She has been a mentor in the truest sense of the word, and these few lines of ... Richard A. Abrams, Sandra Hale, Joel Myerson, Pascal Boyer, Ken Botnick and ...... and reject an aspect that is not part of that association (Johnson & Raye,.
WASHINGTON UNIVERSITY Department of Psychology Dissertation Examination Committee: Richard A. Abrams, Co-Chair Sandra S. Hale, Co-Chair Joel Myerson Pascal Boyer Kenneth Botnick David Carr EFFECTS OF BILATERAL EYE MOVEMENTS AND SHIFTS OF ATTENTION ON RECOGNITION MEMORY IN YOUNGER AND OLDER ADULTS by Carolyn Lisa Dufault
A dissertation presented to the Graduate School of Arts and Sciences Of Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy
December 2009 Saint Louis, Missouri
Acknowledgements I would like to offer a most sincere thanks to Martha Storandt for her teaching, support and guidance during work on this project and throughout my years of graduate school. She has been a mentor in the truest sense of the word, and these few lines of gratitude can’t reasonably convey the full extent of my appreciation for all she has done. I am also very grateful to the members of my dissertation committee including Richard A. Abrams, Sandra Hale, Joel Myerson, Pascal Boyer, Ken Botnick and David Carr for their time, energy and input on this work. A particular thanks to Richard Abrams for his kind encouragement to keep moving forward – it was more helpful than I can say. I also would like to thank David Balota and the NIA Training Grant for funding a portion of this dissertation. For his efforts running participants and helping with data coding, I thank my undergraduate assistant David Getreu. I thank Lily Beck for calling all of the older adults to organize their participation only two weeks after the birth of her third child. I am also grateful to Meg McClelland, Vicki Babbitt and the rest of the Psychology Department administrative staff for their help along the way. I also thank Keith Lyle for several helpful conversations during the course of this work. Though they will likely never read this, I would like to express my gratitude to the hundreds of participants, younger and older, who generously gave their time and energy to participate in these studies. The names of friends and family who helped and encouraged me are too numerous to list here (and could take up an additional dissertation-sized document with all the deserved thanks), though I hope they know who they are and that they are loved. ii
Finally, I offer a most heartfelt thank you to my husband Martin, who has been a constant source of encouragement and support, and to my little daughter Isobel, whose joy in discovering the world inspires me every day. This work is dedicated to my late father, Dr. Roland E. Dufault, a man of great kindness, wisdom and humor.
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Table of Contents Acknowledgements………………………………………………………………………..ii Table of Contents…………………………………………………………………………vi List of Tables…………………………………………………………………………....viii List of Figures……………………………………………………………………….……ix Abstract of the Dissertation……………………………………………………………….x CHAPTER 1………………………………………………………………………..…..…1 Introduction and Overview.……………………………………………….……....1 CHAPTER 2…………………………………………………………………….….….….4 Review of the Literature………..……………………………………….…...……4 Overview……………………………………………………….……..…. 4 The Relationship Between Eye Movements and Memory Enhancement...4 Overview…………………………………………….……..……. 4 Beneficial Effects……………………………..……..………..…..5 Limitations……………………………….………………...….....10 Theoretical Mechanisms………………………………………....13 The Relationship Between Eye Movements and Visual Attention………15 Overview……………………………………………………........15 Behavioral Evidence ……………………………….…...…….…16 Neuroimaging Evidence……………………………………….…18 False Memory……………………………………………………………20 Overview…………………………………………………...….…20 Pertinent Studies of False Memory………...….……………...….21 iv
Reduction of False Memory Effects………………….……….…23 Aging……………………….. ……………………………………..……24 Overview………….……………………………………………...24 Aging and the Visual System…...……………………………..…25 Age-Related Changes in Visual Attention …………...……...…..26 Age-Related Changes in False Memory ………………………...27 CHAPTER 3…………………………………………………………………….…….…28 Purpose, Design and Hypotheses…………………………………..………….…28 Purpose……………………………………………………………..….…28 Research Design……………………………………………………….…30 Research Questions...………….…………………………………………31 CHAPTER 4……………………………………...……..……………………….………33 Experiment 1……………………………………………………………..33 Method.……………………………..……………………………33 Participants………………………………...…….…….…33 Materials…………………………………...…….……....33 Pre-Test Activity…………………………………34 Verbal Recognition Task………………………...34 Handedness Survey………………………………36 Procedure……………………………...……...….………36 Results and Discussion………………………..…………………39 Hits………………………………….……………………41 False Alarms (critical)…………....................……………41 v
False Alarms (non-critical)………………..……..………43 Accuracy (d’) and Response Criteria (β)………………...44 Handedness………………………………………………46 Summary of Experiment 1……………………………………….46 CHAPTER 5…………………………….……..……………………….…….….48 Experiment 2……………………………………………………………..48 Method.……………………………..……………………………48 Participants………………………………...…….…….…48 Materials…………………………………...…….………49 Procedure……………………………...……...….………50 Results and Discussion………………………..…………………50 Hits………………………………….……………………52 False Alarms (critical)…………....................……………52 False Alarms (non-critical)………………..……..………53 Accuracy (d’) and Response Criteria (β)………………..53 Handedness………………………………………………53 Summary of Experiment 2……………………………………….54 CHAPTER 6……………………………………...……..……………………….………55 Experiment 3……………………………………………………………..55 Method.……………………………..……………………………55 Participants………………………………...…….…….…55 Materials…………………………………...…….………56 Procedure……………………………...……...….………56 vi
Results and Discussion………………………..…………………56 Hits………………………………….……………………59 False Alarms (critical)…………....................……………59 False Alarms (non-critical)………………..……..………60 Accuracy (d’) and Response Criteria (β)………………..61 Handedness………………………………………………62 Summary of Experiment 3……………………………………….62 CHAPTER 7……………………………………………………………………………..64 Discussion….…....…….…………………………………………………64 Research Questions………………………………………………66 Question 1……………...…………………………..…….66 Question 2……………...…………………………..…….69 Question 3……………………………………..…..……..70 Question 4……………...…………………..……..….…..71 Question 5………………...………………….…..…..…..72 Limitations……………………………………………………….75 Future Directions………………………………………………...76 Conclusions………………………………………………………79 References………………………………….…………………………….80 Appendix…………………………………………………………………91
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List of Tables Table 1.
