants took part in the study.The young participants (15 men and 5 women) had a mean ageof 23.5 years (SD � 2.8 years; range � 20–30 years). Olderpersons (4 men and 17 women), with a mean age of 77.9 years(SD � 8.5 years; range � 61–90 years), were volunteers recruitedthrough personal contact. The average number of years of educa-tion was 12.8 (SD � 2.2) for the young participants and 11.2(SD � 2.1) for the older participants (z � �2.19, p � .03).1 Thecriteria for the selection of the participants were the following:They had to be right-handed and be without any history of neu-rological or psychiatric illness. To eliminate all risk of includingparticipants with dementia, all the older participants were screenedusing the Mini-Mental State Examination (MMSE; Folstein, Fol-stein, & McHugh, 1975) and the Dementia Rating Scale (DRS;

Mattis, 1976). The mean MMSE score was 28.6 (SD � 1.16;range � 27–30), and the mean DRS score was 138.2 (SD � 2.2;range � 136–142). None of the participants included in this studyhad dementia.

Materials

The lexical decision task used was similar to that of our previousstudies in AD (Giffard et al., 2001, 2002). There were 30 relatedpairs of words: 20 pairs of words semantically related and of thesame semantic level (coordinate relation; tiger–lion) and 10 pairsof words in which the target was a specific attribute of the prime(attribute relation; zebra–stripe). These pairs were drawn fromword association norms (Lieury, Iff, & Duris, 1976; Oleron &Legall, 1962; Rosenzweig, 1970). We showed 100 young partic-ipants 60 of the first written words stemming from those norms:For each of them, they had to give the first word that came to mind.From the pairs of words thus obtained, we selected 30 homoge-neous words according to the association frequency. The nouns,which were all concrete and imageable, were 3 to 10 letters long,and the mean lexical frequency was 60 per million (Brulex; Con-tent, Mousty, & Radeau, 1990). In the two sets of pairs, the wordswere balanced in terms of length (coordinate: 6.1 letters; attribute:5.3 letters), lexical frequency (coordinate: 75 per million; attribute:82 per million), and association frequency (coordinate: 43%; at-tribute: 47%) with no extreme value in any condition. The seman-tically related pairs were also associated because associativestrength is an important determinant of the amount of priming(Moss, Tyler, Hodges, & Patterson, 1995). To ensure that anypriming could not be attributed to the frequency of a co-occurringword, the association frequency was never maximal and was thesame in both related conditions (coordinate and attribute).

The 30 related pairs were included in a list of 300 pairs. All theprimes were words. All the words were nouns. In order to mini-mize the intervention of postlexical attentional processes, we madethe likelihood of encountering a word versus a nonword in thetarget position 50%. Among the pairs in which the target was aword, 20% were semantically related (coordinate or attribute con-dition) and 80% shared no semantic or associative link, whichhelps prevent the participant’s expectancy about the nature of thetarget. The nonwords, which were all pronounceable, were createdby replacing one letter per syllable of a concrete word.

The task was divided into four blocks lasting about 5 min eachand separated by an interval of a few minutes. The distribution ofthese pairs (coordinate, attribute, unrelated words, word–nonword)was done in the same way in the four blocks. In each block, thepseudorandomized distribution of the pairs was the same for allparticipants and respected the following constraints: There werenever more than five occurrences of word or nonword targets in asequence, and the related pairs never occurred at the beginning ofa block and never occurred one next to another.

Procedure

The task was computerized and visual and was performedindividually. Stimuli were presented using the software SuperLab(xxxx; Version 1.68), which allows RT to be measured accuratelyto 1 ms. All stimuli were centered on the screen and were 2 cmhigh.

1 When we changed the composition of the two groups so that,on average, there is no difference in education level (1 young and 2older participants were removed), the whole pattern of resultspresented in the Results section did not change (data are notshown).

3HYPERPRIMING IN NORMAL AGING

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During a trial, the participant saw on the screen a fixation pointlasting 500 ms followed by a prime word for 200 ms. Thereafter,the screen remained blank for 50 ms; the SOA was 250 ms, a timeinterval that was too short to enable the participant to anticipate thenature of the target. Subsequently, the target stimulus appeared andremained visible until a response was made. Then, the screen wasblank for 1,500 ms and another trial started. In order to favor theautomaticity of the task, each participant was instructed to respondfor the target only: If he or she recognized, in the series of letters,a French word, he or she had to press, as fast as possible, the “yes”key with his or her dominant hand. If the series had no meaning forthe participant, he or she pressed the “no” key with his or her otherhand. In order to familiarize the participant with the task, a listof 30 practice trials (unrelated word pairs and word–nonwordpairs) was given.

