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Journal of Clinical and Experimental Neuropsychology

ISSN: 1380-3395 (Print) 1744-411X (Online) Journal homepage: http://www.tandfonline.com/loi/ncen20

Control over interfering memories in eating


disorders

Davide Francesco Stramaccia, Barbara Penolazzi, Arianna Libardi, Aldo


Genovese, Luigi Castelli, Daniela Palomba & Giovanni Galfano

To cite this article: Davide Francesco Stramaccia, Barbara Penolazzi, Arianna Libardi, Aldo
Genovese, Luigi Castelli, Daniela Palomba & Giovanni Galfano (2017): Control over interfering
memories in eating disorders, Journal of Clinical and Experimental Neuropsychology

To link to this article: http://dx.doi.org/10.1080/13803395.2017.1313392

Published online: 11 Apr 2017.

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Download by: [Universita di Padova] Date: 11 April 2017, At: 06:24


JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY, 2017
http://dx.doi.org/10.1080/13803395.2017.1313392

Control over interfering memories in eating disorders


Davide Francesco Stramaccia a, Barbara Penolazzi b
, Arianna Libardia, Aldo Genovesec, Luigi Castelli a
,
Daniela Palombad and Giovanni Galfano a
a
Department of Developmental and Social Psychology, University of Padova, Padova, Italy; bDepartment of Life Sciences, University of
Trieste, Trieste, Italy; cAzienda Provinciale per i Servizi Sanitari, Trento, Italy; dDepartment of General Psychology, University of Padova,
Padova, Italy

ABSTRACT ARTICLE HISTORY


Introduction: Recent studies have suggested that patients suffering from either anorexia nervosa Received 27 September 2016
(AN) or bulimia nervosa (BN) exhibit abnormal performance in the ability to control cognitive Accepted 26 March 2017
interference in response selection. Method: We assessed the status of cognitive control in episodic KEYWORDS
memory by addressing the ability to inhibit interfering memories. To this end, we used the Anorexia nervosa; Bulimia
retrieval-practice paradigm, which allows for measuring both the beneficial and the detrimental nervosa; Cognitive control;
effects of memory practice. The latter phenomenon, known as retrieval-induced forgetting (RIF), Eating disorders; Memory
is thought to reflect an adaptive inhibitory mechanism aimed at reducing competition in memory suppression; Retrieval-induced
retrieval. Twenty-seven healthy controls and 27 patients suffering from eating disorders (either forgetting
AN or BN) performed a retrieval-practice paradigm and a control task addressing general
reactivity and filled a self-report questionnaire on impulsivity. Results: No differences between
patients and healthy controls were observed for the beneficial effects of practice. The same
pattern also emerged for RIF. However, when patients with AN and BN were analyzed separately,
a clear dissociation emerged: patients with AN displayed no hint of RIF, whereas patients with BN
showed an intact memory suppression performance. No group differences emerged in the
control task. Conclusions: Our findings suggest a specific impairment in the ability to suppress
interfering memories in patients with AN, thus extending current evidence of cognitive control
deficits in AN to episodic memory.

Introduction emerges from studies addressing executive functions and


cognitive control, which yielded mixed results. For exam-
Research aimed at investigating the nature and the etiol-
ple, in their systematic review of reactive inhibitory con-
ogy of eating disorders (ED) has been the target of an
trol in eating disorders, Bartholdy, Dalton, O’Daly,
increasing number of studies in recent years (e.g.,
Campbell, and Schmidt (2016) showed that many studies
Treasure, Claudino, & Zucker, 2010). Indeed, there is a
failed to observe impairment of reactive inhibition, as
great bulk of knowledge concerning behavioral manifes-
indexed by stop-signal reaction times, which are thought
tations involved in the psychopathology of anorexia ner-
to reflect the latency of the cognitive process that inhibits
vosa (AN) and bulimia nervosa (BN), with some studies
an initiated motor action whenever that action no longer
suggesting a link between AN and compulsive traits on
fulfills the task rules (Logan, Schachar, & Tannock, 1997).
the one hand (e.g., Serpell, Livingstone, Neiderman, &
They further argued that other inhibitory control com-
Lask, 2002) and BN and impulsive personality on the
ponents could have a stronger relationship with eating
other hand (e.g., Fischer, Smith, & Cyders, 2008). Yet,
disorders and their symptoms. In contrast, a meta-analy-
much more effort needs to be directed toward character-
sis on inhibitory control in bulimic-type eating disorders
izing the cognitive profile of patients with eating disor-
(Wu, Hartmann, Skunde, Herzog, & Friederich, 2013),
ders, as the cognitive counterparts of these mental
which aimed to address the variability in the results
disorders are not fully understood. For instance, evidence
observed so far on this issue, found a general impairment
is accumulating suggesting that AN patients exhibit an
of inhibitory control in both reactive inhibition tasks
alteration in the ability to control shifts of spatial atten-
(e.g., stop-signal task) and cognitive interference control
tion (Dalmaso et al., 2015, 2016; Watson, Werling,
tasks (e.g., Stroop task). A similar deficit has recently been
Zucker, & Platt, 2010). However, a less consistent picture
documented by Yano et al. (2016), who found

CONTACT Giovanni Galfano giovanni.galfano@unipd.it Department of Developmental and Social Psychology, University of Padova, Via Venezia, 8,
Padova I-35131, Italy
© 2017 Informa UK Limited, trading as Taylor & Francis Group
2 D. F. STRAMACCIA ET AL.