Experiment 1: Mean Proportion of “Seen” Responses to Words Presented on a Test of Recognition Memory………………………………………40
Table 2.
Experiment 2: Mean Proportion of “Seen” Responses to Words Presented on a Test of Recognition Memory………………………………………51
Table 3.
Experiment 3: Mean Proportion of “Seen” Responses to Words Presented on a Test of Recognition Memory………………………………………58
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List of Figures Figure 1.
Effect of shift type on spatial memory span, adapted from Lawrence et al., 2004…………………………………………………….17
Figure 2.
Experiment 1: Proportion of hits as a function of pre-test activity and delay condition…………………………………………………………...41
Figure 3.
Experiment 1: Proportion of critical false alarms as a function of pre-test activity and delay condition…………………………………..………….42
Figure 4.
Experiment 1: Proportion of non-critical false alarms as a function of pretest activity and delay condition………………….…………..………….44
Figure 5.
Experiment 1: Criterion sensitivity as a function of pre-test activity and delay condition…………………………………………..…..……….….45
Figure 6.
Experiment 3: Proportion of critical false alarms as a function of pre-test activity and age group…….…………………………………..………….60
Figure 7.
Experiment 3: Proportion of non-critical false alarms as a function of pre-test activity and age group………………………………..………….61
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ABSTRACT OF THE DISSERTATION Effects of Bilateral Eye Movements and Shifts of Attention on Recognition Memory in Younger and Older Adults By Carolyn Lisa Dufault Doctor of Philosophy in Psychology Washington University in Saint Louis, 2009 Professor Richard A. Abrams, Co-Chairperson Associate Professor Sandra Hale, Co-Chairperson There is evidence that making 30 seconds of bilateral eye movements improves memory in young adults who are strongly right-handed. The proposed neural mechanism underlying this effect is an increase in interhemispheric communication. Given that attention and eye movements share many overlapping neural mechanisms, it is possible that bilateral shifts of covert visual attention may have similarly beneficial effects on memory. To test this idea, the present investigation compared performance on a verbal recognition task following either overt shifts of attention (eye movements) or covert shifts of attention in right-handed younger and older adults. Additionally, the effects of increasing the duration of the overt and covert shifts from the typical 30 seconds to 60 seconds was examined to investigate if doubling the shift time produced a greater memory benefit than that observed at 30 seconds. Finally, to provide a greater understanding of the time-course of the effects of bilateral attention shifts on recognition memory, two different delay conditions were directly compared – one with no delay between study and test, and the other with a 30 minute delay. x
Both overt and covert shifts of attention led to a reduction in false memories on the verbal recognition task for the younger adults in the no delay condition. There were no beneficial effects on memory for either shift type in the 30 minute delay condition. Also, unlike the beneficial effects observed in the younger adults, there were no memory benefits for either shift type in the older adult group, and instead there was evidence that overt shifts of attention were related to an increase in false memories for the latter group. These findings are consistent with theories that suggest common neural pathways for covert and overt visual attention and with those that posit an age-related breakdown in interhemispheric communication.
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Chapter 1: Introduction and Overview Over the past several years, there has been a growing market for interventions, in the form of books, movies and video games, that claim to improve memory and general cognitive ability through practice with simple techniques such as driving an unfamiliar route to work or brushing one’s teeth with the non-dominant hand or simply listening to Mozart’s music. These claims are often supported by varying degrees of scientific evidence, but it seems that people will try just about anything to improve their mental fitness. There may be another surprisingly simple and experimentally validated technique added to upcoming editions of these books: Moving one’s eyes back and forth for 30 seconds. A small but accumulating literature supports this claim (for a review see Parker, Relph & Dagnall, 2008). Christman, Garvey, Propper, & Phaneuf (2003) were the first to report that memory performance on a test of verbal recall was improved after participants made 30 seconds of side to side eye movements. Subsequent studies by these and other authors have replicated this unexpected effect. It is not well understood, however, why doing something as simple as making bilateral saccadic eye movements should lead to changes in memory performance. It is also not clear if the benefit is universal, as recent evidence suggests that individuals who are not strongly right-handed may actually experience memory impairment (Lyle, Logan, & Roediger, 2008) following bilateral eye movements. At present there are no published studies of the effects of these types of eye movements on memory in older adults. It would seem logical to study this segment of the population given the great interest in finding interventions that may help reverse or reduce negative age-related effects on memory. One goal of this dissertation was to 1
understand if older adults experienced the same eye-movement-enhanced memory benefits as those reported for younger adults. A second goal was to examine the conditions under which this memory benefit effect is observed. Existing research has demonstrated that effects often thought to be related to eye movements alone, can be explained in part by shifts of visual attention made in the absence of eye movements (Lawrence, Myerson, & Abrams, 2004). This dissertation investigated if covert shifts of attention (those made in the absence of eye movements) would produce similar memory benefits as those documented for eye movements. A third goal was to explore the effect of increasing the duration of eye movements made prior to memory testing. The existing research has only examined memory performance following 30 seconds of bilateral eye movements. Previous research in the area of verbal memory has demonstrated a duration effect, with task performance improving as a function of duration of exposure to the critical stimuli (e.g. Price, Wise, Watson, Patterson, Howard, & Frackowiak, 1994; Harpur, Scialfa, & Thomas, 1995). This dissertation examined if a longer duration of eye movements (60 seconds) would result in improved performance on a subsequent recognition memory test relative to performance following the standard 30 seconds of eye movements. A fourth goal was to examine the time-course of the effects of eye movements and attention shifts on recognition memory by comparing performance with and without a delay between the encoding and retrieval tasks. The beneficial effects of eye movements on memory have been observed after short or no delay conditions (Parker & Dagnall, 2007), as well as longer intervals of up to two weeks (Christman et al., 2003,
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experiment 2), however no study has directly compared different delay periods for the same task. This project sought to bridge this gap in the literature. The primary dependent of measure used in this dissertation was performance on a Deese-Roediger-McDermott (DRM) recognition memory task (Roediger and McDermott, 1995). These materials allowed for assessment of effects on both veridical (true) memory and false memory, and were chosen based on evidence that reduction of false memories may be more consistently observed following bilateral eye movements than are increases in veridical (true) recognition memory (Lyle et al., 2008). Taken together, answers to the questions posed by this work may provide valuable insight into the relationship between eye movements (overt shifts of attention) and covert shifts of attention and may also provide new information about the connections between attentional control and memory. Such insights may be useful in the quest to understand and describe the architecture of the neural mechanisms that support effective memory and attention performance across the life-span. Additionally, if it is shown that simply moving one’s eye back and forth for a few seconds improves memory, future editions of self-help books on this topic may want to add this technique to their list of quick and easy memory enhancers.
