Effects of Stimuli Repetition and Age in False Recognition

Abstract

The aim of the current study is to examine the effects of stimuli repetition and age in false recognition using the Deese–Roediger–McDermott experimental paradigm. Two matched samples of 32 young adults and 32 healthy older adults studied 10 lists of six words associated with three non-presented critical words. On half of the lists, the words were presented once, and on the other five lists, the words were presented three times, always following a same sequential order. After each study list, participants performed a self-paced recognition test containing 12 words: the 6 studied words and 6 other non-studied words (the 3 critical words and 3 distractors). The results show that false recognition increases with age and declines in both samples with repetitions (although more in the young adults than in the older people). Results are discussed in relation to the dual-process theories of (false) memory.

Keywords

False recognition aging repetition memory false memories

Introduction

The aim of the current study is to examine the effects stimuli repetition at encoding and age in false recognition using the Deese–Roediger–McDermott (DRM) experimental paradigm (Deese, 1959; Roediger & McDermott, 1995). In a DRM experiment, the participants study lists of words (e.g. pipe, cigar, ashtray…) associated with a non-studied-related word (or critical word; e.g. tobacco). Subsequently, this critical word is recalled or recognized more frequently than other non-studied unrelated words, giving rise to a robust false memory effect that has been addressed in a large body of literature (see Gallo, 2010, for a review). Through the use of this paradigm, false recognitions and false memories have been also shown to increase with age (see Devitt & Schacter, 2016, for a review). These two robust effects have been mainly explained by the activation-monitoring theory (Gallo, 2001). The activation-monitoring framework (Roediger, Watson, McDermott, & Gallo, 2001) establishes that, during the study task, both the studied items and the items semantically related to them are activated (due to spreading activation from the former to the latter). At the time of retrieval, the subject carries out a conscious monitoring process to distinguish between studied and non-studied items. Given that non-studied lure items can be highly activated because they are related to the studied items, source-monitoring errors can occur (Johnson, Hashtroudi, & Lindsay, 1993), leading to a false memory. However, as young adults have a well-preserved capacity to recollect item-specific information, they can use it to reduce their false alarm rates by employing conscious monitoring strategies such as “recall-to-reject” (Brainerd, Reyna, Wright, & Mojardin, 2003). This strategy involves rejecting a lure because the participant can consciously recollect some instantiating targets (e.g. “I remember that I studied items A, B, and C, but not item D, so I reject D”). Many studies have found support for the correct use of this recollection-based monitoring strategy in young people, but less in healthy older people or patients with cognitive impairment, due to their aforementioned item-specific deficits (Gallo, Sullivan, Daffner, Schacter, & Budson, 2004; Pitarque et al., 2016; Pitarque, Sales, Meléndez, & Algarabel, 2015).

In general terms, the activation-monitoring theory, as well as other frameworks as the fuzzy trace theory (Reyna & Brainerd, 1995), can be considered as dual-process memory models (Koen & Yonelinas, 2014; Schoemaker, Gauthier, & Pruessner, 2014; Yonelinas, 2002) in the sense that they consider that our memory for a past experience can be based either on a conscious, explicit, recollection of contextual details from that experience or on an automatic, implicit, estimation of the strength of that memory trace in the absence of contextual details (familiarity). Evidence from neuropsychological, neuroimaging, and neurophysiological studies of humans and animals seems to indicate that different medial temporal lobe regions are involved both in true and false memories (Devitt & Schacter, 2016; Gallo, 2010): activity in the hippocampus is associated with recollection, whereas activity in the perirhinal cortex is related to familiarity (Eichenbaum, Yonelinas, & Ranganath, 2007).