dysfunctional cognitive control in patients with eating situation where retrieving items from episodic memory
disorders (mainly diagnosed with AN), as measured by impairs later recall of related items. RIF represents the
a modified Simon task, despite preserved sustained enduring detrimental effect of retrieval practice on non-
attention. practiced associated memories and is generally interpreted
Neuroimaging techniques such as functional Magnetic as the by-product of inhibitory mechanisms that are
Resonance Imaging have also been used in order to recruited to reduce interference from associated task-irre-
provide additional evidence regarding the status of inhi- levant items, in order to promote retrieval of the task-
bitory control in eating disorders, as well as its neural relevant items (Anderson, 2003). Moreover, RIF seems to
underpinnings. For example, Skunde et al. (2016) found be an ubiquitous effect in episodic memory, as it has been
evidence of altered activation in the frontostriatal circuit measured with a broad variety of stimuli (e.g., Campbell,
during inhibitory performance in BN and suggested that Dufour, & Chen, 2015; Campbell & Thompson, 2012;
it could moderate the severity of the disease symptoms. Galfano et al., 2011; Tempel & Frings, 2014), and it has
Moreover, a few studies found altered prefrontal activity been found to be impaired in a variety of psychiatric and
in AN, related to cognitive control tasks (e.g., Lock, neuropsychological conditions other than eating disorders
Garrett, Beenhakker, & Reiss, 2011; Zastrow et al., (e.g., Storm & Levy, 2012). In the present study RIF was
2009). For instance, Collantoni et al. (2016) reported investigated by using the retrieval-practice paradigm
impaired response inhibition in a stop-signal task accom- (Anderson, Björk, & Björk, 1994). In the retrieval-practice
panied by aberrant functional connectivity in the right paradigm, participants first study a list of numerous word
inferior frontal gyrus, which is a critical brain region in pairs composed of a semantic category and an exemplar
inhibitory control (e.g., Stramaccia et al., 2015). belonging to that category (e.g., BIRDS–sparrow, TREES–
An important aspect of the studies reviewed so far is that beech, BIRDS–vulture). Subsequently, they perform
they highlighted how executive functions and inhibitory repeated practice on half the exemplars from half the
processing are important not only in the control of action, categories (e.g., BIRDS–sp____). After a short interval,
but also in the control of covert behavior, potentially during which distracting tasks are often administered to
involved in the pathogenesis of eating-disorder symptoms prevent covert rehearsal, participants’ memory for the
(e.g., impulses that drive compulsive eating or obsessive entire study list is tested (e.g., BIRDS–v_____, TREES–
thinking about food/food restriction). However, a limited b_____, BIRDS–s_____). Typically, this procedure results
variety of tasks (e.g., Simon task, Go/No-Go task) has been in two findings, which reflect the memory dynamics trig-
used to address the issue in eating disorders. It is worth gered by the task requests during the previous practice
noting that the need for further studies exploring measures phase: on the one hand, memory at test is enhanced for
of inhibition and impulsivity beyond traditional cognitive practiced (e.g., sparrow) over non-practiced (e.g., beech)
tests has been advocated by recent meta-analyses on neu- exemplars, an effect often called “facilitation”; on the other
ropsychological investigations addressing eating disorders hand, and more surprisingly, memory is impaired for non-
(e.g., Zakzanis, Campbell, & Polsinelli, 2010), which have practiced exemplars that belong to practiced categories
also highlighted the lack of studies on higher order func- (e.g., vulture), compared to non-practiced exemplars that
tions, especially in patients with BN. Here, we aimed to belong to non-practiced categories (e.g., beech). The latter
further this line of research by investigating control of finding is usually referred to as RIF effect.
interference over episodic memory, which may also be Clinical populations characterized by symptoms
important regarding the cognitive profile of patients suffer- associated with either impulsivity or compulsiveness
ing from eating disorders. In particular, recent work with (e.g, attention deficit hyperactivity disorder; obsessive-
healthy participants has pointed out the beneficial role that compulsive disorder, substance-related disorders) often
suppression over interfering or unwanted memories can show reduced levels of RIF, which, in turn, has been
play in achieving goal-oriented behavior, emotion regula- interpreted as evidence for a deficit in the mobilization
tion, and wellbeing (e.g., Nørby, 2015; Storm, 2011; Storm of inhibitory mechanisms in the context of episodic
& Angello, 2010). Therefore, the aim of the present study memory (e.g., Demeter, Keresztes, Harsányi, Csigó, &
was to investigate whether the specific ability to recruit Racsmány, 2014; Racsmány et al., 2008; Storm &
executive control mechanisms that are thought to suppress White, 2010; Stramaccia et al., 2017). Similar findings
interfering memories is altered in patients with a primary have been reported with other experimental tasks that
diagnosis of eating disorder. To this end, we measured for probe memory control, such as the think/no-think
the first time the amount of retrieval-induced forgetting paradigm (Depue, Burgess, Willcutt, Ruzic, & Banich,
(RIF) in a sample of patients suffering from eating disor- 2010; Sala et al., 2009). Because patients with eating
ders and compared it to the performance of a healthy disorders are characterized by impulsive and compul-
control group. The RIF effect describes the counterintuitive sive symptoms, with the former apparently being more
JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY 3

prominent in BN (e.g., Fischer et al., 2008) and the subtype, and 10 as restrictive subtype. Two AN patients
latter in AN (e.g., Serpell et al., 2002), patients with were reported to display obsessive compulsive disorder
eating disorders could exhibit alterations in exerting and borderline personality disorder symptoms, respec-
control over interfering memories. According to an tively. Four BN patients were reported to display
influential class of models available in the literature depressive symptoms. Sixteen patients (10 patients
(Anderson, 2003; Bäuml, Pastötter, & Hanslmayr, with AN, 6 patients with BN) were medicated. Most
2010), RIF and facilitation would be independent phe- common medications consisted of benzodiazepines
nomena, as only RIF would rely on executive proces- and/or serotonin-specific reuptake inhibitors antide-
sing and suppression mechanisms. This view is pressants. Medical treatment also included vitamins
supported by evidence suggesting that the two phe- and dietary supplements. The control group consisted
nomena rely on dissociable neural underpinnings of 8 males and 19 females (Mage = 27.22, SD = 7.63;
(e.g., Penolazzi, Stramaccia, Braga, Mondini, & mean years of education = 15.67, SD = 2.97; mean
Galfano, 2014; Wimber, Rutschmann, Greenlee, & BMI = 21.88, SD = 2.52). There was no significant
Bäuml, 2009). In this regard, it is worth noting that difference in either age, t(52) = –.57, p = .57, or years
the brain regions that seem to be chiefly involved in of education, t(52) = 1.90, p = .07, between the eating
RIF (mainly located in the prefrontal cortex, see disorders group and the healthy control group. All
Anderson, Davis, Fitzgerald, & Hoy, 2015; Penolazzi participants were native Italian speakers with no his-
et al., 2014; Wimber et al., 2009) are partially over- tory of neurological disease or learning disability. The
lapping with those showing a reduced activity in Ethics Committee for Psychological Research of the
patients with eating disorders performing cognitive University of Padua approved the study. All partici-
control tasks (e.g., Lock et al., 2011; Zastrow et al., pants signed an informed consent form prior to their
2009). Based on this reasoning, and in consideration participation, and another one at the end of the whole
of the possible link between eating disorders and dys- procedure.
functional executive processing (Wu et al., 2013), we
expected to observe a weaker RIF effect in the eating
disorders group as compared to the control group, Apparatus and procedures
signifying an impairment in memory control ability.
In contrast, we expected to observe similar levels of Participants sat in front of a 15 laptop monitor
facilitation across the two groups, reflecting an intact (1366 × 768 pixels, 60 Hz), where stimuli were presented
ability to strengthen items in episodic memory through in black against a gray background (Courier New bold
repeated retrieval practice. font, 30pt). All tasks were delivered using E-prime 2.0.