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Chapter 2: Review of the Literature Overview To provide a context for the proposed study and associated hypotheses, the following review of the literature is presented. The first section is a review of the small but growing literature on the effects of eye movements on memory enhancement. The second section reviews theories of visual attention with particular emphasis on the relationship between visual attention and eye movements. The third section covers theories of false memory with an emphasis on strategies and techniques known to reduce the occurrence of false memories. The final section describes age-related changes in vision, attention and memory.
The Relationship Between Eye Movements and Memory Enhancement
Overview During the past several years researchers have begun to examine the relationship between eye movements and memory based on the surprising finding that making 30 seconds of bilateral saccadic eye movements (voluntary side-to-side eye movements) improves memory. In some cases this improvement has come in the form of reduced false memories (Christman, Propper, & Dion, 2004, Experiment 2). Other studies have reported not only false memory reduction but also improved veridical memory (correct recall/recognition; Christman et al., 2003, Experiment 1; Parker & Dagnall, 2007). This beneficial effect of eye movements has been noted across different memory retention 4
intervals, ranging from just a few seconds up to a delay of two weeks (Christman et al., 2003, Experiment 2) and for studied material in both the verbal and spatial domains (Parker et al., 2008). Not all types of eye movements seem to produce a memory benefit. It has been shown that vertical eye movements, as well as all types of smooth pursuit eye movements, are no better than control conditions (Christman et al., 2003). It has also recently been noted that any beneficial effects of eye movements on memory may be limited to those persons who have strongly lateralized cerebral hemispheres (i.e., persons who are strongly right handed; Lyle et al., 2008). Explanations for the locus of this effect have ranged from the behavioral (source monitoring; Christman et al., 2004) to the physiological (increased interhemispheric interaction and a resulting beneficial increase in activation of areas of the brain associated with memory retrieval; Parker et al., 2008). Each of these explanations will be reviewed in the following section.
Beneficial Effects The idea that making simple bilateral eye movements could lead to changes in cognition and behavior has its origins in the clinical therapeutic intervention of Eye Movement Desensitization and Reprocessing (EMDR) in which clinicians claim to reduce their patients’ anxiety and unwanted thoughts after having them move their eyes back and forth for a brief duration (for an overview see Shapiro, 1995). Studies reporting the beneficial effects of EMDR are found throughout the clinical literature (e.g. Shapiro, 1989; see also Korn & Leeds, 2002), however this technique remains controversial (see 5
Davidson & Parker, 2001, for a meta-analysis that concludes EMDR does not work). Despite the controversy, researchers wondered if the types of eye movements used in EMDR might have beneficial effects on memory, similar to those reported for certain types of successful therapeutic interventions. Christman et al. (2003) examined the effects of bilateral eye movements on episodic memory. In the first of two experiments, participants studied a list of words, experienced a 30 minute retention interval, and were then assigned to one of five conditions: no eye movements, horizontal saccadic eye movements, smooth pursuit eye movements, vertical saccadic eye movements, or vertical smooth pursuit eye movements.1 For participants in the saccadic and smooth pursuit groups, eye movements consisted of following a small dot as it moved from one side of the screen to the other twice per second for 30 seconds. In the saccadic eye movement group the dot appeared sequentially on either the left and right side of the screen (horizontal condition) or the top and bottom parts of the screen (vertical condition), giving the appearance of an object bouncing between two locations; in the smooth pursuit condition the dot continuously traced a path between the two locations on the screen. Immediately following the 30 second eye movement condition, participants completed tests of either episodic (recognition) or implicit memory (fragment completion) .
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Typically, and for the purposes of their study, saccadic eye movements were defined as movements used to fixate stable targets, whereas smooth pursuit eye movements were defined as movements used to track moving targets (Christman et al., 2003; Rosano, Krisky, Welling et al., 2002).
