Relationship between memory performance, visuospatial
function and functional lateralization in adults
Katja Bilić
Spring 2015
Master's Thesis in Psychology, 15 ECTS Supervisor: Professor Louise Rönnqvist
2 Acknowledgments
I want to thank my supervisor Professor Louise Rönnqvist for guiding me through the process of writing this thesis. Her advice and support were very valuable and she helped me become a better student.
Also, I want to thank Dr Michael Rönnlund who offered valuable support regarding the Betula project dataset and statistical analyses.
Without Dr Greg Neely's open-mindedness this project wouldn’t have reached its end, thank you for accepting my ideas.
Last but not least, I want to thank my family for any kind of support they have offered throughout my studies.
3 RELATIONSHIP BETWEEN MEMORY PERFORMANCE, VISUOSPATIAL FUNCTIONS,
AND FUNCTIONAL LATERALIZATION IN ADULTS Katja Bilić
Age-related decline in memory and other cognitive functions, such as visuospatial functions is widely studied and well documented. In recent years, some studies have also found relationships between memory performance and functional body lateralization, with individuals who are inconsistently lateralized (e.g. have inconsistent handedness) scoring higher on episodic memory tests. The objectives of this study were to investigate
relationships and possible differences between episodic and semantic memory performance, and visuospatial functions as a function of functional lateralization consistency in a large population-based study. In total, 1283 adult men and women participants, with age ranging from 25 to 100 years, were tested within the Betula prospective cohort study (Nilsson et al., 1997) where they were included in the fifth wave (T5) of data collection. Participants were divided into groups of consistent or inconsistent functional lateralization regarding respective hand-, foot-, and eyedness. Results revealed weak to moderate relationship between variables of functional laterality and its consistency. While age was significant predictor of memory performance and visuospatial functions, sex and functional laterality consistency variables were insignificant. Results are discussed in relation to previous studies and to hemispheric interaction theory.
Age-related decline in performance attracts many researchers who aim to understand human functioning throughout a lifespan. Although some popular laic theories postulate age-related decline in performance and cognitive functions, and older adults are often in everyday life perceived as less functional in cognitive domain than younger adults, evidence from scientific research is usually not so straightforward and studies reveal different and sometimes opposite results. Various confounding variables, such as cognitive reserve (Nyberg, Lövden, Riklund, Lindenberger & Bäckman, 2012) or interhemispheric interaction (Christman & Propper, 2001), have been considered as mediators of the relationship of cognitive performance and age. For instance, interhemispheric interaction, measured as the (in)consistency of lateral preference, is believed to enhance memory retrieval (Lyle,
Hanaver-Torrez, Hacklander & Edlin, 2012). In this study, the relationship between episodic and semantic memory, visuospatial functions, and functional lateralization will be explored.
4 Aging and Memory
Age-related decline is widely studied in the domain of memory. Memory is involved in almost all daily life routines, attention, perception, etc., and its preservation in the older age can be used as an indicator of fitness and health, or an indicator of successful aging (Nyberg et al., 2012). Memory systems and categories are in detail explained in several papers (e.g., Nyberg & Tulving, 1996; Squire, 2004; Tulving, 2002), while neural correlates are explained in Cabeza and Nyberg (2000).
This study focuses on semantic and episodic memory. Semantic memory refers to general knowledge about the world, or memory of facts, and it is usually studied with tasks involving word fluency, vocabulary and category associations (Nyberg and Tulving, 1996;
Squire, 2004). On the other hand, episodic memory consists of knowledge about personally experienced events and is referred to as “the memory of subjective time” (Tulving, 2002). It is usually studied with tasks involving recall and recognition of the material. Although there is reliable evidence for dissociation of semantic and episodic memory systems, well
explained in Nyberg and Tulving (1996), they are not completely dissociated; the systems interact to an extent. For instance, episodic memory encoding is closely related to semantic memory retrieval and the two systems interact in almost all situations which require usage of memory (Cabeza & Nyberg, 2000). Memory systems are also lateralized to an extent,
especially episodic memory. An important model of episodic memory lateralization is the hemispheric encoding/retrieval model known as the HERA model (Tulving, Kapur, Craik, Moscovitch & Houle, 1994; Habib, Nyberg & Tulving, 2003; Tulving, 2002). The HERA proposes left prefrontal cortex is more involved in the encoding of the episodic memory, and right prefrontal cortex is more involved in the episodic memory retrieval (Habib et al., 2003). According to the HERA, episodic memory is more dependent on the hemispheric interaction than semantic memory. A biological marker for the degree of the hemispheric interaction is hand preference or handedness, which is considered to be another important control variable in studies which aim to explore degrees of lateralization of functions and its relation to performance. Handedness and other forms of functional lateralization, such as footedness and eyedness, and its relation to memory performance and visuospatial functions are of interest in this study.