Retrieval-practice paradigm
Method We used an adapted version of the Retrieval-Practice
Paradigm (Anderson et al., 1994). All stimuli were selected
Participants
and adapted from the categorical production norms for the
A total of 54 participants took part in the study: 27 Italian language (Boccardi & Cappa, 1997). Ninety-six
malnourished outpatients with a primary diagnosis of category-exemplar word pairs belonging to 12 semantic
eating disorders (eating disorders group) in treatment categories were included, with 2 parallel subsets of 4 exem-
in a public service located in Northern Italy, and 27 plars for each category. Stimuli were selected according to
healthy volunteers recruited from the local community the following criteria: (a) semantic associations within and
and university (control group). All patients were diag- between categories were minimized; (b) exemplars had
nosed by a board-certified attending research team of medium to high taxonomic strength; (c); on average,
psychiatrists according to the DSM-5 criteria for eating exemplars had a very low lexical frequency, according to
disorders (American Psychiatric Association, 2013). At the itWac database (Baroni, Bernardini, Ferraresi, &
the time of testing, patients were not in remission. The Zanchetta, 2009); (d) categories and subsets were roughly
eating disorders group was composed of 2 males and balanced in terms of taxonomic strength and lexical fre-
25 females and included 15 AN patients (Mage = 29.53, quency of their respective exemplars; (e) exemplars within
SD = 10.97; mean years of education = 14.33, the same category never began with the same initial letter;
SD = 1.76; mean BMI = 17.3, SD = 2.06) and 12 BN (f) no words were longer than 11 or shorter than 5 letters.
patients (Mage= 27.42, SD = 8.72; mean years of educa- The stimuli, which were selected to address RIF in different
tion = 14.25, SD = 1.76; mean BMI = 22.51, SD = 3.94). clinical and non-clinical populations, can be found in the
Five of the AN patients were classified as binge-purge Appendix.
4 D. F. STRAMACCIA ET AL.

Study phase. The participants proceeded to study all the necessary condition for observing RIF in the subsequent
96 category-exemplar word pairs (e.g. “birds–sparrow”), test phase (see, e.g., Storm & Nestojko, 2010), nor it is
with the instruction to memorize each exemplar by think- known to modulate the effect (Erdman & Chan, 2013).
ing of how it could be related to its category (see Exemplars that received practice during this phase were
Figure 1). Study trials started with a 500-ms fixation labeled as RP+ items, while non-practiced exemplars
cross, followed by a category-exemplar word pair that belonging to practiced categories were labeled RP–.
stayed on screen for 4000 ms, followed by a 500-ms Exemplars from one of the subsets of each non-practiced
blank screen. Stimuli were presented in a randomized category were labeled NRP+, whereas exemplars from the
blocked order, with the constraint that 2 items belonging remaining subsets of non-practiced categories were labeled
to the same category were never shown one after the NRP–. The designation of practiced and control categories
other. Each block consisted of 12 items, and each item and exemplars that contributed to the measurement of
was randomly drawn from one of the 12 semantic cate- both RIF (NRP– items greater than RP– items) and facil-
gories. These precautions were used to discourage strate- itation (RP+ items greater than NRP+ items) effects was
gies known to promote integration, which in turn can roughly counterbalanced across all participants by using
reduce RIF (Anderson & McCulloch, 1999). predetermined lists (24 lists in total). Between the practice
phase and the final test phase of the retrieval-practice
Practice phase. Participants actively practiced one subset paradigm, participants performed the Sustained
(four exemplars) of half categories for three times, with 72 Attention to Response Task (SART, Robertson, Manly,
trials in total. Presentation order was similar to the pre- Andrade, Baddeley, & Yiend, 1997; see below), which
vious phase. On each trial, participants were first shown a was included as a control measure to address the presence
fixation cross for 500 ms, followed by the presentation of a of a more general impairment of attentional or reactivity
semantic category alone (e.g. “birds”) for 1500 ms to abilities, as opposed to a specific deficit in the ability to
promote activation of interfering exemplars (see Bajo, exert cognitive control over interference. Participants were
Gómez-Ariza, Fernandez, & Marful, 2006) and subsequent instructed to respond to each item of a rapid sequence of
need for memory control, followed by the same category digits, interleaved with masks, except for the digit “3”, for
and the first two letters of an exemplar (e.g. “birds–sp___”) which they were asked to withhold response. In total, 225
for 8000 ms (i.e., a category-plus-letter cued recall task). single digits from “1” to “9” were presented for 250 ms, 25
During that time, participants were instructed to type in times each, interleaved with a mask (“#”) lasting 900 ms.
full the name of the associated exemplar that they had Digits were presented at a varying font size (48, 72, 94, 100,
previously studied that matched both the category and or 120 point, Symbol font), in order to discourage partici-
the stem provided. No feedback was provided to partici- pants from using perceptual strategies. Stimuli were pre-
pants as to whether or not they had typed the correct sented centrally, in black against a grey background.
response, because retrieval success at this stage is not a Participants were instructed to respond as quickly and