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Relative to participants in all other eye movement conditions, those who made horizontal saccadic eye movements were better able to discriminate words that had previously been seen from those that were new on the recognition test. There were no differences between groups on the implicit memory task. Given the selective effects of horizontal saccadic eye movements, the authors suggested the observed memory benefit could not be attributed to a general oculomotor process but was due instead to some specific aspect of bilateral eye movements. The authors hypothesized that the locus of the beneficial eye movement effect was the production of interhemispheric interaction (IHI) and further speculated that the IHI led to enhanced functioning of areas of the right hemisphere known to underlie efficient episodic memory retrieval. Greater detail about this and other proposed mechanisms underlying this observed eye movement effect are discussed in the next chapter. Christman et al. (2003) also wondered whether this same pattern of memory enhancement would be observed in a more naturalistic task. In a second experiment, participants recorded autobiographical memories of their early childhood in journals. After a two week delay, participants were given a surprise memory test in which they were asked to recall details of the events they had recorded. Half of the participants made 30 seconds of bilateral eye movements prior to a recall test and the other half did not. Those who made eye movements had significantly better memory (resulting from better discriminability between new and old information and a more conservative response bias) than those in the control group. In a follow-up study, Christman et al. (2004) examined the effects of bilateral eye movements on false memory using a list learning task. The authors found that having 7
participants make 30 seconds of bilateral eye movements after reading lists of fifteen related words did not increase the number of hits on a recall task but did reduce the number of false alarms. Verfaellie, Rapcsak, Keane and Alexander (2004) reported a similar pattern of results in their study of persons with frontal lobe impairments. They found that participants with damage to their frontal lobes had impairments in source monitoring resulting in excessive false alarms, but not problems with accurate recall on a verbal associates task. Both Christman et al. (2004) and Verfaellie et al. (2004) suggest source monitoring deficits account for their observed pattern of results. The neuroanatomic underpinnings of source monitoring problems and their relationship to this type of memory illusion will be discussed in a later section on false memory. One of the more intriguing demonstrations of the power of eye movements on memory enhancement comes from a study in which Christman, Propper and Brown (2006) reported that people who made 30 seconds of bilateral eye movements prior to recalling early childhood memories were able to recall events from earlier time points compared with people who made no eye movements before recalling such events. These results suggest, and the authors conclude, that the beneficial effects of eye movements are related to the retrieval component of memory and not the encoding or storage process, as there is no reason to think the encoding aspects of these randomly assigned participants differed across groups. This study also demonstrates that an improved ability to retrieve information after making eye movements occurs even after a very long retention interval (several decades in this study). All studies reviewed thus far reported improvements in recall memory following bilateral eye movements. Parker and Dagnall (2007) applied the same bilateral eye 8
movement methodology to a recognition task and found similar benefits to memory. After studying a standard set of DRM word lists (Roediger & McDermott, 1995), participants were given a recognition test following a 30 minute delay and after either making eye movements (experimental group) or maintaining central fixation (control group) for 30 seconds. As seen in previous studies (e.g., Christman et al., 2003 and Christman et al., 2004), Parker & Dagnall (2007) found that bilateral eye movements improved recognition for presented words as well as reduced false memory for critical lures. The authors note that this set of findings lends only partial support to Christman et al.’s (2004) source monitoring explanation as the locus of this memory effect. Explanations involving monitoring posit expected reductions in false memory without corresponding improvements in veridical memory (Israel & Schacter, 1997). Parker & Dagnall (2007) however, found improvements in performance on both task types. Most recently Parker et al. (2008) examined the locus of these effects and found that improvements in memory following bilateral saccadic eye movements could be localized to the recollection component of memory. Using a remember-know task (after Gardiner, 1988), the authors found that participants in the eye movement condition were better able to discriminate new items from old items on a test of verbal memory; importantly, these respondents were more likely to indicate that they remembered previously seeing a word versus just knowing that they had seen it . A second association task also revealed the same pattern of responding, with participants in the eye movement condition (relative to those in the no eye movement condition) being more likely to recall associated word pairs (recollection memory) than the individual words (familiarity-based memory). Taken together, the authors cite these 9
findings as additional evidence for a source monitoring explanation of memory improvement following eye movements; they speculate that areas of the brain which control allocation of attention, for the purpose of discriminating new information from old, are activated in a useful way during the bilateral eye movements. In a second experiment Parker et al. (2008), examined eye movements and episodic memory using a pictorial task. Once again, participants in the bilateral eye movement condition had better contextual memory for color and spatial location information presented during an encoding phase, compared with those in the vertical or no eye movements conditions. This ability to better remember context is presented as evidence in support of improved recollection memory, as reported in Experiment 1 of Parker et al. (2008), given that contextual associations are typically thought of as relying on recollection and not familiarity based memory processes. Taken together there is a clear pattern of the beneficial effects of bilateral eye movements, made for brief durations, on subsequent retrieval of episodic memories. This benefit has been demonstrated at retention intervals of differing lengths and for a variety of stimulus types including words, autobiographical memories, color, and spatial location. The beneficial effects of eye movements, however, have not been uniformly observed and the known limitations of the extent of this phenomenon are reviewed in the following section.
Limitations As noted previously, Christman et al. (2003) studied horizontal and vertical saccades as well as horizontal and vertical smooth pursuit movements, and concluded 10
that among these possibilities, only bilateral saccadic eye movements improved subsequent retrieval of episodic memories. It has been shown that vertical eye movements, as well as smooth pursuit eye movements, are no different than control conditions in terms of producing subsequent effects on memory (Christman et al., 2003). This unique benefit of bilateral saccadic eye movements has been postulated to arise because of the interhemispheric interaction associated with such movements. Christman et al., (2004) have argued that increased interhemispheric interaction facilitates greater activation of right hemisphere, including structures known to be important for the successful retrieval of episodic memories (Christman & Propper, 2001, see also Cronin-Golomb, Gabrieli, & Keane, 1996). Evidence in support of this argument comes from studies with left handed and mixed handed individuals, as it has been documented that people in these groups have more naturally occurring interhemispheric interaction than do those who are strongly right handed (Christman et al., 2001). In a study of recall for words on an explicit memory task, Propper, Christman & Phaneuf (2005) found that mixed handed people had more hits (correct recall) and fewer false alarms than those people who were strongly right handed. They noted this effect was related to the strength of handedness and they obtained a significant negative correlation (r = -.285) between scores on the Edinburgh Handedness Inventory (EHI) and number of hits (correct recall). In other words, being more strongly right handed was related to lower scores on the recall test. Propper & Christman (2004) also investigated mixed versus right handed participant differences in a verbal remember/know task. They found that although the two groups did not differ in terms of overall recognition accuracy, those in the strongly right 11
handed group versus the mixed handed group were more likely to indicate that a response was known rather than remembered. This pattern of results suggests that those persons with a high degree of interhemispheric interaction were more likely to rely on recollection (a “remember’ response) versus familiarity (a “know” response). Recently, Lyle et al. (2008) investigated the effects of bilateral eye movements on verbal recall and recognition tasks for individuals who were either strongly right-handed (SR) or not strongly right-handed (nSR). They replicated earlier findings with SR individuals, finding this group to have improved recall and recognition of previously seen words and reduced false recall of unseen words. In contrast, following bilateral eye movements, those in the nSR group exhibited a significantly greater level of false recall (but not correct recall) than those in a no eye movement group. Similarly, nSR participants had no improvement in recognition but significantly higher level of false recognition. The authors explain these results in terms of a theory of interhemispheric interaction (IHI), and suggest that people who are strongly right handed may have underlying brain organization that benefits from increased interaction during episodic memory retrieval; those classified as nSR however, may be harmed by such increases in hemispheric interaction beyond an already naturally higher state of this type of brain activity (Lyle et al., 2008). Even among studies on groups of people who are all strongly right-handed, the beneficial effects of eye movement on memory have varied in terms of the degree of improvement and the aspect of memory that has been improved. Some researchers have found eye movements to both increase correct recognition and reduce false recall (Parker and Dagnall, 2007; Lyle et al., 2008, exp 2;), or to increase correct recall and decrease 12
false recall (Lyle et al., 2008, exp. 1); whereas others have found benefits primarily in the form of false memory reduction with a much smaller degree of improvement in correct recall/recognition (Christman et al., 2003; Parker et al., 2008). Given the small size of the accumulated literature on this subject, it is too early to say how much of the variation in these findings may be accounted for by task differences. One important final limitation that should be noted is Christman et al.’s (2003) finding that the benefits of bilateral saccadic eye movements were only observed in those tasks requiring episodic memory. When the authors had participants complete an implicit fragment completion task, they found that those who made horizontal eye movements performed no better than those who made vertical, pursuit or no eye movements. Taken together, this limited but fairly consistent body of literature suggests that bilateral saccadic eye movements made just prior to episodic memory retrieval enhance recall and recognition of remembered items, likely through an increased ability to discriminate new information from old. The theoretical mechanics of this effect are reviewed in the next section.