Different forms of memory are differently influenced by age. For instance, semantic memory shows positive age gradients until the age of 60 (Lövden et al., 2004), while episodic memory shows negative age-related gradients. On the other hand, non-declarative forms of memory are rarely changed during a lifetime (Rönnlund, Nyberg, Bäckman & Nilsson, 2005). Previous studies have reported mixed evidence on the average age of onset of the
5 memory decline. Cross-sectional studies show episodic memory decline begins as early as age of 20, while longitudinal studies report that episodic memory decline does not start until the age of around 60 (Lövden et al., 2004). Population-based studies report high variability in successful cognitive aging, with some individuals showing no age-related decline, and some showing high rates of decline (Nyberg et al., 2012). Such variability and different results across studies lead to an assumption of confounding variables which may underlie the relationship between performance and age. One of those mechanisms was recently proposed in very influential theories of successful aging which focus on so called brain maintenance hypothesis. For detailed explanation of the brain maintenance reader should consult Nyberg et al., (2012), Pudas et al., (2013), and Pudas, Persson, Nilsson and Nyberg, (2014).
Handedness, Aging and Memory
Handedness is a feature which in many studies represents brain lateralization. It can include a range of abilities, such as hand preference, hand performance or hand strength (Siengthai, Kritz-Silverstein & Barrett-Connor, 2008; Somers, Shields, Boks, Kahn & Sommer, 2015).
Results from research on handedness can be helpful in addressing the relationship of brain lateralization and behaviour or brain functions. Besides handedness, biological markers for the degree of brain lateralization are footedness, eyedness, and together they are comprised into an overall laterality index (Porac, 1997). Handedness is so far the most explored feature of lateral preference, but suggestions on including the assessment of footedness and
eyedness exist in spite of so far inconsistent results on the relationship between hand, foot and eye (Barut, Ozer, Sevinc, Gumus & Yunten, 2007; Porac, 1997). Handedness is argued to be under greater influence of social learning and culture, and therefore exploration of other laterality indicators and their relationship with handedness is considered to be more reliable index of lateral preference (Mandal, Pandey, Singh & Ashtana, 1992; Barut et al., 2007). A brief literature review is available from Barut et al., (2007). In general, hand, foot and eye preference are positively correlated, but different coefficients emerge as a consequence of laterality measurement.
Relationship of handedness and aging is a less explored field so far.
Sivagnanasunderam et al., (2015) give an interesting review of handedness throughout a lifespan and present a study of changes in the strength of manual asymmetries, defined as differences in performance between dominant and non-dominant hand. They conducted a study in which they hypothesized asymmetry differences will follow a reversed U-shape curve as people age, and their study shows manual asymmetries are highly dependent on the nature of the task participants are engaged into. One important notice considering the
6 relationship of hand and eye preferences and their relation to aging was reported by Porac (1997). Her study revealed older adults have more congruent hand and eye preference than younger adults, which was also reported in Bourassa, McManus and Bryden (1996).
Research on handedness reveals that when handedness stands for hand preference, people are usually divided into left- or right-handers. According to Siengthai et al., (2008) and Somers et al., (2015) around 90% of population is right-handed which has been stable since the early history of humanity. Handedness has a genetic and cultural background, but some theories also link left-handedness to birth trauma and prenatal testosterone levels (Somers et al., 2015; Van der Elst, Van Boxtel, Van Breukelen & Jolles, 2008).
Handedness can also be considered as a continuous ability or an individual difference variable. Then, people are divided into consistent handers (CH) and inconsistent handers (ICH) groups (Beaton, Magowan & Rudling, 2012; Lyle, McCabe & Roediger, 2008;
Prichard, Propper & Christman, 2013). For instance, if a person belongs into a CH group, he or she consistently uses the same hand in particular manual situations, but if he or she belongs to an ICH group that means he or she uses the non-dominant hand for at least one manual activity (Prichard et al., 2013). The same rule applies for the usage of the foot or the eye. In the context of sex differences, men show more bilateral activity and are more often ICH (Porac, 1997; Prichard et al., 2013). It has been argued handedness consistency assessment is a more reliable approach to handedness measurement. Lyle et al., (2012) suggest the consistency of handedness, regardless of its direction, is an important factor to study in relation to memory because it predicts baseline memory accuracy and potential for memory enhancement. Their results showed subjects from the consistent handedness group had poorer results on associative recognition tests and showed more false recognition. Lyle et al., (2012) debate non-consistent participants had better inter-hemispheric
communication and that hand (in)consistency is an individual difference factor which should not be neglected in studies involving memory. Propper, Christman and Paneuf (2005) follow a similar suggestion when they propose handedness is best measured as a category from perfectly mixed handed to perfectly consistent, and Cherbuin, Sachdev and Anstey (2011) agree. Prichard et al., (2013) give a more detailed review of the studies and follow the same suggestions as Cherbuin et al., (2011), Lyle et al., (2012), and Propper et al., (2005).
The theory which links handedness and memory performance is the hemispheric interaction theory (Christman & Propper, 2001; Lyle, et al., 2008). ICH participants showed superiority on memory tests which are dependent on the hemispheric interaction, such as free recall, paired-source recall, autobiographical memory and source memory, and they are believed to have a higher degree of communication among brain hemispheres (Prichard et
7 al., 2013). This theory has two main assumptions, one is that handedness is a behavioural marker for the degree of hemispheric interaction and the other is that hemispheric interaction has consequences for memory. One of such consequences is that ICH may enhance memory retrieval (Christman & Propper, 2001). The size of corpus callosum plays an important role in this theory because it is the main brain structure involved in the hemispheric interaction (Luders et al., 2010). Under this assumption, Lyle et al., (2008) conducted a study where verbal paired associate recall task, source memory task (episodic memory tests, both believed to rely on the hemispheric interaction), facial recognition task and forward digit span (semantic memory tests, both believed not to rely on the hemispheric interaction) task were used with younger and older adults. Observed results are in line with the hemispheric interaction theory, but only in case of younger adults. Older ICH group of adults was not superior in verbal paired associate recall task and source memory task.