Figure 1. Schematic illustration of the experimental procedure, with tasks ordered chronologically from left to right. Participants
studied all the experimental material from the retrieval-practice paradigm (RPP) first, and after that they immediately engaged in
repeated practice on a subset of the material (see Method section). Subsequently, participants performed the SART and filled the
BIS-11 questionnaire. Finally, participants performed the test phase of the retrieval-practice paradigm, where they were tested on all
the stimuli from the study phase.
JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY 5

accurately as possible with a key press of the spacebar, and Data analyses
to withhold response upon presentation of the digit “3”. As
As regards the retrieval-practice paradigm, for the sake of
the main purpose of the SART is to elicit slips of attention,
completeness, we started by analyzing the data collected
the task works at a very quick and repetitive pace but also
during the practice phase. More important to the purpose
incorporates highly infrequent trials that require a different
of the current study, we also analyzed data from the test
response. After completing the SART, participants also
phase to obtain an individual measure of facilitation and
filled a questionnaire aimed at measuring impulsivity
RIF effects. For each participant, we computed the propor-
(i.e., the tendency to act prematurely, without sufficient
tion of correct recall for each item type (i.e., RP+, NRP+,
evidence or concern about the consequences, especially
RP–, NRP–). Comparisons were then performed to deter-
when a strong desire/urge/habit co-occurs). Although
mine whether practice had beneficial (i.e., facilitation: RP+
impulsivity and inhibitory control should not be used as
greater than NRP+) and/or detrimental (i.e., RIF: NRP–
synonyms, the two constructs are somehow related given
greater than RP–) effects on recall performance in the test
that impaired inhibitory control can result in an increased
phase. We first performed two mixed-design ANOVAs on
impulsive behavior (Bartholdy et al., 2016). Hence, an
facilitation and RIF effects, with group (eating disorder,
inverse association between self-report impulsiveness and
control) as a between-participant factor and item type (i.e.,
inhibitory abilities as indexed by RIF could be expected. To
RP+, NRP+ for facilitation, NRP–, RP– for RIF) as a
this end, the Italian version of the Barratt Impulsiveness
within-participant factor. Subsequently, we explored
Scale-11 (BIS-11; Fossati, Di Ceglie, Acquarini, & Barratt,
whether patients diagnosed with AN and those diagnosed
2001), the semantic content of which is unrelated to the
with BN displayed similar patterns of cognitive perfor-
material used in the retrieval-practice paradigm, was admi-
mance. Because visual inspection of the data suggested
nistered. The questionnaire consists of 30 items rated on a
different patterns in the two types of patients, we per-
4-point Likert scale, pertaining to three dimensions: Motor
formed the same analyses on facilitation and RIF effects,
Impulsiveness (tendency to act on impulse without fore-
with the group factor now consisting of three levels (i.e.,
thought), Nonplanning Impulsiveness (lack of future plan-
AN, BN, control). Because the latter analyses yielded the
ning), and Attentional Impulsiveness (difficulty in
most informative results, all the subsequent analyses were
maintaining attention).
performed with group as a three-levels factor.
For the SART, we conducted three one-way
Test phase. After the practice phase, participants took ANOVAs with group as factor, each dealing with a
part in the test phase of the retrieval-practice paradigm different dependent measure (mean RTs for correct
(see Figure 1), and they were tested on all the stimuli responses only, percentage of total errors, and percen-
presented in the study phase (96 trials). Each trial started tage of commission errors). A similar approach was
with a 500-ms fixation cross, followed by the stimulus used to analyze data from the BIS-11 measures of
onset for 8000 ms, with a similar presentation format self-reported impulsivity (total score, and Motor
and response modality as in the practice phase, with the Impulsiveness, Nonplanning Impulsiveness, and
exception that participants were shown the category along Attentional Impulsiveness subscales). Finally, we com-
with the first letter only of the to-be-recalled exemplar (e.g. puted Pearson’s correlations to detect potential associa-
“birds–s____”). Participants were instructed to type the tions between RIF, facilitation, the indexes of efficient
corresponding exemplar in full. Presentation order was sustained attention obtained by the administration of
handled as in the previous phases, with the additional the SART, and the self-reported impulsivity scores as
constraint that all RP– and NRP– items were shown before measured by BIS-11 (total score, Motor Impulsiveness,
the RP+ and NRP+ items. It is important to note that this Nonplanning Impulsiveness, and Attentional
presentation order in our paradigm was aimed at isolating Impulsiveness scores).
the contribution of inhibitory mechanisms to forgetting of
competitors, as opposed to other factors, that may have
affected recall performance for these items, such as asso- Results
ciative blocking and output interference (see Anderson,
2003; Anderson et al., 1994) – i.e., the natural tendency to Retrieval-practice paradigm: collapsed ED patient
recall practiced items first – that results in hampering recall group analyses
of associated items (see Roediger, 1978). Not controlling A t test with group as factor was conducted on the
for these confounds produces an inflated estimation of proportion of correct recall during the practice phase,
RIF, which has nothing to do with executive control and which yielded a significant effect, t(52) = −2.53, p < .01,
inhibitory processing. revealing a better recall for patients (M = 79.61,
6 D. F. STRAMACCIA ET AL.

95% CI [74.08, 85.14]) than for controls (M = 69.75, suggesting an intact ability to suppress interfering mem-
95% CI [64.22, 75.28]). ories in the eating disorders group, and was at odds with
Turning to the test phase, which is more relevant for our predictions, as well as with previous evidence hinting
the purpose of the present study, for the facilitation at an altered ability to control interference in eating dis-
effect, the mixed ANOVA revealed a significant main orders (e.g., Wu et al., 2013).
effect of item type, F(1, 52) = 274.53, p < .01, η2p = .84.
This reflected a better recall of RP+ items (M = 67.75,
95% CI [64.48, 71.01]) than NRP+ items (M = 38.04,
Retrieval-practice paradigm: split AN and BN
95%CI [34.44, 41.64]), in line with a facilitation effect.
patient groups analyses
The main effect of group, F(1, 52) = 13.49, p < .01,
η2p = .21, was also significant, with patients (M = 58.26, In order to ascertain whether the two categories of
95% CI [54.11, 62.4]) displaying an overall better per- patients included in the eating disorder group displayed
formance than controls (M = 47.53, 95% CI [43.39, the same pattern for both RIF and facilitation, we per-
51.67]), in line with recent evidence of elevated perfor- formed the same analysis on the three groups (control,
mance-based perfectionism in patients with eating dis- BN, AN), which yielded quite different results.
orders (Lloyd, Yiend, Schmidt, & Tchanturia, 2014). For the sake of completeness, a one-way ANOVA
The Group × Item Type interaction was not significant, with group as factor was conducted on the proportion
F(2, 52) = .82, p = .37. Therefore, all groups benefited of correct recall during the practice phase. Group
from retrieval practice to a similar extent. yielded a significant effect, F(2, 51) = 4.02, p = .02,
Concerning the RIF effect, a mixed ANOVA revealed a η2p = .14, revealing a better recall for both AN patients
significant main effect of item type, F(1, 52) = 14.76, (M = 82.69, 95% CI [75.30, 90.07]) and BN patients
p < .01, 2p = .22, indicating better recall of NRP– items (M = 75.76, 95% CI [67.51, 84.02]) than for controls
(M = 48.26, 95% CI [44.64, 51.81]) than of RP– items (M = 69.75, 95% CI [64.25, 75.26]).
(M = 40.51, 95% CI [36.79, 44.22)], consistent with a As for the test phase, the scenario observed for the
standard RIF effect (Murayama, Miyatsu, Buchli, & facilitation effect was consistent with that emerged in the
Storm, 2014). Again, group yielded a significant main previous analysis, as a mixed ANOVA showed a main
effect, F(1, 52) = 6.72, p = .02, η2p = .11, suggesting an effect of item type, F(1, 51) = 252.21, p < .01, η2p = .83, a
overall better memory performance in the patient group significant main effect of group, F(2, 51) = 6.69, p < .01,
(M = 48.30, 95% CI [44.00, 52.61]) as compared to healthy η2p = .21 (control, M = 47.53, 95% CI [43.35, 51.71]; BN,
controls (M = 40.43, 95% CI [36.13, 44.74]). Most impor- M = 57.47, 95% CI [51.19/63.74; AN, M = 58.89,
tantly for the purpose of the study, the Group × Item Type 95% CI [53.28, 64.50]), and no Group × Item Type inter-
interaction was not significant, F(1, 52) = .02, p = .88, action, F(2, 51) = .57, p = .57 (see Figure 2), confirming