Theoretical Mechanisms In discussions about why bilateral eye movements enhance memory, increased interhemispheric interaction (IHI) during episodic memory retrieval has been the most frequently cited underlying mechanism (Christman et al., 2001; Christman et al., 2003; Lyle et al., 2008; Propper et al., 2005). Although no studies have demonstrated a direct link between IHI following eye movements with improved memory, many have speculated about the relationship based on several lines of converging evidence. 13
One finding cited by all researchers working in this area is Bakan & Svorad’s (1969) observation that following alternating left-right saccades, participants had corresponding increases in activation (as measured by EEG) in the contralateral hemispheres. Current researchers (Christman et al., 2001; Christman et al., 2003; Lyle et al., 2008; Propper et al., 2005) have pointed to Bakan & Svorad’s finding as evidence for the biological basis of IHI effect, though few have noted the problems associated with basing such important theoretical assumptions on this single, unreplicated study. Researchers in this area have also pointed to studies of split-brain patients (CroninGolomb, Gabrieli, & Keane, 1996; Zaidel, 1995) who have impaired performance on tests of explicit memory, but not implicit memory, following commissurotomy as evidence for the role of interhemispheric communication in successful explicit memory performance. If one accepts that bilateral eye movements increase IHI, the next consideration is to ask how such interaction improves episodic memory. There is strong support for the HERA (hemispheric encoding/retrieval asymmetry) model of memory (Habib, Nyberg and Tulving, 2003) which states that for most healthy adults, left prefrontal regions of the brain are primarily responsible for processes associated with episodic memory encoding and right prefrontal regions handle events involved in episodic memory retrieval. Christman et al. (2003) suggested that bilateral eye movements may increase activation in the right hemisphere with the greatest effect in regions thought to support retrieval of episodic memories previously encoded into memory by the left hemisphere. Parker et al. (2008) extended this line of reasoning based on their findings that bilateral eye movements led to improved recognition but not recollection memory. They 14
posited that successful recognition (and rejection of memories based on recollection) depends on intact production monitoring. Production monitoring theories of memory (also called “recall-to-reject” explanations) suggest that accurate memory retrieval depends on the ability to first call to mind the specific associated aspects of a memory in order to compare and reject an aspect that is not part of that association (Johnson & Raye, 2000). Failure to accurately recall a previous memory then leads to a breakdown in the ability to assess if a test item was part of an initially encoded set. Parker et al. (2008) suggest that one of the mechanisms through which bilateral eye movements exert their beneficial effects is by improving the access to previously encoded memories, allowing for more careful monitoring and eventual rejection of test items that were never presented. Further review of the role of source monitoring is reported in a later section of this chapter covering theories of false memory.
The Relationship Between Eye Movements and Visual Attention Overview The set of findings reviewed in the previous section suggests there is a reliable improvement in memory following 30 s of bilateral eye movements. It is possible however, that the covert shifts of attention which accompany overt eye movements may produce a similar memory benefit, given that the two systems underlying such shifts share common neural mechanisms (de Haan, Morgan, & Rorden, 2008). Evidence for such a link also comes from behavioral studies (Abrams & Dobkin, 1994; Lawrence et al., 2004; Rizzolatti, Riggio, Dascola, & Umiltà, 1987) as well as neuroanatomic studies (Corbetta et al., 1998; Hoffman & Subramaniam, 1995) that demonstrate overlapping 15
activity in the brain areas underlying both covert shifts of attention (those made in the absence of head or eye movements) and overt shifts of visual attention (eye movements). Given these converging findings, reviewed in detail below, it may be reasonable to hypothesize that bilateral covert shifts of attention will lead to a similar pattern of enhanced memory retrieval as that observed following bilateral eye movements.
Behavioral Evidence It has been established that attention aides visual processing by enhancing aspects of the visual scene relevant to action by the observer (Posner, 1980). Behavioral evidence demonstrates the benefits of a system where shifts of covert attention precede eye movements to an intended target, resulting in a fast and efficient processing of the target (Rizzolatti et al., 1987; Sheliga, Riggio, & Rizzolatti, 1994). Recent evidence from neuroimaging lends support to the idea that overt and covert shifts of visual attention arise from activation of a common frontal-parietal network (de Haan et al., 2008). This clear anatomical link between overt and covert attention shifts, often described as the premotor theory of attention (Rizzolatti et al., 1987), fits nicely with the results of behavioral studies conducted over the past two decades (Deubel & Schneider, 1996; Hoffman & Subramaniam, 1995; Kowler, Anderson, Dosher, & Blaser, 1995; Peterson, Kramer, Irwin, 2004; Rafal, Calabresi, Brennan, &Sciolto, 1989) that provide evidence for such a coupling. There is still not complete agreement that the premotor theory accounts for some observations in the visual attention literature (see Hunt and Kingstone, 2003 and Klein & Pontefract, 1994 for reviews of this argument). 16
In a study that directly compared the effects of eye movements and attention shifts alone, Lawrence et al. (2004) found that both behaviors produced significantly more interference with maintenance of information in spatial memory when compared to a control condition. Specifically, Lawrence et al. (2004, experiment 2) asked participants to recall a series of spatial locations, presented one at a time, with an interleaved secondary task that involved either shifting attention, making eye movements or maintaining fixation in a control condition. As shown in Figure 1, spatial spans (the maximum number of recalled spatial locations in an array) in the fixation condition were, significantly higher than those in the eye movement and attention conditions.