Authors believe such results have emerged as a consequence of degeneration of the corpus callosum which happens with age. It gets smaller and differences between CH and ICH individuals slowly diminish. Similar study was conducted earlier by Propper, et al., (2005) and results were in line with those observed by Lyle et al., (2008).
It is notable that the interactions among memory, handedness and age are highly complex. Both memory and brain lateralization undergo age-related changes and studies conducted so far lead to an assumption that changes in cognitive functioning and changes in laterality may moderate one another. Research results presented in this paper focus on handedness since to our knowledge footedness and eyedness have not been studied in relation to memory. Nevertheless, results based on handedness can be used as guidance for research on other aspects of laterality. Various studies (e.g. Christman & Butler, 2011;
Christman & Propper, 2001; Lyle et al., 2008, 2012; Propper et al., 2005) have attempted to explain the relationship between functional lateralization (measured as handedness),
memory and age, but so far research consensus does not exist and is rarely extended to various cognitive functions. Focus is mainly on episodic memory and there is strong evidence of ICH superiority in that domain (Christman & Butler, 2011), but ICH superiority does not seem to extent to a domain of semantic memory (Lyle et al., 2008) and prospective memory (Sahu & Christman, 2014). A study by Piper et al., (2011) examined handedness differences in spatial functions, but they categorized handedness only as being left- or right-handed, and found left hand superiority in visuospatial functions, which was a novel finding at that time.
Thus, it seems that different results emerge as a consequence of measurement and
constructs involved in the analysis and general consensus on the assessment still does not exist.
8 The objectives of the present study were to investigate the relationship and possible differences between memory performance, visuospatial functions, and functional
lateralization in a large population-based sample. In addition to previous studies, this study will also, besides assessment of hand preference and its consistency, include assessment of foot and eye preference and consistency. The aim is to address the following questions:
1. To what extent is inconsistent and consistent functional lateralization,
operationalized as hand-, foot-, and eye-consistency, and overall strength of laterality related to cognitive functions, operationalized as episodic memory, semantic memory and visuospatial functions?
2. To what extent are functional lateralization, cognitive functions and the relationship among them affected by age and sex?
Based on previous research, hypotheses to provide answers to research questions were set as follows: 1. Inconsistent functional lateralization is related to superior episodic memory performance. 2. Age and sex moderate the relationship between functional lateralization and cognitive functioning.
Method Participants
Participants in the present study were derived from the Betula prospective cohort study (Nilsson et al., 1997, 2004), a longitudinal study based in Umeå, Sweden, in which data collection began in 1988. So far, data was gathered during six waves (T1-T6) of collection and around 4500 participants were assessed. Attendance in this study is voluntary and
participants were randomly selected from a population. The objectives of the Betula (Nilsson et al., 1997, 2004) include investigation of memory development and changes in adulthood, as well as health development. Also, the goal is to determine risk factors and predictors of dementia, and define successful aging. During data collection participants undergo complex cognitive, health, social and lifestyle testing. Detailed description of all tests and materials used in the Betula can be found in Nilsson et al., (1997, 2004).
Since the focus of the present paper is on associations between cognitive performance and functional laterality, the later variables were tested at T5 of the Betula study, the
participants of the core sample for the current study belonged to the fifth wave of data collection in the Betula study (Nilsson et al., 1997, 2004): sample T5, which took place between years 2008 and 2010. The sample consisted of data from in total 1283 participants
9 whose age ranged from 25 to 100 years with a mean of M = 64.56 (SD = 14.91), and included people in 16 age cohorts: 25, 30, 35, 40, 45, 50, 55, 60, 65, 70, 75, 80, 85, 90, 95, 100 of age when tested. In this sample, 583 (45.4%) participants were male, and 700 (54.6%) female.
Average age of education was M = 12.22 (SD = 4.27).
Notification: before T5 (in samples T1-T4), data regarding handedness was gathered simply on hand preference (right- or left-handed), while T5 included more detailed
assessment of handedness, together with footedness and eyedness.
Procedure and measures
Materials used in the Betula study were constructed with an aim of covering various memory systems and processes. All used materials, study design and detailed procedure is explained in Nilsson et al., (1997). To briefly summarize, health and memory testing each lasted from 1.5 to 2 hours for each participant, and each wave of data collection lasted for 2 years. In the following section measures relevant for this study are described.
