Brain and Cognition 92 (2014) 118–122

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Handedness differences observed in episodic memory retrieval do not extend to the domain of prospective memory Aparna Sahu, Stephen D. Christman ⇑ University of Toledo, United States

a r t i c l e

i n f o

Article history: Accepted 24 October 2014 Available online 14 November 2014 Keywords: Handedness Individual differences Prospective memory Intentions Episodic memory

a b s t r a c t A robust inconsistent handed advantage exists for episodic retrospective memory processes. The current study was undertaken to test whether this handedness difference extends to the domain of prospective memory (PM). Two studies, one based on a self-report measure (the Prospective and Retrospective Memory Questionnaire) and the second involving a performance-based test (Memory for Intentions Screening Test), were carried out. Handedness effects were absent for both measures of PM. The absence of a handedness effect strongly suggests that PM processes are primarily characterized by executing intentions that depend on semantic networks for retrieval and do not necessarily rely on recalling spatio-temporal context, as is the case with episodic retrospective memory. Ó 2014 Published by Elsevier Inc.

1. Introduction A large body of evidence shows a robust advantage in episodic memory retrieval for mixed/inconsistent-handers, relative to strong/consistent handers. For example, inconsistent-handedness is associated with superior recall of lab-based and real world-based memories (Chu, Abeare, & Bondy, 2012; Lyle, Hanaver-Torrez, Hackländer, & Edlin, 2012; Parker & Dagnall, 2010; Propper, Christman, & Phaneuf, 2005), superior source memory (Christman, Propper, & Dion, 2004; Lyle & Jacobs, 2010; Lyle, Logan, & Roediger, 2008; Lyle, McCabe, & Roediger, 2008), an increased tendency for recognition to be accompanied by recollection (as indexed by ‘‘Remember’’ judgments) vs. familiarity (as indexed by ‘‘Know’’ judgments) (Propper & Christman, 2004), an earlier offset of childhood amnesia (Christman, Propper, & Brown, 2006), superior incidental learning under conditions of deep, but not shallow, levels of processing (Alipour, Aerab-Sheybani, & Akhondy, 2012; Christman & Butler, 2011), superior memory for faces (Lyle & Orsborn, 2011), and superior memory for hand usage (Edlin, Carris, & Lyle, 2013). These results have been interpreted in terms of the conjunction of two other findings. First, according to the hemispheric encoding and retrieval asymmetry model (HERA model; Babiloni et al., 2006; Tulving, Kapur, Craik, Moscovitch, & Houle, 1994), left vs. right frontal areas are primarily involved in the encoding vs. retrieval ⇑ Corresponding author at: Department of Psychology, University of Toledo, Toledo, OH 43606, United States. E-mail address: [email protected] (S.D. Christman). http://dx.doi.org/10.1016/j.bandc.2014.10.010 0278-2626/Ó 2014 Published by Elsevier Inc.

of episodic memories, thus implicating the role of the corpus callosum in the transfer of episodic memory information between hemispheres. Second, the corpus callosum is larger in inconsistent-handers, relative to consistent-handers (Luders et al., 2010; Witelson & Goldsmith, 1991). Thus, the superior performance of inconsistent-handers in episodic retrieval presumably reflects the greater interaction and transfer of information between the two hemispheres in inconsistent-handers. Handedness differences in memory are obtained in retrospective memory paradigms, in which participants attempt to recall past events. A related form of episodic memory, called prospective memory, refers to the ability to remember ‘‘to perform previously planned actions at the right time, or within the right time interval or after a certain event takes place while being involved in other activities’’ (Groot, Wilson, Evans, & Watson, 2002, p. 645). Moreover, there is considerable overlap between the neural areas involved in both retrospective episodic and prospective memory (Martin et al., 2007; West & Krompinger, 2005), and prospective memory can be thought of as a type of episodic memory (Roediger, 1996). This raises the possibility that handedness differences observed for retrospective memory may extend to prospective memory. Accordingly, Experiment 1 explores potential handedness differences in self-reported prospective memory, while Experiment 2 looks at potential handedness differences in a performancebased measure of prospective memory in young adults in the age group of 17–25 years. This strict age criterion was adopted following results that show changes in PM and the choice to use aids for better PM performance as a function of age (Cuttler & Graf, 2007;