Stimuli repetition at encoding, as a means of increasing learning, allows us to analyze the role that activation and monitoring processes play in both true and false recognition and how they evolve throughout the life cycle (Benjamin, 2001; Gallo et al., 2004; Jennings & Jacoby, 1997; Watson, McDermott, & Balota, 2004). Stimuli repetition is well known to increase true memories both in young and healthy older adults (Tussing & Greene, 1999; Watson et al., 2004), because practice improves both the items encoding and their retrieval process (either based on recollection or familiarity). However, experimental results about its effect on false memories in young people are inconsistent (Dubuisson, Fiori, & Nicolas, 2012; Seamon et al., 2002; Tussing & Greene, 1999), most studies showing that repetition decreases false memories (Benjamin, 2001; Budson, Daffner, Desikan, & Schacter, 2000; Kensinger & Schacter, 1999; Tussing & Greene, 1999, experiment 5; Watson et al., 2004), but others showing that repetition has no effect on false memories (Dubuisson et al., 2012; Tussing & Greene, 1997, 1999, experiments 1–4), or has an inverted-U-shaped effect (Seamon et al., 2002). And the same pattern of inconsistent results is found in healthy older people: most studies showing that repetition decreases false memories in healthy older people (Budson et al., 2000, 2002; Kensinger & Schacter, 1999; Schacter, Verfaellie, Anes, & Racine, 1998), but others showing that repetition increases false memories (Benjamin, 2001) or has no effect on them (Abe et al., 2011; Watson et al., 2004). Thus, giving these inconsistent results, we intend to manipulate stimuli repetition in a DRM paradigm, comparing young and healthy older people, as a way to analyze how practice and aging affect false recognition.

In our opinion, the aforementioned discrepant results about the role of repetition on false memories could be due to several reasons: One could be related to the different time allocated to study the items. For example, McDermott and Watson (2001) showed that false recognition increases between 20-ms and 250-ms presentation durations, but decreases between 250-ms and 5-s duration ranges. In this sense, Seamon et al. (2002) showed that following 20-ms exposures false recognition increased monotonically with repetitions, whereas following 2-s exposures false recognition first increased and then decreased with additional repetitions. Watson et al. (2004) showed that both young and old adults reduced their false recall more with 2.50-s presentation rates than with 1.25-s exposures. In general terms, repetitions seem to lead to a decrease in false memories in healthy people when available time is enough during the study phase to explicitly process the stimuli, but tend to increase false memories as study times become faster (e.g. below 250 ms) due to an implicit processing of stimuli (Dubuisson et al., 2012; Watson et al., 2004). A second reason could be that the procedures used to manipulate repetitions were quite dissimilar, from massed to spaced repetitions, and with various intervals between them (Dubuisson et al., 2012). For example, Tussing and Green (1999) found no effect of repetitions on false recognition when repeated stimuli were studied in a random order within lists (experiments 1–4), but found a decrease on false recognition when repeated stimuli were studied following always the same order within lists (blocked repetitions; experiment 5). A third reason that could explain the discrepant results found about the role of repetition on false memories could be related to some methodological aspects when using the DRM paradigm, such as the large number of lists (and words) to be studied by the subjects, since each list is commonly associated with only a critical word. And this problem is increased when we manipulate repetitions, which logically increase the number of stimuli to be studied (but not the number of critical words). In an attempt to solve this problem, some studies have included some kind of variations on the standard procedure to increase the number of critical words per study list. For example, Beato and Díez (2011) have recently developed a normative database of 60 six-word lists (e.g., bridal, newlyweds, bond, commitment, couple, to marry), each associated with three critical words (e.g., love, wedding, marriage). So, in an original way in literature, we intend to use these kind of norms to examine the role of repetitions and aging on false recognition, maximizing the critical words that can be elicited by each study list. Finally, another methodological aspect that could explain the discrepant results found about the role of repetition on false memories could be whether the basal level of false alarms on distractors (lures not related to the critical word) is or not included to estimate false recognition. It is known that older people (and especially those with cognitive impairment) tend to show a more liberal response than young people, which makes them increase their rates of both hits and false alarms (Budson, Wolk, Chong, & Waring, 2006). Thus, the recommendation would be to estimate both true and false recognition by subtracting the rates of false alarms on unrelated distractors (or words not related to the critical word, FAN) from the individual rates of hits (H) and false alarms on critical (FAC) words, respectively (Budson et al., 2006; Cadavid & Beato, 2017; Dubuisson et al., 2012; Seamon et al., 2002). So, we also intend to use this adjustment in our experiment to estimate both true and false recognition to shed light on the discrepant experimental results found in literature.