Figure 1. Effect of shift type on spatial memory span, from Lawrence et al., 2004.
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The importance of this finding for the current investigation is that both eye movements and attention shifts had effects on subsequent memory. It is possible that the effects of the different shift types were independent, but given the clear evidence of previously demonstrated overlap in neural activation and behavioral coupling (de Haan et al., 2008, Peterson, Kramer, & Irwin, 2004), it is possible that the eye movement effects could be accounted for by the inherently coupled shifts of attention. In the Lawrence et al. study there were larger effects of eye movements (in the form of greater memory interference) than shifts of attention, but this observation doesn’t necessarily undermine the possibility that the effects of the eye movements were the result of the indirect effects of the associated attention shifts; rather the component of the eye movement effect that was above and beyond that observed for shifts of attention may reflect the additional activation of the common frontal-parietal network known to accompany overt versus covert shifts of attention (Beauchamp, Petit, Ellmore, Ingeholm, & Haxby, 2001; de Haan et al., 2008).
Neuroimaging Evidence Using functional magnetic resonance imaging (fMRI), Corbetta et al. (1998) established that one network of brain regions activated during covert shifts of attention is nearly identical to areas activated during overt saccadic eye movements. Specifically, the authors identified a parietal-temporal network with primary involvement in the areas already known to play important roles in visual attention including the frontal eye fields (FEF) and the supplementary eye fields (SEF). Single unit recording studies in primates
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have previously identified these areas as being activated by both covert and overt orienting of visual attention (see Bruce & Goldberg, 1985; Schlag & Schlag-Rey, 1987). Recent work using transcranial magnetic stimulation (TMS) has elegantly demonstrated the role of the FEF in the coupling of visual attention and eye movements (Neggers, Huijbers, Vrijlandt, Vlaskamp, Schutter, & Kenemans, 2007). The authors used TMS to stimulate participant’s FEF after they received an attentional cue to a specific location, but 30 ms before they were able to make an eye movement to complete a visual discrimination task at that location. Normally, this type of discrimination would be enhanced when preceded by an informative attentional cue (Deubel & Schneider, 1996), however when TMS was applied to the FEF following an attentional cue Neggers et al. found a significant reduction in correct identifications at saccade target locations. The authors conclude that this result provides clear evidence for the link between covert shifts of attention and eye movements, with the FEF serving as the neural point of coupling between these two processes. Most recently, de Haan et al. (2008) added to the accumulated neuroscientific evidence of an attention shift and eye movement link with an fMRI study that addressed and corrected methodological problems in previous imaging studies (Corbetta et al., 2008; Nobre, Gitelman, Dias, & Mesulam, 2000). With task difficulty equated in a new way, de Haan et al. (2008) concluded that brain regions in a frontal-parietal network underlying both covert shifts of attention and overt eye movements are not only similar, but are in fact identical. The authors noted however, a difference in overall magnitude of activation in the network, with covert shifts of attention resulting in higher levels of
19
network activation than overt shifts, consistent with a similar finding by Beauchamp et al. (2001). Taken together, there is strong evidence that eye movements and shifts of visual attention share a common neural basis and that eye movements are accompanied by shifts of attention. If these two assertions are correct, then it is plausible to think that the mechanisms underlying the beneficial memory effects following eye movements (Christman et al. 2003; Parker and Dagnall, 2007) may also be observed following shifts of attention; this possibility was a primary topic of investigation in the current study. A determination that attention shifts alone have effects on memory would be informative by providing further evidence for the overlapping nature of the overt and covert orienting systems. Such a finding would also be of practical interest, as it would suggest a simple memory enhancement technique (moving ones eyes back and forth) is even simpler than originally thought.
False Memory Overview The benefits of 30 s of bilateral eye movements have been most consistently demonstrated in terms of benefits to the accurate recall of verbal information, with reductions in false memory being more widely reported than improvements in veridical recall (Christman et al., 2003; Parker et al., 2008). Given this demonstrated sensitivity to the positive effects of bilateral eye movements (and potentially for shifts of attention as well), a verbal recognition task with both a veridical and false memory component was chosen as the primary dependent measure for the following experiments. As such, a short 20
review of the pertinent literature on false memory, with an emphasis on the DRM paradigm (Roediger & McDermott, 1995) is presented in the next section. Basic theories behind the processes that lead to accurate and false remembering, as well as variables known to reduce false memories, are covered.