Priming effects in raw scores are based on differences of RTbetween unrelated and related conditions. To express primingeffects independently of overall cognitive slowing, regressionanalyses of coordinate RT and attribute RT on the unrelated RT aredone separately. The residuals—which represent what remainsunexplained after the variable unrelated RT has explained all thevariation it can in the variables coordinate and attribute RTs—areworked out. These residual RTs are statistically independent ofunrelated condition RTs and therefore appropriate to study primingeffects. It is common practice to scale the residuals so they all havethe same variance. The most frequently used method to do so is to“studentize” the residuals as follows:

ti �ri

��i��1 � hi

,

where ti is the scaled residual for the ith individual; ri is the rawresidual for the ith individual; and �(i) is the estimate of thevariance of the errors excluding the ith individual from the calcu-lation and is given by

�2�i� �

�r�2

n � p � 1�

ri2

�n � p � 1��1 � hi�,

where n is the sample size (41 in our case); p is the numberof parameters in the model (two for the current study); and hi

is the ith diagonal element of the matrix H defined as H �X(XTX)�1XT, where X is the matrix of regressors.

Let us call ti the t score. This t score has a Student’s distributionwith n � p � 1 degrees of freedom.

Statistical Analysis

Nonparametric Wilcoxon–Mann–Whitney rank-sum tests wereused to compare several performances between the young and theolder groups: years of education, number of outlier responses,

errors in the lexical decision task, unrelated RTs, semantic primingeffects, and residual studentized scores. Wilcoxon tests for pairedsamples were carried out in order to compare in each age groupunrelated and coordinate RT, and unrelated and attribute RT, inorder to see if the priming effects are significant. This test was alsoused to compare, in each group, coordinate priming effects withattribute priming effects, and coordinate t scores with attribute tscores. We used a chi-square analysis to compare the sex distri-bution of the groups. To delimit the respective role of severalvariables (cognitive slowing, age, education, gender) on the se-mantic priming effects, we conducted a multiple regressionanalysis.

Results

We report only results of the three conditions for whichthe response is “yes” (coordinate, attribute, unrelated):These conditions are those that permitted calculation of thesemantic priming effects. Moreover, the errors of the olderparticipants (see Table 1), which were in most cases imme-diately self-corrected, were 4.1% and were not significantlymore numerous than those of young participants (3.7%, z ��0.18, p � .85), whatever the condition was. Likewise, inorder to ensure that the performances were not influencedby extreme scores, in each condition, response latenciesexceeding 3 standard deviations above each participant’smean were treated as outliers and were therefore excludedfrom further analysis, and the mean was calculated againwithout them. The mean number of outliers was 4.1(SD � 2.4) for the young group and 5.1 (SD � 2.6) for theolder group. The difference was not significant (z � �1.2,p � .23).

The RT and errors of both groups are presented in Ta-ble 1. On targets preceded by an unrelated word, olderparticipants had a mean RT of 878.51 ms. This is signifi-cantly slower than the same condition for young participants(610.83 ms; z � �4.69, p � .0001).

When the semantic priming effects are in raw scores(unrelated RT � related RT; see Figure 1), the youngparticipants showed a mean priming effect of 40.02 ms inthe coordinate condition (Mdn � 32.79 ms) and a meaneffect of 50.51 ms in the attribute condition (Mdn � 50.83ms). These priming effects were significant, Wilcoxon testfor paired samples, z � �3.88, p � .0001, for the coordi-nate priming effects, and z � �3.92, p � .0001, for theattribute priming effects (as the number of tests is small ineach comparison, all probabilities are uncorrected). Theolder participants showed a mean priming effect of 64.63ms in the coordinate condition (Mdn � 59.03 ms) and 75.66

Table 1Lexical Decision Response Times (in Milliseconds) to Word Targets and AccuracyData for Young and Older Participants

Group

Experimental conditionUnrelatedconditionCoordinate Attribute % error

M SD M SD M SD M SD

Young 570.81 87.77 560.32 81.13 610.83 88.59 3.70 2.36Older 813.88 151.46 802.85 169.25 878.51 170.72 4.10 3.43