To sum up, as the effects of repetition and age on false memory are unclear and the experimental data are relatively inconsistent (Dubuisson et al, 2012; Seamon et al., 2002; Tussing & Green, 1999), we decided to carry out an experiment using the DRM experimental paradigm. Participants (32 young and 32 healthy older people) studied 10 lists each containing 6 words associated with 3 non-presented critical words (Beato & Díez, 2011; Cadavid & Beato, 2017). On half of the lists, the words were presented once, whereas on the other half of the lists, the words were presented three times, always following a same sequential order (blocked repetitions; Tussing & Green, 1999). After each study list, the participants performed a self-paced recognition task (old/new) of 12 words: the 6 studied stimuli within each list and 6 other non-studied stimuli consisting of the 3 critical words and 3 unrelated distractors from other non-studied lists (i.e. Meade, Watson, Balota, & Roediger, 2007). We decided to use an immediate recognition test after each study list because it is well known that this type of presentation leads to greater levels of true and false recognition in healthy adults than the presentation of all study lists together followed by just one global recognition test (Algarabel, Pitarque, Sales, Meléndez, & Escudero, 2015; Brainerd, Reyna, & Forrest, 2002; Tussing & Greene, 1997). On the study tasks, each word was visually presented for 1 s to ensure an adequate encoding and avoiding ceiling or floor effects in young or older people, respectively (the exposure time was chosen by a previous pilot experiment). Finally, we also decided to use blocked repetitions to avoid likely null results when using randomized repetitions (Tussing & Green, 1999, experiments 1–4).

It is difficult to make predictions about the effects of repetitions and aging on false recognition because activation and monitoring processes have opposite effects on critical words (Gallo et al., 2004; Jennings & Jacoby, 1997; Seamon et al., 2002; Tussing & Green, 1999), whereas repeated activation tends to increase false memories, repetition can also decrease them by improving accurate monitoring processes (e.g. recall-to-reject). We hypothesize that if older people respond based mainly on the activation of the items, an increase in their false recognition with the repetitions would be expected. In the case of the young people, a reduction in their rates of false recognition with the repetitions would be expected because practice would allow them to improve their recollection-based monitoring strategies. If the older people also use practice to improve their recollection-based monitoring strategies a reduction in their rates of false recognition with the repetitions would be also expected, but this reduction should be, in any case, less than what is observed in the young people, given their well-known binding deficits (Old & Naveh-Benjamin, 2008) and recollection deficits (Koen & Yonelinas, 2014).

Method

Participants

Participants were 32 young adults (Psychology undergraduates at the University of Valencia, Spain; 6 men and 26 women, mean age = 22.19 years, SD = 3.46 years) and 32 older adults (recruited from several courses for elderly people conducted in the city of Valencia; 9 men and 23 women, mean age = 65.69 years, SD = 6.78 years). Sample size was chosen by a priori power analyses (1 − β = .95, α = .05; Faul, Erdfelder, Lang, & Buchner, 2007). All the participants gave their informed consent to free participate and reported being in good physical and mental health, with no known memory impairments. In this regard, the mean on the Mini-Mental State Examination (Folstein, Folstein, & McHugh, 1975) for the older adults was 29.41 (SD = 0.84), thus showing no memory impairment. The two groups were matched for gender (χ₁²= 0.78), years of education (t_42.84 = 1.98, means of 15.84 and 13.88 years, and SD of 2.28 and 5.14, for young and older people, respectively) and Wechsler Adult Intelligence Scale vocabulary (Wechsler, 2001; t₆₂ < 1, means of 39.20 and 38.91, and SD of 6.90 and 11.77, for young and older people, respectively). Subjects were selected to match these variables of interest. There were no more variables collected in our study. There were no data excluded from the statistical analysis (Simmons, Nelson, & Simonsohn, 2011).

Materials

We selected two sets (A and B) of 10 lists of words from the Beato and Díez (2011) database; each list contained six study words, associated with three critical words. These two sets of 10 lists were matched for percentage of true recognition (mean set A = 78.59, SD = 9.31; mean set B = 73.32, SD = 9.90), false recognition (mean set A = 38.33, SD = 13.06; mean set B = 37.66, SD = 9.34) and backward associative strength (mean set A = 2.20, SD = 0.37; mean set B = 2.54, SD = 0.37). Previous research has shown that backward association strength is to be closely related to the production of false memories (Roediger et al., 2001). Sets A and B were counter-balanced across subjects. In later analyses of our results, both sets produced statistically similar results for hits, false alarms to the critical words, and false alarms to the unrelated distractors.