Figure 2. Recall performance from the final test phase for items relevant to the facilitation effect (RP+ recall greater than NRP+
recall) in the three groups. The facilitation effect was significant in all groups. Bars represent 95% CIs.
JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY 7

Figure 3. Recall performance from the final test phase for items relevant to the Retrieval-Induced Forgetting (RIF) effect (NRP– recall
greater than RP– recall) in the three groups. RIF was significant in the control and BN groups only. Bars represent 95% CIs.

that the three groups displayed a robust and very similar impairment, which cannot be accounted for by a general-
facilitation effect. ized memory problem in AN patients, as testified by a
In sharp contrast, a mixed ANOVA for the RIF reliable facilitation effect with the same magnitude as
effect not only confirmed a significant effect of item that displayed by healthy controls (see Figure 3), and
type, F(1, 51) = 20.70, p < .001, η2p = .29, as well as a by their performance during the practice phase.
significant main effect of group, F(2, 51) = 7.40,
p < .01, η2p = .23 (control, M = 40.43,
Sustained attention to response task (SART)
95% CI [36.36, 44.50]; BN, M = 42.19,
95% CI [36.08, 48.29]; AN, M = 53.19, The series of one-way ANOVAs performed on SART
95% CI [47.73, 58.66]), but, crucially, also a signifi- measures with group as factor did not reveal any significant
cant Group × Item Type interaction, F(2, 51) = 7.80, effect (mean RTs for correct responses: F(2, 51) = 1.29,
p < .01, η2p = .23 (see Figure 3). Two-tailed t tests p = .28; percentage of total errors: F(2, 51) = .13, p = .88;
comparing memory performance on NRP– and RP– percentage of commission errors: F(2, 51) = 1.53, p = .23).
items showed that RIF was present in healthy con- Therefore, the three groups exhibited a similar ability to
trols, t(26) = 2.85, p < .01, in BN patients, t maintain attention (see Table 1).
(11) = 4.64, p < .01, but not in AN patients, t
(14) = –.29, p = .77. In addition, RIF was signifi-
Barratt impulsiveness scale (BIS-11)
cantly more pronounced in BN patients as compared
to healthy controls, t(37) = 2.46, p = .02. Because The series of one-way ANOVAs performed on the BIS-11
gender was not balanced among our groups, we con- questionnaire measures with group as factor failed to show
ducted further statistical analyses after removing significant effects (total BIS-11 score: F(2, 51) = .23, p = .80;
male participants from our samples. The overall pat- Motor Impulsiveness score: F(2, 51) = .12, p = .88;
tern of results was fully confirmed, in that the critical Nonplanning Impulsiveness score: F(2, 51) = .66, p = .52;
Group × Item Type interaction was significant when Attentional Impulsiveness score: F(2, 51) = 1.61, p = .21).
addressing RIF, F(2, 41) = 4.61, p = .016, η2p = .18, This suggests that the three groups did not differ in terms
but not when addressing facilitation F(2, 41) = .53, of impulsiveness (see Table 1).
p = .60, η2p = .03.
Overall, these analyses suggest that AN patients have
Correlation analyses
an impaired ability to overcome interference in memory,
as shown by the lack of RIF in this group. Importantly, Pearson’s correlation analyses (see Table 2) conducted on
this pattern highlights a selective memory control the retrieval-practice paradigm measures, SART
8 D. F. STRAMACCIA ET AL.

Table 1. Demographic and clinical characteristics of the anorexia nervosa, bulimia nervosa, and control groups, and related
descriptive statistics concerning SART and BIS-11 measures.
AN group BN group Control group
(N = 15) (N = 12) (N = 27)
M SD M SD M SD
Age (years) 29.5 11.1 27.4 8.7 27.2 7.6
Gender (male count) 2 8
Education (years) 14.3 1.8 14.3 1.8 15.7 3.1
Onset of disorder (years) 17.7 4.1 15.7 4.1
Duration of disorder (years) 11.9 10.1 11.8 8.2
SART CEs (%) 40.3 30.6 38.0 26.2 51.6 23.2
SART RTs (ms) 369.1 88.9 382.9 120.0 338.1 68.9
BIS-11 Attentional 17.6 3.6 16.9 2.1 16.1 2.8
BIS-11 Motor 19.3 4.5 18.7 2.8 19.1 3.1
BIS-11 Nonplanning 24.2 3.8 22.8 4.2 24.1 3.4
BIS-11 Total 60.5 10.2 58.4 6.2 59.1 7.7
Note. AN = anorexia nervosa; BN = bulimia nervosa; SART = Sustained Attention to Response Task; CEs = commission errors; RTs = reaction times; BIS-11 = Barratt
Impulsiveness Scale.