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ms in the attribute one (Mdn � 68.39). These effects weresignificant, Wilcoxon test for paired samples, z � �4.09,p � .0001, and z � �3.77, p � .0002, respectively. Wil-coxon–Mann–Whitney tests revealed a significant differ-ence in the coordinate priming effects between the youngand the older groups, z � �2.10, p � .04, and there was amarginally significant difference in the attribute primingeffects (z � �1.81, p � .06). To compare, in each agegroup, the semantic priming effects in the coordinate con-dition with those in the attribute condition, we conductedWilcoxon tests for paired samples. These analyses showedequivalent priming effects in coordinate and attribute con-ditions in the older group (z � �1.23, p � .22) as in theyoung group (z � �1.34, p � .07).

The two age groups differed not only in global RT butalso in education ( p � .03) and sex distribution ( p � .001).To delimit the respective role of cognitive slowing, age,education, and gender on the semantic priming effects, weconducted a standard multiple regression analysis, withpriming effects in raw scores as the dependent variable, forthe 41 participants. Four independent variables were en-tered: age, years of education, gender, and RT in the unre-lated condition (chosen as index of cognitive slowing).Globally, the independent variables as a whole significantlyinfluenced the variation of the semantic priming effects,R2 � .23, F(4, 75) � 5.26, p � .0009. However, the onlysignificant predictor of the priming effects in raw scores wasRT in the unrelated condition. Partial correlation coeffi-cients derived from the analysis are presented in Table 2.They illustrate the fact that age, as well as education, failedto predict the priming scores.

When the scores are expressed independently of overallcognitive slowing, that is, as regression residual scores (seeFigure 2), a Wilcoxon–Mann–Whitney test shows that the tscores are identical in the young and older groups in coor-dinate and attribute conditions (z � �0.06, p � .94, andz � 0.40, p � .68, respectively). Therefore t scores of theyoung and older groups are identical in each condition. Thedifference between the t scores in the coordinate conditionand those in the attribute condition is not significant in theyoung group, z � �0.66, p � .51, nor in the older group(z � 0.30, p � .76).

Discussion

The main finding of the present investigation was thatolder and younger participants exhibited equivalent seman-tic priming effects in both the coordinate and attribute

Figure 1. Dispersion of the semantic priming effects in raw scores (unrelated RT � related RT) for each participant group (young andolder) in the coordinate and attribute conditions. The boxes have lines at the lower quartile, median, and upper quartile values. The barsextending from each end of the boxes show the extent of the rest of the data. There was a significant difference between the two groupsin the coordinate condition ( p � .04) and a marginally significant difference in the attribute condition ( p � .06). RT � response time.

Table 2Partial Correlation Coefficients of Independent Variables

Variable pr SE t p

Constant 27.28 39.98 0.68 .50Age 0.20 0.24 0.82 .42Education �1.41 2.13 �0.66 .51Gender �9.94 9.39 �1.06 .29Unrelated RT 0.07 0.03 2.21 .03*

Note. The dependent variable was semantic priming effects inraw scores. Unrelated RT � response times in the unrelatedcondition.* p � .05.

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conditions when the scores were expressed independently ofthe overall cognitive slowing that characterizes the olderpopulation. On the contrary, when the priming effects wereanalyzed in raw-score form (unrelated RT � related RT),they were significantly greater for older than for youngadults in the coordinate condition, and the difference wasmarginally significant in the attribute condition.

As expected, mean RT in the unrelated condition waslonger in the older group than in the young group. More-over, multiple regression analyses showed that the factor RTin the unrelated condition (the index of cognitive slowing)was the only significant predictor of semantic priming ef-fects when they were in raw-score form. We can concludethat there is actually a relation between increased semanticpriming effects (in raw scores) and the cognitive slowinglinked to normal aging. To avoid the influence of thisartifact on the priming effects, expressing the data for eachparticipant as studentized residual-related (coordinate andattribute) RT scores statistically independent of variations inunrelated RT seems to be a satisfactory alternative. Thisconclusion is strengthened by Lyons et al.’s (1995) study,which suggests that the priming effects of fast older partic-ipants are similar to those of young participants, whereas theperformances of slow older participants are greater thanthose of young participants. Burke et al. (1987) used anothermethod to control for the effects of the cognitive slowing;they expressed priming scores in percentages and thereforeobtained equivalent priming in a young and an older group.However, the scores of this study are difficult to comparewith ours because the protocol of Burke and colleagues

involved attentional processing: Before the test, the partic-ipants were informed that the prime could serve as a clue toguess the target.