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Long, Cameron, Karju, Lutz, & Means, 1999). Additionally, the current study is theorized on the rationale that handedness has its links to inter-hemispheric interaction, hence the involvement of the corpus callosum studies show a progressive decline in its myelination with increasing age (e.g., Hasan et al., 2009). 2. Experiment 1 2.1. Method 2.1.1. Participants 105 participants from an Introduction to Psychology course participated as part of another memory study in exchange of research credit towards their class. However, due to – incomplete questionnaire data (n = 18) and over aged participants whose age was over 3 SD from the mean (n = 5; 25–50 years), data from 82 participants (55 females, Mage = 19.24 years, SD = 1.24, range – 17–24 years) were included for the final analysis. 2.1.2. Materials The Prospective and Retrospective Memory Questionnaire (PRMQ; Crawford, Smith, Maylor, Della Salla, & Logie, 2003) is a 16-item scale that was administered to obtain self-report data on minor memory mistakes experienced in daily life. The scale is composed of PM questions (e.g., do you forget appointments if not prompted by someone else or by a reminder such as calendar or diary?) and retrospective memory (RM) questions (e.g., Do you fail to recall things happened to you in the last few days?). Participants were asked to report the frequency of such cognitive failures on a Likert scale of 5 points (1 = never to 5 = very often) with higher scores reflecting increased difficulties in the memory domain. The Edinburgh Handedness Inventory (EHI; Oldfield, 1971) is a 10-item scale that was administered to check for hand preference and to categorize participants on the basis of strength of handedness (consistent vs. inconsistent handers). 2.1.3. Procedure PRMQ and EHI questionnaires were administered as filler tasks as part of another memory study. Degree of handedness was measured by administering the EHI and the median split method was performed on the absolute scores to obtain a cut off to divide the group into consistent- vs. inconsistent-handers (Propper et al., 2005). The EHI median score was 80, and all those who were above the median score were classified in the consistent-handed group (n = 38; MEHI score = 96.05, SD = 5.71) and those with a score of 80 and below were classified in the inconsistent-handed group (n = 44; MEHI score = 57.84, SD = 18.69).

case of RM scale, there was a main effect of gender, F(1, 78) = 6.44, p = 0.01, partial g2 = 0.08. No significant main effect of handedness, or interaction effect between gender and handedness were present (p > .1) A 2  2 between subjects’ ANOVA was attempted on the total scores of the PRMQ; The main effect of gender was present, F(1, 78) = 4.97, p = 0.03, partial g2 = 0.06. Gender was a significant factor in self-report memory lapses, with females reporting significantly less RM memory lapses and nominally better PM recall in daily life as compared to males. Studies have not found gender differences in metamemory abilities (e.g., Hultsch, Hertzog, & Dixon, 1987; Ponds & Jolles, 1996), however there may be a female advantage in verbally recalling/being conscious of episodic memory performances from the past (Herlitz & Rehnman, 2008). Results did not show main effects of handedness in PM or RM based on PRMQ, although a past study on the Everyday Memory Questionnaire showed consistent handers’ reporting significantly more difficulties in monitoring tasks and conversations, factors that tap into absent mindedness and recall failures (Christman & Propper, 2008). In the current study, both consistent- and inconsistent-handed individuals in this study reported more or less similar frequency of PM lapses in daily life. It is worth noting that despite the robust evidence for handedness differences in actual episodic retrieval, there were no handedness differences in participants’ self-reporting of their memory ability. This may reflect that fact that consistent-handers are more prone to the Dunning–Kruger effect, in which people overestimate their ability (and/or underestimate others’ ability) on common tasks (Rose, Jasper, & Corser, 2012). Thus, consistent-handers may have overestimated their retrospective memory skills. Owing to limitations of self-report data, a follow-up study was carried out to check for handedness differences in a performancebased PM task using the Memory for Intentions Screening Test (MIST; Raskin & Buckheit, 1998). While there are several experimental and clinical tests available to measure PM, the MIST was used for the study for the following reasons. It is a standardized test that can be used for both healthy and patient samples to assess PM. The test incorporates not only the important PM based measures of time and event cues but also attributes such as responding in verbal or action modes, and the effect of delay from the time the intention is encoding until it is executed at the requested time point. Furthermore, it’s an ecologically valid tool with instructions having strong relevance to daily life (Raskin, 2009). Finally, in addition to extending the handedness study in the PM domain, we also took this opportunity to extend handedness research into the clinical area.