Episodic memory (EM)
Episodic memory was measured by six tests. Four tests focus on a task of studying a list of 16 short sentences in an imperative form (e.g. “roll the ball”, “break the match”) with or without enactment of the material, and include (1) free recall of 16 enacted sentences, (2) free recall of 16 non-enacted sentences, (3) category-cued recall of nouns from enacted sentences, (4) category-cued recall of nouns from non-enacted sentences. Other two tests include (5) free recall of 12 verbally presented nouns, and (6) activity memory measure where participants had to remember all the tests they have participated in. Six episodic memory test were used as a basis for computing an episodic memory score. This score was derived from a principal component analysis with promax rotation that extracted a single component using the Kaiser rule (eigenvalue > 1). The regression option in SPSS was used as a basis for computing the factor score.
Semantic Memory (SM)
Semantic memory was measured by three tests: (1) vocabulary, (2) word fluency and (3) general knowledge. In (1) vocabulary or word comprehension test participants had to choose a synonym for a given word among 5 words on a list. The list included 30 words and their synonyms, and participants had 7 minutes to complete the task. (2) Word fluency measure was comprised of three separate test situations, each lasting one minute. In the first
situation, task of the participants was to generate as many words as possible starting with a
10 letter “A”. In the second situation task was to generate as many five-letter words as possible starting with the letter “M”. In the third situation, task was to generate as many professions as possible starting with the letter “B”. (3) General knowledge measure was derived from the test called Item Recall. It consists of 10 questions to which answer is possible only on the basis of general knowledge. Three semantic memory tests were used as a basis for computing a semantic memory score. This score was derived from a principal component analysis with promax rotation that extracted a single component using the Kaiser rule (eigenvalue > 1).
The regression option in SPSS was used as a basis for computing the factor score.
The psychometric properties of the memory measures used in the Betula project have in previously study been found to be acceptable (Rönnlund and Nilsson, 2006a). It was found that the reliability estimates for both episodic memory (r = 0.83) and semantic memory (r = 0.82) were high. In addition, stability coefficients were substantial (r = 0.77–
0.83) and did not differ between younger (35–55 years) and older adults (60–80 years), as available from Rönnlund and Nilsson, (2006a).
Block Design Test (BDT; Wechsler, 1981)
The BDT is a sub-test of the Wechler Adult Inteligence Scale (WAIS). To complete the BDT participants have to duplicate a maximum of 10 target patterns of four or nine two-colour bricks. The BDT is designed to assess visuospatial constructional abilities, and it was
administered according to the WAIS-R manual (Wechsler, 1981). Reliability analysis for this test is available from Rönnlund and Nilsson (2006a).
Functional Lateralization
Functional lateralization was measured by self-report questions for hand, foot and eye preference. To control false answers due to not knowing or not being sure, participants were instructed to imagine performing a task and to perform it at the concrete testing situation.
The hand-, foot-, and eye-preference indexes were further calculated by the equation (Right – Left) / (Right + Left) from the laterality questionnaires outcome scores, respectively.
Hand preference, hand consistency and handedness was assessed by a modified version of Edinburgh Handedness Inventory (Oldfield, 1971). In a modified version the participants had to answer 10 questions about preferred hand in following activities: writing, drawing, throwing a ball, cutting with scissors, teeth-brushing, using a knife without a fork, eating with a spoon, holding a stick while mopping the floor, lighting a match, and opening a jar. Participants had to respond if they always use one hand (right or left), use one hand most of the time (right or left), or use both hands equally often. The outcome was a handedness
11 index which ranged from -1 (consistent left preference) to 1 (consistent right preference).
Later in the analysis values were transformed to a range from 0 (consistent left preference) to 2 (consistent right preference).
Foot preference, foot consistency and footedness was assessed by a modified version of Lateral Preference Inventory (Coren, 1993). In this modified version the participants had to answer 6 questions about preferred foot in the following activities: kicking a ball, climbing up a ladder, picking up marble with toes, putting on shoes while sitting, beating time, and moving from a standstill. Participants had to respond if they always use one foot (right or left), use one foot most of the time (right or left), or use both feet equally often. The outcome was a footedness index which ranged from -1 (consistent left preference) to 1 (consistent right preference). Later in the analysis values were transformed to a range from 0 (consistent left preference) to 2 (consistent right preference).
Eye preference, eye consistency and eyedness was assessed by a modified version of Lateral Preference Inventory (Coren, 1993). In this modified version the participants had to answer 3 questions about preferred eye in the following activities: peeking through a
keyhole, looking through a telescope, and looking in a sniper scope. Participants had to respond if they always use one eye (right or left), use one eye most of the time (right or left), or use both eyes equally often. The outcome was an eyedness index which ranged from -1 (consistent left preference) to 1 (consistent right preference). Later in the analysis values were transformed to a range from 0 (consistent left preference) to 2 (consistent right preference).
In the analysis participants were divided into inconsistent (IC) group and consistent (C) group. Based on the definition of inconsistent or mixed lateralization, IC participants use non-dominant joint/sensory organ for at least one activity and should not be confused with ambidexterity (Prichard et al., 2013; Propper et al., 2005). Lyle et al., (2008, 2012) and Propper et al., (2005) suggest using a median as a cut-off value between groups. That suggestion was followed with beliefs it will ensure better comparison of results from this study with previous studies. In this study, groups were split into IC and C based on a median value of C = 2 for handedness, C = 1.5 for footedness and C = 1.58 for eyedness. IC
handedness group comprised of 667 (52.0%) participants, and C handedness group of 606 (48.0%) participants. IC footedness group had 438 (40.1%), and C footedness group 654 (59.1%) participants. IC eyedness group consisted of 374 (34.4%), and C eyedness group of 712 (65.6%) participants. In addition, an overall laterality index was calculated and
participants were also split into IC and C groups. In this case, median value was C = 1.67, and IC group consisted of 555 (49.7%) and C group of 561 (50.3%) participants.