Procedure

Each participant performed the experiment individually, seated in front of a computer. The experiment began by studying a list of 6 words (either presented once or repeated 3 times, and associated with 3 non-presented critical words; Beato & Díez, 2011) and then performing its corresponding recognition test containing 12 words (the 6 studied words, the 3 critical words, and 3 other distractor words). This process was repeated 10 times on 10 study and recognition lists. On the study tasks, each word was visually presented for 1 s (with an inter-stimuli period of 500 ms). On half of the study lists, words were presented once, and on the other half, three times, in an alternating and counter-balanced way between subjects. Thus, in the even subjects, the words on lists 1, 3, 5, 7, and 9 were presented once (i.e., 6 study words, in the same order in which they appear in Beato & Díez, 2011), whereas the words on lists 2, 4, 6, 8, and 10 were presented three times (i.e., 18 study words in three similar cycles, each following the same order of presentation as in Beato & Díez, 2011; called spaced repetitions by Dubuisson et al., 2012, or blocked repetitions by Tussing & Green, 1999, experiment 5). In the odd subjects, lists 1, 3, 5, 7, and 9 were composed of words presented three times and lists 2, 4, 6, 8 and 10 were composed of words presented once. After each study list, the participants performed a distractor task for 1 min (simple arithmetic tasks) followed by its corresponding self-paced recognition task (old/new) with 12 stimuli: the 6 studied words within each list and 6 other non-studied words (the 3 critical words within each list and 3 unrelated distractors from other non-studied lists: a critical word and two words unrelated to the studied list). After each recognition test, a new distractor task was performed for 1 min. In summary, each participant performed 10 study tasks and 10 recognition tasks, each task spaced by 1-min distractor task. Participants were informed that the words would sometimes be repeated, and other times they would not.

Results and discussion

Table 1 shows the overall results of our experiment. First, to examine whether there was a false recognition effect within the non-repeated stimuli, which would validate our materials and procedure, two analyses of variance (ANOVAs) were carried out (one for young people and another for older people) with the type of word (studied, critical, distractor, and control critical) as a within-subject factor (Cadavid, Beato, & Fernandez, 2012). Both ANOVAs showed as significant the effect of the type of word (F_{3, 93} = 399.52, p < .001, η²_p = .93, 95% CI [.90, .94], and F_{3, 93} = 356.15, p < .001, η²_p = .92, 95% CI [.89, .94], for younger and older people, respectively). In the young people (Table 1), post hoc Bonferroni comparisons showed that the mean proportion of hits on studied words (H = 0.84, 95% 95% CI [.81, .87]) was significantly greater than the mean proportion of FAC words (FAC = 0.45, 95% CI [.37, .54]), which, in turn, was significantly greater than the proportion of false alarms on distractors and control critical words (0.01, in both cases). In the older people, post hoc Bonferroni comparisons showed a similar pattern of results; that is, the proportion of hits on studied words (H = 0.77, 95% CI [.73, .82]) was significantly greater than the proportion of FAC words (FAC = 0.63, 95% CI [.54, .71]), which, in turn, was significantly greater than the proportion of false alarms on distractors (0.017, 95% CI [.001, .03]) and control critical words (0.006, 95% CI [−.006, .02]), with no significant differences between these two latter conditions. Thus, given that in both samples there were no significant differences between the proportion of false alarms on distractors and control critical words, we decided to join up them just in one category, called FAN (Table 1). These results clearly show a significant false recognition effect in both samples within the non-repeated stimuli, which validates both the materials and the procedure we have used.

Table 1.

Mean proportions (and SE) of hits, FAC FAN, and estimations of true and false recognition in young and healthy older people for non-repeated and repeated conditions.