Table 2. Pearsons’s correlations between RIF, facilitation, SART measures, and BIS-11 scores.
SART BIS-11
RIF FAC CEs RTs Att. Mot. Non. Tot.
RIF —
FAC .019 —
SART CEs −.239 .094 —
SART RTs .232 0 −.714* —
BIS-11 Attentional .015 −.078 −.006 .063 —
BIS-11 Motor −.044 −.226 −.111 .007 .377* —
BIS-11 Nonplanning −.193 −.102 −.107 .106 .354* .48* —
BIS-11 Total −.078 −.18 −.085 .086 .695* .808* .787* —
Note. RIF = Retrieval-Induced Forgetting; FAC = Facilitation; SART = Sustained Attention to Response Task (CEs = Commission
Errors; RTs = Reaction Times); BIS = Barratt Impulsiveness Scale (Att. = Attentional; Mot. = Motor; Non. = Nonplanning;
Tot. = Total). N = 54. *p < .05. The theoretically relevant correlations are those involving RIF and facilitation (FAC), and none of
them was statistically significant.

commission errors and mean RTs for correct responses, To this end, we used the retrieval-practice para-
and BIS-11 scores across all participants showed a clear digm, a behavioral procedure that is known to elicit
lack of association between RIF and facilitation (p = .89), two phenomena thought to reflect both the benefi-
in line with the view that the two latter phenomena reflect cial and the detrimental effects of memory retrieval
independent processes. In addition, neither RIF nor facil- practice on the subsequent recall (Anderson et al.,
itation displayed significant correlations with the different 1994). The former phenomenon, known as the facil-
SART measures and BIS-11 scores (lowest p = .08, uncor- itation effect, reflects the well-established advantage
rected for multiple comparisons). Therefore, individual of trained over untrained material due to active
difference in sustained attention and impulsiveness, as practice. The latter phenomenon, known as RIF, is
measured by SART and BIS-11, respectively, do not thought to probe an adaptive aspect of forgetting,
appear to be reliable predictors of the strength of inhibi- which, according to a prominent class of models, is
tory control in the episodic memory domain. No signifi- achieved through the implicit recruitment of inhi-
cant correlations were observed between SART and BIS- bitory processing aimed at decreasing interference
11 measures (lowest p = .53). from competing memories (Anderson, 2003; Bäuml
et al., 2010). The choice of this paradigm was moti-
vated by the fact that, even though evidence of
Discussion
impaired cognitive control over interference has
The present study was aimed at enriching the been reported in eating disorders, this pattern has
knowledge concerning the cognitive profile of been observed almost exclusively by means of tasks
patients with eating disorders. Specifically, our addressing selective attention (e.g., Yano et al.,
goal was to address cognitive control in a group of 2016; see Wu et al., 2013; for a review). Therefore,
patients with either AN or BN, by focusing on the the present research represents the first attempt to
previously unexplored domain of episodic memory. investigate the cognitive profile of patients with
JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY 9

eating disorders in the specific domain of resistance who otherwise performed as well as healthy indivi-
to interference in episodic memory. duals in both control measures of attention and
The procedure also included the SART as a control task reactivity as revealed by SART, and in the ability to
to rule out general reactivity deficits (Robertson et al., benefit from memory practice as revealed by the
1997), and the BIS-11 questionnaire (Fossati et al., 2001) facilitation effect. The specificity of this impairment
to explore potential correlations between self-reported in inhibition and memory control processes is in line
dimensions of impulsivity and cognitive control in with recent findings of dissociable cognitive control
memory. and sustained attention (Yano et al., 2016) and is
We expected patients with eating disorders to further supported by the version of the retrieval-
exhibit a weaker RIF as compared to a group of practice paradigm used here, which was designed to
healthy controls based on two lines of evidence: (a) control for the main confounds that may affect RIF
hampered cognitive control in eating disorders (Wu (e.g. Anderson, 2003; Storm & Levy, 2012), such as
et al., 2013; Yano et al., 2016); and (b) similar pre- associative blocking and output interference.
frontal brain regions associated with abnormal activ- Interestingly, Demeter and colleagues (2014) found a
ity in patients with eating disorders performing similar pattern of results (impaired RIF in the face of
cognitive control tasks (e.g., Collantoni et al., 2016) intact facilitation) in patients suffering from obsessive
and RIF in healthy participants (e.g., Wimber et al., compulsive disorder, which are thought to have many
2009). In addition, we expected a similar perfor- important similarities with patients diagnosed with AN
mance across groups in both the beneficial effects (Pollack & Forbush, 2013; Serpell et al., 2002). Because
of memory practice (i.e., facilitation effect; see the psychopathological features shared by AN and obses-
Demeter et al., 2014 for a similar dissociation in sive-compulsive personality disorder are not fully under-
patients with obsessive-compulsive disorder) and stood (Altman & Shankman, 2009; Boisseau, Thompson-
general reactivity (i.e., SART measures; e.g., Yano Brenner, Pratt, Farchione, & Barlow, 2013), our results
et al., 2016). suggest that the retrieval-practice paradigm may be used
The results were partially in line with our pre- as a benchmark to further investigate differences and
dictions. Indeed, both facilitation and sustained similarities between these psychiatric disorders, which
attention as measured by SART were preserved in could, in turn, provide useful information to orient both
patients with eating disorders, as expected. their diagnosis and treatment.
However, a similar pattern emerged also for RIF. Turning to BN patients, the results were unex-
Subsequently, based on an explorative inspection of pected, in that we hypothesized a decreased RIF
the data that suggested a different performance in effect irrespective of the specific type of eating dis-
the retrieval-practice paradigm depending on the order diagnosis. The obtained pattern of findings
specific eating disorder type, we re-analyzed the suggests that the ability to suppress interfering
data with group as a three-level factor (i.e., AN, memories was fully preserved in patients with BN.
BN, control). These analyses confirmed that the Indeed, RIF in the BN group persisted even when
groups had comparable levels of performance in participants showing a RIF that exceeded 2 SD from
both SART and facilitation measures. In sharp con- sample average were removed from the analyses. A
trast, critical for the purpose of the study, the new tentative interpretation to account for the observed
analyses revealed a difference in memory control, as findings might be related to the observation that
indexed by RIF, as a function of group. Specifically, RIF is known to be associated to working memory
patients with AN did not display any evidence of functioning (e.g., Aslan & Bäuml, 2011; Storm &
RIF, whereas patients with BN exhibited a signifi- Bui, 2016), in that individuals with higher working
cant RIF effect whose magnitude was larger than memory performance have a larger RIF effect. In
that of healthy controls. this regard, Zakzanis et al. (2010) reported intact
The results observed in patients with AN are in working memory in patients suffering from BN, but
line with our predictions, and they extend our not in those affected by AN. Indeed, in their meta-
knowledge about the status of cognitive control to analysis, Zakzanis et al. (2010) showed that patients
the domain of episodic memory in this clinical popu- with AN display impairments on a broad range of
lation, which was previously unexplored, pointing to cognitive measures related to working memory,
a very specific deficit. Indeed, in our study we used whereas little to no evidence exists for similar def-
RIF as a probe to investigate cognitive control over icits in patients with BN. In addition, a recent study
interference in memory. Crucially, RIF appeared to by Weider, Indredavik, Lydersen, and Hestad (2015)
be selectively impaired in patients affected by AN, also supports a possible dissociation among AN and
10 D. F. STRAMACCIA ET AL.