12 Statistical analyses
Data was analysed with a help of IBM SPSS Statistics 22.0 for Windows. To address research questions, data was analysed by calculating correlation and partial correlation coefficients among variables of functional lateralization and variables of cognitive functioning. Also, data was analysed by hierarchical multiple regression analyses with cognitive functions as an outcome and functional lateralization variables, age as a continuous variable, sex,
interactions between age and variables of functional lateralization, and interactions between sex and variables of functional lateralization as predictors.
Results Correlation and partial correlation coefficients
To explore the direction and strength of the relationship between variables of cognitive functioning and functional lateralization, calculations by use of Pearson correlation coefficients were conducted.
Correlation coefficients and their significance values are shown in Table 1.
Table 1. Correlation coefficients between EM, SM, BDT, handedness,
footedness, eyedness, overall laterality index, and age.
EM SM BDT Handedness Footedness Eyedness Overall Age
EM 1
SM .53** 1
BDT .58** .40** 1
Handedness .04 .04 -.01 1
Footedness -.07* -.11** -.12** .58** 1
Eyedness .04 -.01 .05 .33** .28** 1
Overall .01 -.03 -.02 .76** .74** .78** 1
Age -.52** -.11** -.60** .04 .09** -.07* .00 1
Note: *p < .05, ** p < .01
After controlling for age and sex in partial correlation analysis, almost all correlation coefficients and their significance remain the same. Change was noticed only in the
relationship between episodic memory and footedness, where correlation coefficient before controlling for age and sex was r = -.07 (p < .05), and after controlling for age and sex coefficient was r = -.08 (p < .01).
13 Episodic memory as an outcome variable
Multiple regression analysis with age, sex and handedness as predictors indicated that three predictors accounted for 29% of variance in episodic memory (R² = .29, F (3, 1078) = 145.74, p < .001). Age significantly negatively predicted episodic memory (β = -.52, p < .001), as did sex (β = -.13, p < .001) and handedness (β = -.05, p < .05). After including interaction terms between age and handedness, and sex and handedness, predictors accounted for 29% of variance in episodic memory (R² = .29, F (5, 1976) = 87.97, p < .001). Age remained the only significant predictor of episodic memory (β = -.40, p < .001), while sex (β = -.16, p > .05) and handedness (β = -.09, p > .05) became insignificant. Interaction terms age*handedness (β = -.12, p > .05) and sex*handedness (β = .04, p > .05) did not significantly explain variance in episodic memory. In this case, younger participants had better results in episodic memory tests.
Age, sex and footedness together accounted for 30% of variance in episodic memory (R² = .30, F (3, 1060) = 148.93, p < .001). Age significantly negatively predicted episodic memory (β = -.52, p < .001), as did sex (β = -.15, p = .001) and footedness (β = -.10, p <
.001). After including interaction terms between age and footedness, and sex and footedness, predictors accounted for 30% of variance in episodic memory (R² = .30, F (5, 1058) = 89.85, p < .001). Age (β = -.39, p < .001) remained the only significant, while sex (β = -.13, p > .05) and footedness (β = -.08, p > .05) became insignificant predictors of episodic memory.
Interaction terms age*footedness (β = -.13, p > .05) and sex*footedness (β = -.03, p > .05) do not significantly explain variance in episodic memory. In this case also, younger participants had better results in episodic memory tests.
Age, sex and eyedness together accounted for 29% of variance in episodic memory (R² = .29, F (3, 1054) = 140.41, p < .001). Age significantly negatively predicted episodic memory (β = -.52, p < .001), as did sex (β = -.13, p = .001). Eyedness did not emerge as a significant predictor of episodic memory (β = -.04, p > .05). After including interaction terms in the analysis, predictors accounted for 29% of variance in episodic memory (R² = .29, F (5, 1052) = 84.30, p < .001). Age remained the only significant predictor of episodic memory (β = -.44, p < .001). Sex became insignificant predictor (β = -.14, p > .05). Eyedness (β = -.05, p > .05) and interaction terms age*eyedness (β = -.08, p > .05), and sex*eyedness (β = .01, p > .05) did not significantly predict episodic memory. Again, younger participants showed better results in episodic memory tests.
Age, sex, and overall lateral preference together accounted for 29% of variance in episodic memory (R² = .29, F (3, 1083) = 144.65, p < .001). Age (β = -.53, p < .001), and sex (β = -.12, p = .001) significantly negatively predicted episodic memory, while overall lateral
14 preference was not a significant predictor (β = -.04, p > .05). The results remain the same after including interaction terms in the analysis, predictors accounted for 29 % of variance in episodic memory (R² = .29, F (5, 1081) = 87.16, p < .001). Age*overall laterality (β = .03, p >
.05) and sex*overall laterality (β = .15, p > .05) interaction terms do not significantly predict episodic memory. Here, younger participants and women had better results in episodic memory tests.