	Young (n = 32)		Healthy older (n = 32)
	Non-repeated	Repeated × 3	Non-repeated	Repeated × 3
Hits (H)	0.84 (0.02)	0.89 (0.01)	0.77 (0.02)	0.84 (0.01)
FAC	0.45 (0.04)	0.24 (0.04)	0.63 (0.04)	0.50 (0.04)
FAN	0.02 (0.01)	0.002 (0.003)	0.02 (0.01)	0.004 (0.003)
True recognition (H-FAN)	0.82 (0.02)	0.89 (0.01)	0.75 (0.02)	0.84 (0.01)
True recognition (A′)	0.95 (0.005)	0.97 (0.002)	0.93 (0.005)	0.95 (0.002)
False recognition (FAC−FAN)	0.43 (0.04)	0.24 (0.04)	0.61 (0.04)	0.50 (0.04)
False recognition (A′)	0.84 (0.01)	0.74 (0.02)	0.88 (0.01)	0.85 (0.02)

Note. FAN: false alarms on unrelated distractors; FAC: false alarms on critical words.

True recognition

True recognition was estimated by subtracting the individual rates of false alarms on unrelated distractors (FAN) from the individual rates of hits (H). A mixed ANOVA 2 groups (young vs. older people; between-subjects) × 2 repetition conditions (non-repeated vs. repeated; within subjects) on the true recognition scores (H−FAN; Table 1) showed as significant the main effect of both variables, groups (F_{1, 62} = 11.70, p = .001, η²_p = .16, 95% CI [.03, .32]) and repetition conditions (F_{1, 62} = 30.69, p < .001, η²_p = .33, 95% CI [.15, .48]), indicating that true recognition was higher for young people than for older people (means of 0.86, 95% CI [.83, .88], and 0.80, 95% CI [.77, .82], respectively), and higher for repeated stimuli than for non-repeated stimuli (means of 0.86, 95% CI [.85, .88], and 0.79, 95% CI [.76, .82], respectively), as commonly shown in the literature (Tussing & Greene, 1999). The interaction was not significant (F_{1, 62} < 1), showing that the repetitions produced similar improvements in younger and older people, although with different basal levels (for young and older people’s means of .82 and .75, respectively; t₆₂ = 2.47, p = .016, 95% CI [.01, .13]), due to the binding deficits (Old & Naveh-Benjamin, 2008) and recollection deficits (e.g. Yonelinas, 2002) commonly found in older people.

True recognition was also estimated by A′ scores (Table 1), a non-parametric counterpart of the signal detection statistic d′ (e.g. Carneiro, Albuquerque, Fernandez, & Esteves, 2007). A mixed ANOVA 2 × 2 on the A′ individual scores mimetically replicated the former results (so, for simplicity, we do not repeat them again).

Participants were very precise in their answers when recognizing the non-repeated words. This global level of true recognition was higher than what was found in other normative studies using DRM lists with three critical words (0.63 in Cadavid & Beato, 2017; 0.66 in Cadavid et al., 2012; 0.74 in Beato & Díez, 2011). Likewise, the percentage of false alarms on the unrelated distractors was also low (0.02) compared to these studies (0.10 in Cadavid & Beato, 2017; 0.08 in Cadavid et al., 2012; 0.03 in Beato & Díez, 2011). These different results are probably due to having used an immediate recognition test after each study list, instead of using a global recognition test after all study lists (as in Beato & Díez; 2011; Cadavid & Beato, 2017; Cadavid et al., 2012).