3. Study 2 2.2. Results and discussion 3.1. Method Separate 2 (handedness groups) by 2 (gender) between subjects’ ANOVA was performed on the PM and RM scales and the total scores of the PRMQ; descriptive statistics are presented in Table 1. In terms of the PM scale, there were no significant main effects of handedness, gender and their interaction (p > .1). However, in the

3.1.1. Participants 159 participants from an Introduction to Psychology class participated in the study in exchange for research credit towards their class. However, 16 participants were excluded from the analyses

Table 1 Mean scores (SD) of the prospective memory scale of the PRMQ across handedness and gender groups. PRMQ

Prospective memory Retrospective memory Total PRMQ scores

Consistent handers

Inconsistent handers

Males n = 11

Females n = 27

Males n = 16

Females n = 28

27.73 (3.32) 31.55 (4.63) 59.27 (7.00)

26.26 (5.21) 28.37 (3.51) 54.63 (8.04)

28.75 (4.75) 30.56 (4.05) 59.31 (8.38)

26.32 (5.28) 28.96 (4.03) 55.29 (8.60)

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because of incomplete handedness data (n = 3), comprehension issues due to either non-fluency in English or hearing problems (n = 3), ages more than 3 SD from the sample mean (n = 7; 27– 50 years) and poor performance on the MIST specified as scores that were 3 SD below the mean (n = 3). Data from 143 participants (80 females, Mage = 19.06 years, SD = 1.14, range = 17–23 years) were analyzed for this study. 3.1.2. Materials Prospective memory (PM) was assessed using the Memory for Intentions Screening Test (MIST; Raskin, 2004; Raskin & Buckheit, 1998). The test measures PM based cues, (a) time based – that requires performing the intent after the lapse of time and (b) event based – that requires performing the intent in response to an external event or physical stimulus. The test also provides results for the effect of delay between encoding an intention and recalling it at a later point (2 min vs. 15 min), during which time participants are also involved in a secondary ongoing task (solving word puzzles), and the response modality for the tasks (verbal vs. action). Thus, test items are combinations of all three characteristics; e.g., In 2 min, ask me what time this session ends (time based = In 2 minute and verbal modality = the participant is required to ask about when the session ends); e.g., when I show you the tape recorder, ask me to rewind the tape (event based = showing of the tape recorder, verbal modality = asking the experimenter to rewind the tape); e.g., when I hand you a red pen, sign on the paper (event based = handing over the red pen, action modality = sign on the paper). The test consists of eight different PM tasks administered in about 30 min with a distractor task that involves solving word search puzzles. Scoring is based on a three point scale for time based items: Correct response = 2 points, partially correct response = 1 point, and no response/incorrect response = 0 points, whereas event based items are scored on an all or none basis, with 2 points for a correct response and 0 points for partially/completely incorrect response. The test generates six scores for the six subscales that represent time PM, event PM, PM responses given at varying lengths of delay after the instruction is given (2 min and 15 min), verbal modality of responding and action based modality of responding (scores range between 0 and 8, with each scale being composed of four items; for detailed psychometric properties, see Raskin, 2009; Woods, Moran, Dawson, Carey, & Grant, 2007). 3.1.3. Procedure PM task and the EHI were part of a battery of tests that was administered individually to each subject. The order of the test was maintained for all participants, with the PM task administered before the completion of the EHI. A median split was performed on the EHI absolute scores, and the obtained median was 85. Participants with scores at or above the median were classified as the consistent-handed group (n = 73; MEHI score = 95, SD = 5.95) and the rest were classified as the inconsistent-handed group (n = 70; MEHI score = 58.29, SD = 23.31). The MIST Form A was administered to the participants as per the standardized method proposed by the authors (for more information about the test and the administration protocol, see, Woods et al., 2007).

edness and gender) in each ANOVA. Data are shown in Table 2. None of the mixed ANOVAs yielded main effects or interactions involving handedness (p > 0.1), although nominal differences between handedness groups were seen, with the inconsistenthanders scoring higher than the consistent-handers across PM tasks. Significant gender differences were present for time and event PM, (F(1, 139) = 6.112, p = 0.015, partial g2 = 0.04), delay periods for time PM (F(1, 139) = 6.112, p = 0.015, partial g2 = 0.04), and response modality, (F(1, 139) = 6.112, p = 0.015, partial g2 = 0.04), with females outperforming males in all the three PM tasks. 3.3. Discussion Systematic gender differences were obtained, with females displaying better prospective memory than males, replicating previous findings (e.g., Maylor & Logie, 2010). However, no significant handedness differences in prospective memory were observed, and, although inconsistent handers did perform nominally better across conditions, the effect sizes were very small. Thus, unlike retrospective episodic memory, there do not appear to be reliable handedness differences in prospective memory. 4. General discussion The research aimed to check for handedness effects in PM by means of a self-report measure and an objective, performancebased test of PM. These studies were based on the premise that since both RM and PM are episodic in nature (Roediger, 1996), and use similar neural networks (e.g., West & Krompinger, 2005), an inconsistent-handed advantage may be present in PM, as has been the case for retrospective episodic memory paradigms. Neither of the studies presented here show a significant handedness effect. One of the explanations for not finding a handedness effect could be that PM follows a different trajectory for retrieving intentions. Unlike RM paradigms, where recall may be better facilitated by using spatiotemporal context, recalling intentions are more often than not, required to be internally generated (particularly for time based PM tasks) to successfully execute a task at a later point. It is possible that the role of spatiotemporal context is present, but it may be secondary whereas, generating the intention by oneself to execute a task is a primary requirement. Additionally, recalling intentions in their exact forms may initially load on a semantic memory network (in other words, remembering the gist of the intention) than on an episodic memory network. This explanation gains support from past studies that have not shown handedness differences in direct (Christman et al., 2004; Propper et al., 2005) and indirect (Lyle, Logan, et al., 2008; Lyle, McCabe, et al., 2008) tests of semantic memory. Another possible reason for not finding the handedness difference in PM is the possibility of participants indulging in rehearsal in order to keep the intention in its active state for actualization in