Semantic memory as an outcome
Age, sex and handedness together accounted for 1% of semantic memory (R² = .01, F (3, 1074) = 5.52, p = .001). Age was the only significant and negative predictor of semantic memory (β = - .098, p = .001). Sex (β = .04, p > .05) and handedness (β = -.04, p > .05) did not significantly predict semantic memory. After including interaction terms in analysis, predictors accounted for 1% of variance in semantic memory (R² = .01, F (5, 1072) = 2.80, p
< .01). Age*handedness (β = -.14, p > .05) and sex*handedness (β = .06, p > .05) interaction terms did not significantly predict semantic memory. In other words, younger participants had better results in semantic memory tests.
Age, sex and footedness together accounted for 2% of variance in semantic memory (R² = .02, F (3, 1057) = 8.71, p < .001). Age was significant negative predictor (β = -.099, p = .001) of semantic memory, as well as footedness (β = -.107, p = .001). Sex (β = .01, p > .05) did not significantly predict semantic memory. After including interaction terms in the analysis, predictors accounted for 3% of variance in semantic memory (R² = .03, F (5, 1055)
= 6.75, p < .001). Results in footedness and sex domain remain the same, while age becomes insignificant (β = .17, p > .05) predictor of semantic memory. Interaction between age and footedness is significant (β = -.28, p < .01), which makes age a moderator of the relationship between footedness and semantic memory. Here, age was split into 2 categories, younger (from 25 to 60 years) and older (from 65 to 100 years) adults. Scatter-plot showed relationship between footedness and semantic memory is stronger in older group (R² = 0.026) of participants than in younger (R² = 0.001) group. Interaction between sex and footedness was not statistically significant (β = .10, p > .05).
Age, sex and eyedness together accounted for 1% of variance in semantic memory (R²
= .01, F (3, 1051) = 6.25, p < .001). Age was significant negative predictor (β = -.10, p = .001) of semantic memory, as well as eyedness (β = -.07, p < .05). In this case, sex (β = -.06, p >
.05) also did not significantly predict semantic memory. After including interaction terms in the analysis, predictors accounted for 1% of variance in semantic memory (R² = .01, F (5, 1049) = 3.96, p = .001). Age (β = -.00, p > .05) and eyedness (β = -.03, p > .05) became
15 insignificant predictors, as well as age*eyedness (β = -.10, p > .05) and sex*eyedness (β = - .07, p > .05) interaction terms.
Age, sex and overall lateral preference together accounted for 2% of variance in semantic memory (R² = .02, F (3, 1079) = 7.30, p < .001). In this case, age (β = -.11, p < .001) and overall lateral preference (β = -.08, p < .001) were significant negative predictors, while sex did not significantly predict semantic memory (β = .04, p > .05). After including
interaction terms in the analysis, predictors explained 2% of variance in semantic memory (R² = .02, F (5, 1077) = 7.77, p < .001). Age (β = -.19, p = .052) and sex (β = -.18, p = .052) became borderline significant predictors, while overall laterality (β = -.30, p = .001) remained significant predictor of semantic memory. Interaction between age and overall laterality was not significant (β = .08, p > .05), while interaction between sex and overall laterality was significant (β = .32, p < .05), which makes sex a moderator of the relationship between overall laterality and semantic memory. When analysis was done split by sex, interaction between overall laterality and sex is significant only in case of female participants (β = -.14, p < .01), but not in male (β = .01, p > .05). The regression coefficient indicated inconsistently lateralized women had better results on semantic memory test then consistently lateralized women.
Block Design Test (BDT) as an outcome
Age, sex and handedness together accounted for 35% of variance in BDT (R² = .35, F (3, 1084) = 200.02, p < .001). Age was significant negative predictor of BDT (β = -.57, p < .001), as well as handedness (β = -.07, p < .01). Sex was significant positive predictor of BDT (β = .08, p = .001). After including interaction terms in the analysis, predictors accounted for 35%
of variance in BDT (R² = .35, F (5, 1081) = 120.46, p < .001). Age (β = -.48, p < .001)
remained significant, while sex (β = .02, p > .05) and handedness (β = -.15, p > .05) became insignificant predictors of BDT. Interactions between age and handedness (β = -.09, p > .05), and sex and handedness (β = .08, p > .05) also did not significantly predict BDT. Younger participants also had better results in BDT.
Age, sex and footedness together accounted for 35% of variance in BDT (R² = .35, F (3, 1066) = 196.71, p < .001). Age was significant negative predictor of BDT (β = -.57, p <
.001), as well as footedness (β = -.07, p < .01). Sex was significant positive predictor of BDT (β = .08, p < .01). After including interaction terms in the analysis, predictors accounted for 35% of variance in BDT (R² = .35, F (5, 1064) = 118.06, p < .001). Age (β = -.51, p < .001) remained the only significant, while sex (β = .03, p > .05) and footedness (β = -.11, p > .05) became insignificant predictors of BDT. Interactions between age and footedness (β = -.06, p
16
> .05), and sex and footedness (β = .05, p > .05) were not significant. Again, younger participants had better results in BDT.