False recognition

False recognition was estimated by subtracting the rates of FAN from the rates of false alarms on critical words (FAC). A mixed ANOVA 2 groups × 2 repetition conditions on the false recognition scores (FAC−FAN; Table 1) showed as significant the main effect of both variables, groups (F_{1, 62} = 16.59, p < .001, η²_p = .21, 95% CI [.06, .37]) and repetition conditions (F_{1, 62} = 40.19, p < .001, η²_p = .39, 95% CI [.21, .53]), which indicate that the level of false recognition was higher for older people than for young people (means of 0.55, 95% CI [.48, .63], and 0.34, 95% CI [.26, .41], respectively) and lower for repeated stimuli than for non-repeated stimuli (means of 0.37, 95% CI [.30, .43], and 0.52, 95% CI [.46, .58], respectively), as usual in literature (Devitt & Schacter, 2016; Tussing & Greene, 1999). These results give support again both the materials and the procedure we have used. The interaction was also significant (F_{1, 62} = 4.22, p = .044, η²_p = .06, 95% CI [.00, .20]), indicating that young people reduced more their false recognitions with repetitions than older people (means of 0.43, 95% CI [.36, .52], and 0.24, 95% CI [.15, .32], for the non-repeated and repeated stimuli, respectively, in young people; means of 0.60, 95% CI [.52, .68], and 0.50, 95% CI [.41, .58], for the non-repeated and repeated stimuli, respectively, in older people; Table 1). However, both samples significantly reduced their false recognitions with practice, as shown by the post hoc Bonferroni tests for the analysis of this significant interaction (t₃₁ = 7.58, p < .001, 95% CI [.15, .26], for the young people’s means of 0.43 and 0.24, for the non-repeated and repeated stimuli, respectively; and t₃₁ = 2.57, p = .015, 95% CI [.02, .19], for the older people’s means of 0.60 and 0.50, respectively).

False recognition was also estimated by A′ scores (Table 1; Carneiro et al., 2007). A mixed ANOVA 2 × 2 on the A′ scores mimetically replicated the former results (so, for simplicity, we do not repeat them again).

Overall, our experiment using in an original way new normative materials with greater number of critical words per study list, and controlling response bias, has clearly shown that older people elicit more false memories than young people, as established in the literature (Devitt & Schacter, 2016). However, in relation to the contradictory experimental data found in the literature, stimuli repetition during encoding reduces false recognition in both young people (coinciding with Benjamin, 2001; Budson et al., 2000; Kensinger & Schacter, 1999; Schacter et al., 1998; Tussing & Greene, 1999; experiment 5; Watson et al., 2004) and healthy older people (coinciding with Budson et al., 2000, 2002; Kensinger & Schacter, 1999; Schacter et al., 1998; Watson et al., 2004), although much more in the former group. These results seem to indicate that, with practice, both samples learn to improve their recollection-based monitoring strategies to reduce the rate of false alarms produced by the repeated activation of the stimuli, but being young people much more efficient than older people. But we must be cautious in generalizing our results as they may depend on the specific manipulation conditions we have used (e.g. 1-s presentations, massed repetitions, immediate tests, etc.). A more extensive research that also manipulates different presentation rates, other repetition types (e.g. randomized repetitions) and other types of tests (e.g. just one global recognition test) would increase the validity of our results, thus further research is needed along these lines.

In general terms, our results support the idea that there are two ways to retrieve knowledge from human memory, as the dual-process theories propose (Koen & Yonelinas, 2014; Schoemaker et al., 2014; Yonelinas, 2002): an implicit one, based on the automatic activation of the studied items and items related to them (or familiarity), and an explicit one, based on the conscious recollection of episodic traces from memory and the (correct or incorrect) use of inferential monitoring strategies. False recognition depends on the interrelationship between the two processes, as, for example, the dual activation-monitoring theory proposes (Benjamin, 2001; Gallo et al., 2004; Pitarque et al., 2015, 2016; Roediger et al., 2001; Seamon et al., 2002). The recollection or inferential capacity declines throughout the life cycle (as older people age, they tend to rely more on familiarity; Devitt & Schacter, 2016), whereas automatic processing remains stable throughout the life cycle or, at least, declines much more slowly than recollection (Koen & Yonelinas, 2014, 2016). And, as Devitt and Schacter (2016) have pointed out, this enhanced likelihood of memory errors in aging seem to be linked to neural declines in medial temporal and prefrontal brain areas. Our sample of older people consisted of cognitively healthy older people, and their explicit information processing capacity was probably preserved to a certain degree. If this is correct, the reduction observed in false recognition in our sample of older people would be expected to disappear in patients with mild cognitive impairment or Alzheimer’s disease. These patients would have to mainly use an automatic information processing, given their well-known recollection deficits (Budson et al., 2002). Results such as those offered in the studies by Abe et al. (2011), Gallo et al. (2004), or Pitarque et al. (2016) point in this direction, but further research is also needed along these lines.

Footnotes

Article Notes

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