BN patients, with AN patients exhibiting a lower subtype or the binge-purge subtype. Because past
performance in tests assessing executive functions work has provided mixed evidence concerning dif-
such as the Trail Making Test and the Wisconsin ferent behavioral performance between the two sub-
Card Sorting Test. It is important to note that the types in several cognitive tasks (see, Dalmaso et al.,
significant differences in RIF that emerged between 2016; Rosval et al., 2006; Yano et al., 2016), we have
BN and control groups do not necessarily indicate no specific reason to hypothesize that a dissociation
that the former group has a better inhibitory ability should emerge in the retrieval-practice paradigm.
(possibly related to working memory functioning) However, this is an open empirical question that
with respect to the latter group. Inhibitory proces- needs to be addressed in future studies.
sing in the retrieval practice paradigm is called into Another relevant limitation is the presence of medi-
play to reduce interference generated by RP– items. cated patients in the clinical sample, within both the
As a result, the specific performance in the recall of AN and BN groups, which might have influenced the
RP– items could specifically be considered as results. While we cannot entirely exclude medication
reflecting the inhibitory abilities. As shown in effects on our measures of interest, additional control
Figure 3, the significant difference between BN analyses, summarized below, compared medicated with
and Controls as regards RIF is mostly driven by nonmedicated patients in RIF magnitude, facilitation
differences in the recall of NRP– items (better magnitude, and the three SART measures in the groups
recalled by the BN patients than by healthy con- of patients with AN and BN. In a series of independent
trols) rather than RP– items (whose recall is com- samples, two-tailed t tests failed to show any differ-
parable in the two groups). Importantly, this ences in the above measures due to medication in
argument does not hold true when considering the either AN or BN patients (lowest p = .11). Even though
performance of AN patients. Indeed, as shown in these control analyses may suggest that medication did
Figure 3, their lack of RIF suggests a lack of inhibi- not play a critical role in the present findings, we
tion of the RP– items (recall of which was as good acknowledge that this may also be due to the small
as for NRP– items). Clearly, the present pattern of sample size investigated here. Therefore, further studies
results calls for further studies in order to confirm with larger patient cohorts are needed to clarify the
these findings and possibly collect measures of RIF, relationship between medication and performance in
working memory, and broader executive function- tasks addressing cognitive control over memory retrie-
ing in the same samples of patients with eating val. In addition to medication, depression could also
disorders. have influenced the results, specifically by reducing the
As for the BIS-11 measures, the data showed no hint magnitude of RIF (e.g., Groome & Sterkaj, 2010), due
of differences as a function of group. This question- to the presence of comorbidity in four of the BN
naire was administered to test for a potential correla- patients tested here. However, because the BN sub-
tion between self-report measures of impulsivity and group displayed an intact RIF, we can safely assume
RIF. Recently, Stramaccia et al. (2017) have reported that the presence of depressive symptoms played only a
differences between healthy control and groups of limited role – if any – in shaping the results.
patients with substance-related disorders in both RIF A final limitation is related to the use of a wide
and BIS-11 scores (with patients exhibiting no RIF and range of categories as stimuli, some of which were
higher impulsivity scores). Importantly, however, in not entirely “neutral” in terms of affective valence
that study no significant correlations were observed with reference to the specific disorder of the clinical
between these BIS-11 measures and RIF. This pattern, participants (i.e., food-related categories). In addi-
when considered together with the lack of significant tion, food-related categories were probably heteroge-
correlations observed also in the present study, sug- neous in the way they could be appraised by patients,
gests that BIS-11 measures may actually describe dif- in that they could be perceived either as functional to
ferent aspects of cognitive control with respect to those reduce weight (vegetables) or as largely dysfunctional
measured in the retrieval-practice paradigm. in this regard (desserts). These two factors prevent a
Although we made every effort to control for more in-depth examination of the possible differ-
major confounds in this study, a few important lim- ences in RIF triggered by the different categories.
itations remain that need to be addressed. First, due However, exploratory analyses limited to food-unre-
to the small sample size, we were not able to distin- lated categories basically replicated the results
guish performance as a function of whether patients obtained for the whole dataset, thus suggesting that
affected by AN were diagnosed with the restrictive RIF was not influenced by the potential affective
JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY 11

valence of some stimulus categories for the clinical ORCID


participants.1 Davide Francesco Stramaccia http://orcid.org/0000-0002-
In conclusion, the present study suggests a selective 9744-0445
impairment of the ability to inhibit interference from Barbara Penolazzi http://orcid.org/0000-0001-8717-6233
competing information in episodic memory in patients Luigi Castelli http://orcid.org/0000-0002-1472-4507
suffering from AN, whereas this ability was apparently Giovanni Galfano http://orcid.org/0000-0001-5327-4062
preserved in patients with BN. No general deficit in
sustained attention or motor reactivity, nor substantial
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1
Given that some of the categories used in our study (see Appendix) involved food and hence were not “neutral” to the
patients examined in our study, we conducted exploratory analyses limited to food-unrelated stimulus material, aimed at
testing the extent to which the overall pattern of results for RIF was influenced by these potentially salient categories. In
so doing, we were forced to restructure the data file in that we had to remove specific portions of the dataset. This data
processing stage, and all the subsequent exploratory analyses, were performed using the R software (R Core Team, 2016).
Next, we fitted logistic mixed models using the glmer procedure in the lme4 package (Bates, Mächler, Bolker, & Walker,
2015). For both the whole and the food-unrelated datasets, we fitted two main models: the “MAIN” model, with item
type and group as fixed effects, and the “INTER” model, with the same fixed effects as the previous model, with the
addition of the interaction term between group and item type. In both models, participant and category were also
entered as random interaction terms. We then compared the two models, in both datasets, using the Akaike’s
information criterion (AIC; Akaike, 1973). Specifically, the model that displayed the lowest AIC value was considered
the one that best fitted the available data. The results from these analyses confirm that the model that included the
predicted interaction best fits the available data in both analyses (whole dataset: AICMAIN = 3395.2, AICINTER = 3387.1, χ2 =
12.09, p = .002; food-unrelated dataset: AICMAIN = 1992.2, AICINTER = 1987.1, χ2 = 9.17, p = .01), suggesting that the
presence of food-related categories in the whole data set did not affect the overall pattern.
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14 D. F. STRAMACCIA ET AL.