Age, sex and eyedness together accounted for 35% of variance in BDT (R² = .35, F (3, 1061) = 191.02, p < .001). Age was significant negative predictor of BDT (β = -.58, p < .001).
Sex was significant positive predictor (β = .09, p < .001), while eyedness did not significantly predict BDT (β = .00, p > .05). After including interaction terms in the analysis, the
percentage of explained variance in BDT remained the same (R² = .35, F (5, 1059) = 114.57, p
< .001). Age remained significant (β = -.54, p < .001), eyedness remained insignificant (β = - .04, p > .05), and sex became insignificant (β = .04, p > .05) predictor of BDT. Interactions between age and eyedness (β = -.04, p > .05), and sex and eyedness (β = .06, p > .05) were not significant. In other words, younger participants had better results on BDT.
Age, sex and overall lateral preference together accounted for 35% of variance in BDT (R² = .35, F (3, 1089) = 197.34, p < .001). Age was significant negative predictor of BDT (β = -.58, p < .001). Sex was significant positive predictor (β = .09, p < .001), while overall laterality did not significantly predict BDT (β = -.03, p > .05). After including interaction terms in the analysis, predictors accounted for 35% of variance in BDT (R² = .35, F (5, 1087)
= 118.51, p < .001). Age remained significant (β = -.59, p < .001), overall laterality remained insignificant (β = -.10, p > .05), while sex became insignificant (β = .02, p > .05) predictor of BDT. Interactions between age and overall laterality (β = .01, p > .05) and sex and overall laterality (β = .10, p > .05) were not significant. Here also, younger participants had better results on BDT.
Discussion
This study was conducted with the objectives of investigating the relationship and possible differences between memory performance, visuospatial functions, and functional
lateralization by means of handedness, footedness and eyedness in a large population-based sample. To address research questions, participants were divided into groups of inconsistent (IC) and consistent (C) functional lateralization, independent of side preference for
respective category of hand-, foot-, and eyedness. Correlation analyses were applied to address the relationship between variables of functional lateralization and variables of cognitive functioning, whereas regression analyses were applied to address predictive role of variables of functional lateralization, age and sex on variables of cognitive functioning.
Correlation analysis revealed positive, and weak to moderate, relationship between handedness, footedness and eyedness, while correlation coefficients between those variables and an overall laterality index were positive and high. Overall laterality index was included in
17 the analysis in order to see whether global side preference and its consistency is related to measures of cognitive functioning differently than individual variables of functional lateralization. Although the relationship between variables of functional lateralization was significant, its strength observed in this study suggests constructs of handedness, footedness and eyedness are distinct and give valuable information when studied separately. Similar suggestions are given by Mohr and Bracha (2004). In addition, Porac (1997) reports that handedness and footedness respectively are more strongly related with each other than with eyedness, which was also observed in this study.
When predictive value of age, sex and variables of functional lateralization on episodic memory was tested, age was the only significant predictor of episodic memory, respectively. In this study, regression coefficients indicated younger participants performed better than older on episodic memory tests, which is in line with results reported in Lövden et al., (2004) and Nyberg et al., (2012). It is important to note that here age ranged from 25 to 100 years, therefore “young” does not include only young adults, and it also includes middle aged participants. Here age was not further split into categories, what should be something of interest for future research. More detailed review of aging and memory in the Betula study can be found in Lövden et al., (2004). In addition, sex emerged as a significant predictor of episodic memory when entered into analysis with overall laterality index, with regression coefficients indicating women performed better, which was reported previously (Lewin, Wolgers, & Herlitz, 2001). From previous studies (Christman & Butler, 2011;
Christman & Propper, 2001; Lyle et al., 2012), it was expected inconsistent functional lateralization would be related to better episodic memory performance. Although
handedness and footedness emerged as significant predictors of episodic memory, this study did not confirm the first research hypothesis since the effects disappeared after controlling for age and sex. Christman and Propper (2001) conducted a study with 180, Christman and Butler (2011) with 182, and Lyle et al., (2012) with 120 participants. All studies included university students as subjects, and age could not have been controlled since the age range was very limited. This study included a large number of participants from various
backgrounds and in our opinion presents results which could give more reliable information.
In case of semantic memory as dependent factor, age was also a significant predictor when entered into the analysis together with sex, handedness, footedness, and overall laterality index. In those cases, regression coefficients indicated that younger participants showed better results on sematic memory tests. Even though footedness and eyedness also emerged as significant predictors, the effects disappeared after age and sex were controlled for. On the other hand, overall laterality remained significant predictor of semantic memory even after age and sex were controlled for. Here, regression coefficients indicated
18 inconsistent participants had better results on semantic memory tests. Interaction terms between age and footedness, and overall laterality and sex were significant which proposes a moderative role of age and sex in the relationship between footedness and semantic memory, with stronger relationship among older adults, and overall laterality and semantic memory, with stronger relationship among inconsistently lateralized women compared to consistently lateralized women, something that is interesting for further exploration. This part of the study was more explorative in nature, since research in domain of semantic memory is very limited. Predictive value of variables of functional lateralization was statistically significant, but effect sizes and proportion of accounted variance in presented models are low which raises the questions of importance of such models in real-life situations and how much of that may be due to statistical artefacts. Previously, Lyle et al., (2008) have not found significant effects of inconsistency of lateral preference on tests which fall into domain of semantic memory.