Indeed, unlike most studies concerning semantic primingeffects in normal aging, the results of the present investiga-tion were derived from a protocol that was specificallydesigned to limit the intervention of controlled processes.Hasher and Zacks (1979) proposed that controlled but notautomatic processes are diminished during aging, and theuse of a semantic priming paradigm has the advantage,contrary to explicit tests of semantic memory, of minimiz-ing their implementation. However, most of the studiesshowing increased semantic priming in older groups(Balota, Black, & Cheney, 1992; Laver, 2000; Lyons et al.,1995; Myerson et al., 1997) used tasks that favor the inter-vention of attentional processes (long SOAs with a highproportion of related pairs).

However, our results clearly show that the use of aprotocol that minimizes the intervention of attentional pro-cesses may be necessary, but not at all sufficient, to preventan increase of the priming effects of older participants incomparison to young participants: In spite of use of aprotocol designed to produce automatic processing only, weobserved increased semantic priming—in raw scores—forthe older group. Nevertheless, in order to conclusively dem-onstrate this effect of attentional processes on the amount ofsemantic priming, one would have to conduct a study inwhich the two processes, automatic and attentional, aretested. With such an experiment, we suppose that, in anattentional condition, the priming effects of older partici-

Figure 2. Dispersion of the “studentized” residual scores (t scores) for each participant group (young and older) in the coordinate andattribute conditions. The bars extending from each end of the boxes show the extent of the rest of the data. There was no significantdifference between the two groups of participants in the coordinate condition ( p � .94) or in the attribute condition ( p � .68).

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pants would be increased too, but their extent may be higherin comparison with an automatic condition. Thus, we sup-pose that the intervention of attentional processes alone isnot sufficient to produce increased priming effects in ag-ing—the cognitive slowing is the sine qua non—but theycould increase the priming effects even more.

The results of this study taken as a whole strengthen thehypothesis that, after minimizing the influence of the cog-nitive slowing, semantic priming effects are intact duringnormal aging: This goes in the direction of a preservation ofthe semantic memory system with aging. Otherwise, theresults suggest that the amount of spreading activation ac-cumulated in the target node is the same across age and thespeed of spreading semantic activation does not seem toslow with age in spite of the pervasive slowing of othercognitive processes: The short SOA used in this study (250ms) limited the time available for transmission of activation.The results obtained show that older participants do notrequire longer SOAs than young adults to benefit fromsemantic context (see also Balota et al., 1992; Bowles,1994; Burke et al., 1987). However, as shown by Howard,Shaw, and Heiser (1986), who used a shorter SOA (150 ms),only young participants obtained significant priming effects.

Finally, in accordance with the hierarchical structure ofsemantic memory, the related pairs of words were dividedinto two conditions (coordination and attribution). Alter-ations in that kind of structure are characteristic of AD; theyfollow a bottom-up evolution with an initial deficit of theattributes of concepts. Recently, we used the methodologi-cal paradigm used in the present study to assess deficits ofsemantic memory in AD (Giffard et al., 2001, 2002). In thecoordinate condition only, we observed increased primingeffects in patients with AD in comparison with controls whodid not have AD, even though slowing and attentionalprocesses were controlled. On the contrary, in the presentstudy, when these two processes were controlled (overallslowing and attention), the semantic priming effects weresimilar for young and older participants in the coordinatecondition as in the attribute condition. This result reflectsthe absence of alteration in the hierarchical structure ofsemantic memory, as already showed by Eustache, Des-granges, Jacques, and Platel (1998). We must add that themethods used to suppress the overall slowing were differentin the present study (regression analyses to obtain residualscores) and our previous studies on AD (priming effectsexpressed in percentages on the unrelated RT). Neverthe-less, in the present study, we used the percentage method,too, for comparison with the data issued from the regressionanalyses, and we obtained the same results (data notshown).

The results of the present study confirm that the hy-perpriming phenomenon observed in AD would be theresult not of the intervention of attentional processes or ofthe cognitive slowing effect (even if they are increased withthe disease) but, more probably, of a semantic memorydeficit. On the contrary, in normal aging, the hyperprimingeffect is just observed when several variables are not con-trolled: This phenomenon would more probably be in part aconsequence of cognitive slowing in normal aging.

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Received June 10, 2002Revision received February 10, 2003

Accepted February 11, 2003 �

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