Appendix
Stimuli used in the Retrieval-Practice Paradigm

Set A Set B
Exemplar Eng. Translation LFREQ TSTR Exemplar Eng. Translation LFREQ TSTR
ALBERI (TREES)
quercia oak 7.7 2.0 cipresso cypress 1.4 11.0
faggio beech 1.6 8.0 salice willow 1.6 11.0
pioppo poplar 1.3 7.0 abete spruce 3.0 3.0
larice larch 0.6 13.0 betulla birch 0.9 6.0
M 2.8 7.5 M 1.7 7.8
SD 3.3 4.5 SD 0.9 3.9
ALCOLICI (ALCOHOLIC DRINKS)
grappa grappa 4.7 3.0 cognac cognac 0.9 8.0
marsala marsala 3.5 17.0 amaretto amaretto 0.3 23.0
spumante sparkling wine 2.3 10.0 tequila tequila 0.5 11.0
brandy brandy 1.0 9.0 vodka vodka 1.4 4.0
M 2.9 9.8 M 0.8 11.5
SD 1.6 5.7 SD 0.5 8.2
AUTOMOBILE (CAR PARTS)
cofano hood 1.5 8.0 batteria battery 19.4 21.0
motore engine 72.6 3.0 pistone piston 3.2 15.0
freno brake 10.8 7.0 sedile seat 5.7 2.0
lunotto rear window 0.4 24.0 ruota wheel 27.8 3.0
M 21.3 10.5 M 14.0 10.3
SD 34.5 9.3 SD 11.6 9.3
DESSERT (DESSERTS)
tartufo sweet truffle 4.6 24.0 meringa meringue 0.2 22.0
panettone panettone 1.6 20.0 crostata pie 0.8 5.0
sorbetto sorbet 0.6 12.0 budino pudding 0.7 4.0
gelato ice cream 8.4 1.0 frittella pancake 0.9 31.0
M 3.8 14.3 M 0.7 15.5
SD 3.5 10.1 SD 0.3 13.2
FIORI (FLOWERS)
giglio lily 4.7 6.0 orchidea orchid 1.5 4.0
tulipano tulip 1.1 3.0 papavero poppy 0.6 12.0
azalea azalea 0.3 22.0 ciclamino cyclamen 0.4 11.0
narciso narcissus 1.5 20.0 mimosa mimosa 0.8 23.0
M 1.9 12.8 M 0.8 12.5
SD 1.9 9.6 SD 0.5 7.9
FRUTTA (FRUITS)
mango mango 1.2 13.0 arancia orange 6.0 4.0
pesca peach 50.3 7.0 limone lemon 10.1 18.0
banana banana 5.5 3.0 fragola strawberry 3.8 10.0
dattero date 1.2 28.0 ciliegia cherry 3.1 11.0
M 14.6 12.8 M 5.8 10.8
SD 23.9 11.0 SD 3.2 5.7
INSETTI (INSECTS)
pulce flea 2.2 18.0 libellula dragonfly 0.4 14.0
mosca fly 19.2 1.0 formica ant 3.1 4.0
termite termite 0.3 19.0 grillo cricket 9.7 16.0
vespa wasp 6.1 6.0 cimice bedbug 0.4 10.0
M 2.8 7.5 M 1.7 7.8
SD 3.3 4.5 SD 0.9 3.9
METALLI (METALS)
magnesio magnesium 1.6 15.0 alluminio aluminum 7.6 6.0
piombo lead 12.5 7.0 litio lithium 0.9 19.0
zinco zinc 1.7 5.0 stagno tin 5.9 12.0
cromo chrome 1.1 19.0 nichel nickel 0.8 10.0
M 2.8 7.5 M 1.7 7.8
SD 3.3 4.5 SD 0.9 3.9
PESCI (FISHES)
branzino bass 1.0 19.0 carpa carp 1.4 13.0
sogliola sole 0.6 8.0 luccio pike 1.0 14.0
trota trout 2.5 1.0 merluzzo cod 0.9 10.0
orata sea bream 0.6 17.0 anguilla eel 1.7 7.0
M 2.8 7.5 M 1.7 7.8
SD 3.3 4.5 SD 0.9 3.9
SPORT (SPORTS)
atletica athletics 25.1 8.0 ippica horse racing 0.6 17.0
pattinaggio skating 1.8 18.0 ciclismo cycling 11.0 14.0
rugby rugby 2.5 12.0 nuoto swimming 7.5 4.0
(Continued )
JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY 15

(Continued).
Set A Set B
Exemplar Eng. Translation LFREQ TSTR Exemplar Eng. Translation LFREQ TSTR
tennis tennis 8.3 3.0 basket basketball 8.4 6.0
M 2.8 7.5 M 1.7 7.8
SD 3.3 4.5 SD 0.9 3.9
UCCELLI (BIRDS)
merlo blackbird 3.0 8.0 corvo crow 4.4 7.0
rondine swallow 2.2 6.0 gabbiano seagull 4.3 12.0
struzzo ostrich 1.6 22.0 falco hawk 6.4 4.0
passero sparrow 1.0 3.0 avvoltoio vulture 1.2 20.0
M 2.8 7.5 M 1.7 7.8
SD 3.3 4.5 SD 0.9 3.9
VERDURA (VEGETABLES)
lattuga lettuce 1.0 18.0 sedano celery 2.7 7.0
finocchio fennel 2.0 5.0 zucchina zucchini 2.0 6.0
carota carrot 4.8 2.0 peperone pepper 3.2 13.0
melanzana aubergine 2.8 9.0 verza cabbage 0.7 12.0
M 2.8 7.5 M 1.7 7.8
SD 3.3 4.5 SD 0.9 3.9
Note. Stimuli used in the experiment, divided by semantic category (listed in alphabetical order) and counterbalance set (A /B), with English translations and
related lexical frequency (LFREQ) and taxonomic strength (TSTR) as measured in the Italian language. The English translations provided here are not
suitable for use in the retrieval-practice paradigm as stimuli are balanced with respect to the Italian language (see the Method section for details).

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