Table 2 Mean scores (SD) of the six sub scales and the total score of PM (MIST) across handedness and gender groups. MIST

3.2. Results Given there are six sets of scores generated, we considered pairs of scores for each domain (cue: time vs. event; length of delay for time based: 2 min vs. 15 min; response modality: verbal vs. action) separately as within subject variables. This resulted in three separate 2  2  2 mixed ANOVAs, one for each of the aforementioned within subject variables, with two between subjects’ factors (hand-

Time Event 2 min 15 min Verbal Action Total score

Consistent handers

Inconsistent handers

Males n = 27

Females n = 46

Males n = 36

Females n = 34

6.85 (1.10) 6.81 (1.39) 7.81 (0.55) 5.85 (1.46) 7.78 (0.58) 5.89 (1.55) 41.00 (4.99)

7.02 (1.04) 7.35 (1.20) 7.91 (0.41) 6.46 (1.60) 7.67 (0.63) 6.70 (1.41) 43.11 (5.27)

6.92 (1.05) 7.17 (1.30) 7.83 (0.51) 6.25 (1.75) 7.67 (0.53) 6.42 (1.70) 42.25 (5.84)

7.24 (0.92) 7.59 (0.96) 7.94 (0.34) 6.88 (1.32) 7.76 (0.55) 7.06 (1.13) 44.47 (4.21)

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the future time (Tan & Kvavilashvili, 2003); this factor is not necessarily recruited in RM processes as recall is often times tested incidentally. It was initially proposed that both RM and PM processes recruit similar neural networks (in specific Brodmann’s area (BA) 10), however RM retrieval recruits additional sites within the prefrontal cortex (BA 8, 9, 47/45) and though bilateral, show a right hemisphere more than left bias (Lepage, Ghaffar, Nyberg, & Tulving, 2000) as compared to PM processes which tend to be predominantly bilaterally represented (Burgess, Gonen-Yaacovi, & Volle, 2011; Burgess, Scott, & Frith, 2003). The current results could also be related to the Cortical Asymmetry of Reflective Activity hypothesis (CARA; Nolde, Johnson, & Raye, 1998). The hypothesis is in accordance with the HERA model but additionally states that the left hemisphere engages in deliberative systematic processes (detailed, initiation of self-cueing) whereas the right hemisphere engages in reflective heuristic processes (temporarily holding on to actively maintained information). It is possible that PM is dominated by the deliberative attempts to remember the intentions but less by heuristic processes. Future studies could address this point of view. Both studies showed a female advantage for experiencing less number of memory problems in daily life and in the performance based PM task. As an individual difference factor, some studies that have found robust gender differences attribute it to females indulging in rehearsal of the intention more than males (Tan & Kvavilashvili, 2003). Furthermore, females show the intention-superiority effect whereby anything related to the intention is noticeable, especially in the first minutes of the intention formulation (Penningroth, 2005). In conclusion, the current studies strongly suggest that handedness differences obtained in the domain of episodic retrieval of episodic memories do not extend to the domain of prospective memory. The presence of gender, but not handedness, differences in prospective memory stands in contrast to the routine finding of handedness, but not gender differences in retrospective memory, providing further support for the functional and anatomical distinctions between these two memory types.

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Handedness differences observed in episodic memory retrieval do not extend to the domain of prospective memory.

A robust inconsistent handed advantage exists for episodic retrospective memory processes. The current study was undertaken to test whether this hande...
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