When BDT was entered as a dependent variable, age was again significant predictor, respectively, with regression coefficients again indicating younger participants performed better. Even though handedness, footedness, and sex also significantly predicted results on BDT, the effects were not significant after controlling for age and sex. Age-related
deterioration is well documented for this test in the Betula study (Rönnlund & Nilsson, 2006b) and therefore such outcomes were expected. Although, only one study (Piper et al., 2011) aimed to explain effects of handedness on visuospatial functions, but with a different methodological approach, which makes this part of the study also more explorative in nature. Piper et al., (2011) showed left-handers were better in visuospatial functions, while here at least the direction of regression coefficients, although not significant, shows results are in direction of inconsistent group’s superiority.
Observed results show second research hypothesis is partially confirmed, since age moderated only the relationship between footedness and semantic memory, and sex moderated only the relationship of overall laterality and semantic memory. When
interpreted in context of hemispheric interaction theory presented in the introduction of this paper (Christman & Propper, 2001; Lyle, et al., 2008), results presented here poorly support this theory. If inconsistent participants indeed had better interhemispheric interaction, they would have had better results on episodic memory tests, which was not the case here. Also, in spite of limited effect sizes, inconsistent group’s superiority was noticed in case of
semantic memory, which is not proposed by the theory. Research on hemispheric interaction theory and functional lateralization is very limited and if future researchers want to address interaction between brain hemispheres and its relationship with functional lateralization, our suggestion is to follow designs by a group of Australian researchers (e.g. Cherbuin et al.,
19 2011; Luders et al., 2010) who are including structural and functional imaging methods in their studies. Possible explanation of such results may lie in the fact some previous studies (e.g. Lyle et al., 2008) have included only consistent and inconsistent right-handers in the analysis and those authors have been active in postulating the hemispheric interaction theory. The present study included right- and left-handers, based on a paper by Lyle et al., (2012), who propose handedness consistency, regardless of direction, has implications for memory. Also, it is possible results in this study are not as expected because IC and C groups were categorized differently. Although suggestions from Lyle et al., (2008, 2012) and
Propper et al., (2005) for a median as cut-off value between groups were followed, here median value in handedness context produced more rigorous categorization of IC and C participants. Another possible explanation lies in the fact materials used in the Betula study have not been used anywhere else and differences in results may reflect differences in measurement. In addition, studies presented here were in many cases experimental in nature, while a case in this study was linear modelling and correlational design.
Importance of studying relationship of memory and functional lateralization lies in Propper et al.’s (2005) suggestion that research on functional lateralization is helpful in re- formulation of some theories of memory, for instance theories on episodic and prospective memory. So far proposed theories rarely include brain commissures, such as corpus callosum, in their postulates. If measurement of handedness consistency and its relation with hemispheric interaction and communication is more represented in brain imaging studies on memory, we can expect formulation of new theories involving these brain structures and their functions. Also, research on inter-hemispheric interaction and
handedness could reveal some brain motor networks included in memory (Lyle et al., 2012).
Hemispheric interaction theory is based on some interesting evidence and has a potential to have wider practical implications in, for instance, potential treatment of patients with various memory impairments. Findings from the presents study are not in line with the hemispheric interaction theory, nor are the findings from a study by Luders et al., (2003).
Nevertheless, the findings from this study shed some new light on the hemispheric interaction theory and on the role of functional lateralization in cognitive performance.
Conclusion
Higher cognitive functions, such as memory, are included in almost all daily-life tasks and routines and it is important to study it in relation to, for instance, aging where studies have shown almost all forms of memory undergo some age-related changes (e.g. Lövden et al., 2004; Nyberg et al., 2012; Rönnlund et al., 2005). In recent years, research on both structural and functional lateralization and its relation to memory has received much
20 attention. A majority of these studies have shown that participants who are inconsistently lateralized perform better on tests of episodic memory, explained by a higher degree of interaction among brain hemispheres in so called hemispheric interaction theory (e.g.
Christman & Butler, 2011; Lyle et al., 2008; Lyle et al., 2012). This study was conducted to address to what extent is inconsistent and consistent functional lateralization, related to episodic memory, semantic memory and visuospatial functions, and to question to what extent are functional lateralization, variables of cognitive functioning and the relationship among them affected by age and sex. Results were not in line with expected outcomes.
Variables of functional lateralization emerged as significant predictors of episodic and semantic memory, and BDT, but after age and sex were controlled for they became
insignificant. Moreover, presented results were not in line with the hemispheric interaction theory. Nevertheless, some questions, such as interactions of variables of functional
lateralization, especially footedness, with age and sex, are of interest for future research and for more detailed assessment. Also, in order to further explore and develop the hemispheric interaction theory and with potential to reformulate theories of memory, future researchers should focus on imaging the hemispheric interaction and linking it to consistency of
functional lateralization.
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