Pertinent Studies of False Memory In the past decade, there has been no single study on false memory that has been more influential than Roediger and McDermott (1995), from which the “DRM task” draws its name. This paper has been cited many hundreds of times and the DRM task has been applied across a huge variety of research programs, including with studies of interhemispheric interaction and eye movements, a set of findings reviewed earlier in this section. The basic DRM task involves presentation of lists of semantically related words that are all strong associates of a critical, but not presented, word. On subsequent tests of recall and/or recognition, these critical lures are reliably reported as having been seen, often at the same rate of veridical (true) recognition of previously presented words (Deese, 1959: Roediger and McDermott, 1995; Roediger, Watson, McDermott, & Gallo, 2001; for a comprehensive overview see Brainerd & Reyna, 2005). The current set of experiments used recognition memory (and not recall) on a DRM task as the primary dependent measure and thus it is important to review a few of the key findings related to this type of memory process. Roediger and McDermott (1995, Experiment 2) reported DRM task results in which true recognition was significantly higher, relative to control words (non-presented, non-lures), with a mean hit rate of .65 21
and false alarm rate of .11, respectively. In terms of false alarms to critical lures on the same task, the recognition rate was .72 and thus comparable to the hit rate for presented words. Importantly, participants in this experiment were also asked to give a “remember” or “know” judgment for each response, with “remember” responses indicating an ability to remember specific details at the time of encoding that particular word, whereas “know” responses were used to indicate a memory based more on feelings of familiarity with the word having been presented (see Yonelinas, 2002 for a review of this methodology). The authors found that participants were just as likely to indicate “remembering” the critical lures as they were for the presented words. These findings suggests that the false memories reported on this type of DRM task are perceived by the participants to have been just as real as words that were actually presented (Roediger and McDermott, 1995) Why such false memories are reliably produced from this type of DRM task remains a strongly debated issue (see Gallo, 2006, for a review), however there is a general consensus that associations play an important role. Some argue that hearing (or seeing) a given word activates a network of spreading activation whereby strong semantic associates of that word are also automatically activated, increasing the chances these associates will later be recalled as having been seen (Roediger, Balota, & Watson, 2001). Others argue that associations arise as result of feature overlap, pointing to findings like that of Koutstaal and Schacter (1997) who reported false memories in a DRM task using picture stimuli. Koutstaal and Schacter found similar false memory effects for pictures as those reported for standard words lists and suggested this as evidence for the encoding of memories as groups of perceptual features. In a comprehensive review of the literature, 22
Hutchinson (2003) concluded that there is evidence for the role of both spreading activation and feature overlap in explaining these memory process.
Reduction of False Memory Effects The occurrence of false memories in everyday life (Clancy, McNally, Schacter, Lenzenweger, & Pitman, 2002; Platt, Lacey, Iobst, & Finkelman, 1998) and those created in the laboratory (Gallo, 2006; Roediger & McDermott, 1995) have been well documented and, as described in the previous section, there seems to be some consenseus regarding their origin. What is less clear however, is how to reduce these types of typically unwanted memories. In laboratory settings there is evidence that warnings and practice reduce, though do not eliminate, false memories on standard DRM tasks (Gallo, Roberts, & Seamon, 1997). In a study demonstrating the strong persistence of false memories, McDermott and Roediger (1998) warned participants about the nature of false memories and gave them specific instructions to identify the critical lure in a standard DRM task. On a subsequent recognition task in which the first word was always the critical lure, it was still reported as having been seen 38% of the time. To the extent that warnings reduce false memories to some degree, Gallo, Roediger and McDermott (2001) demonstrated that the timing of such warnings matter. The authors presented three groups of participants with a standard set of DRM word lists. In one condition participants were given no warning about the nature of false memory production. In a second condition, participants were warned before studying the lists, and in the third condition participants received the warning after study but before the recognition test. The participants in the no-warning and post-study warning conditions 23
showed the typical pattern of false alarms to critical lures, whereas the group that received the earliest warning (the pre-study condition), showed a significant reduction in their false alarm rate. The authors suggest that participants in the pre-study condition were able to adopt a strategy of identifying the critical lure as the study lists were presented (Roediger and McDermott, 2001). This last example of successful reduction of false memories differs from the reported reductions that occur following 30 seconds of bilateral eye movements in that the beneficial effects observed with eye movements happen when the key manipulation occurs after the material had already been encoded in memory (post-study). Thus the mechanisms underlying false memory reduction following bilateral eye movements are likely to be quite different from those related to explicit warnings. Given this important difference, one goal of the current set of experiments was to further elucidate the timecourse of false memory reduction following bilateral eye movements and attention shifts.
Aging Overview The current set of studies included two experiments with younger adults and one with older adults (65-85 years of age). The existing literature on the beneficial effects of eye movements on memory has been limited to studies with young adults only. It is important to know if older adults exhibit similar memory benefits, either in the form of increased veridical memory or reduced false memory, as those observed in younger adults following bilateral eye movements. If older adults exhibit a similar benefit from eye movements or shifts of attention, this would distinguish this technique from other 24
forms of memory enhancement reported in the cognitive aging literature that typically require long periods of training (Ball et al., 2002) or special equipment (Basak, Boot, Voss, & Kramer, 2008). More importantly, such a finding might also prompt researchers to re-examine the idea that only people with strongly lateralized hemispheres derive a memory benefit following bilateral eye movements (Lyle et al., 2008), given known agerelated breakdowns in hemispheric asymmetry (Cabeza, 2002). Basic age-related changes in the visual system are reviewed in the following section, however it is unclear what effect (if any) these changes might have had on the eye movement and attention shift manipulations used in the current study. Pertinent studies of age-related changes in visual attention and false memory are also reviewed.
Aging and the Visual System Older adults experience a series of well documented age-related changes in sensory and perceptual aspects of the visual system and an enormous literature exists cataloging the specific nature of these changes (for a review see Fozard & Gordon-Salant (2001). Primary sensory changes with age include increased light scatter resulting from corneal changes, reduced visual acuity due to stiffening of the lens, changes in color vision and a decrease in contrast sensitivity (Michaels, 1993). Higher order visual systems are also affected with increasing age, and include impairments in motion perception (Scialfa, Guzy, Leibowitz, Garvey, & Tyrell, 1991), depth perception (Faubert & Overbury, 2000), and a decrease in the effective field of view (Habak & Faubert, 2001).
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Because there are no comparable studies with older adults, it is unclear what effects, if any, these general age-related changes will have on the eye movement and attention shift components of the proposed investigation. Even when diseases of the eye (e.g., macular degeneration, glaucoma, and cataracts), which disproportionately affect older adults, are removed from analyses of other studies, general effects of aging on the visual system still exist (Spear, 1993). In the current experiments, participants will be screened prior to participation, and only those known to be free from the aforementioned eye diseases will be included in these experiments.
Age-Related Changes in Visual Attention Previous research has found age-related declines in performance on some types of visual attention tasks including visual search (Veiel, Storandt, & Abrams, 2006), spatial localization of targets (Scialfa & Kline, 1988) and controlled inhibition of reflexive eye movements (Faust and Balota, 1997). Performance on other types of visual attention tasks, however, has been shown to be relatively age-invariant. For example, reflexive eye movements made to peripheral cues (exogenous orienting of attention) have been shown to be relatively unaffected by age (Greenwood, Parasuraman, & Haxby, 1993; Hartley, 1993). These task differences have been explained in terms of a sparing of early attentional systems found in posterior regions of the brain known to underlie aspects of attentional capture and a breakdown in anterior brain regions known to be involved in more controlled aspects of visual attention (Faust and Balota, 1997; Kramer, Hahn, Irwin, & Theeuwes, 1999). If this view is correct, the visual attention task proposed for use in
26
these experiments (bilateral shifts of attention to an exogenous cue) should yield equivalent effects for both younger and older adults.
Age-Related Changes in False Memory The primary outcome measure used in the current set of experiments was recognition memory performance on a DRM task. Gallo (2006) reviewed the results of 21 experiments that compared younger and older adults on DRM recognition memory tasks and found that although both groups had high rates of false recognition, there was evidence for small or no differences between the two groups in these rates. In the same experiments, rates of true recognition memory differed significantly, with older adults recognizing fewer words on average than younger adults (correct recognition rates were .73 and .77, respectively). Some studies have documented higher rates of false recognition in older adults than younger adults for standard DRM word lists (Tun, Wingfield, Rosen, & Blanchard, 1998) and false memory recognition tasks for pictures (Koutstaal & Schacter, 1997). Even with these exceptions, Gallo (2006) suggests that in general, tests of false recognition may not be as sensitive to age-related changes as are tests of false recall, where age-related impairments in memory are consistently demonstrated. This potential for greater task equivalence for the younger and older adults is important, because if there are beneficial effects of either eye movements or shifts of attention (or both), having a similar baseline on the primary dependent measure will allow for a more straightforward comparison of effects of the independent variable on both groups.
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Chapter 3: Purpose, Research Design, and Research Questions
Purpose Researchers are constantly searching for reliable ways to help people improve their memory. Christman et al. (2003) have reported a surprisingly simple technique that seems to accomplish this goal. They and others have demonstrated that making 30 s of bilateral eye movements reduces the occurrence of false memories and in some cases increases the ability to retrieve veridical memories. The neurological underpinnings of this phenomenon is not well understood, however the primary candidate mechanism is interhemispheric interaction (IHI). It has been suggested that for those individuals with strongly lateralized brain hemispheres (i.e., those who are strongly right-handed) bilateral eye movements activate areas of the brain important for accurate memory retrieval through IHI. There is evidence that not everyone benefits from these types of eye movements and in fact they may impair efficient retrieval in mixed and left-handed individuals (Lyle et al., 2008). At this time, no published studies have tested this effect with older adults. It would be important to know if this simple technique can be used to offset any of the observed age-related declines in memory. It is also not clear what the necessary conditions are to produce this effect. Research in the area of visual attention has found that effects thought to rely on eye movements alone may in fact be explained in large part by the accompanying shifts in visual attention (Lawrence et al., 2004). This dissertation includes a condition in each experiment that compares attention shifts with eye movements and a control condition to 28
see if similar effects are observed. If it is found that shifts of attention produce a similar benefit in terms of reduction of false memories and/or an increase in veridical memories, it may compel investigators to reconsider the mechanisms through which eye movements produce beneficial effects on memory. Similarly, the issue of bilateral eye movement duration has not been studied at all. Existing research has only examined these effects after participants made 30 seconds of eye movements. This work will be the first to ask if there is an increase in the observed memory benefit when there is a corresponding increase in the duration of eye movements made just prior to memory retrieval. There is reason to believe that such a relationship could exist, given the well-documented occurrence of a “dose-effect” elsewhere in the cognitive literature (see Price, Wise, Watson, Patterson, Howard, & Frackowiak, 1994; see also Harpur, Scialfa, & Thomas, 1995). In other words, if making 30 s of eye movements is good for memory, is making 60 s of such movements even better? The present investigation has four primary goals. The first is to determine if bilateral attention shifts made just prior to memory retrieval have similar memory benefits as those observed for bilateral eye movements. The second goal is to study the relationship between duration of eye movements/attention shifts and degree of memory improvement. The third goal is to examine if older adults experience a similar memory benefit following eye movements/shifts of attention as has been documented in younger adults. The fourth and final goal is to examine the time-course of any observed benefit by testing memory performance across different study-test delay periods.
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Research Design The first experiment addressed the question of whether there was a similar memory benefit following shifts of attention as has been reported for eye movements in terms of reducing false memories and/or improving veridical memory. This experiment also examined the effect of delay (none or 30 minutes) on memory enhancement following the different types of pre-test activity (eye movements, shifts of attention, and control fixation). Six groups of strongly right-handed young adults (ages18 to 23 years) with normal or corrected to normal vision participated in Experiment 1. All participants completed a verbal recognition memory task and were randomly assigned to one of two delay conditions. One group had a 30 minute delay between study and test, while the other group had no delay. All participants were then randomly assigned to complete one of three types of pre-test activity; eye movements, attention shifts or control fixation. For all groups, the pre-test activity lasted for 30 seconds. Immediately following the pre-test activity, participants were given a brief test of recognition for the previously studied words. The second experiment examined the effect of increasing the duration of the pretest activity from 30 seconds to 60 seconds. This experiment also examined the effect of delay (none or 30 minutes) on recognition memory improvement following the pre-test activity. Experiment 2 was almost identical to Experiment 1 and included six new groups of young adults. In this experiment all participants experienced a 60 second delay condition (with three equal groups in each of the pre-test activity groups). Once again, 30
half of all participants experienced a 30 minute delay period and the other half had no delay between study and test. When taken together with the results of the Experiment 1, the results from Experiment 2 will be used to examine the effects of pre-test duration on recognition memory. In the third and final experiment of this dissertation, older adults and a new group of younger adults were given the same DRM memory task used with the younger adults in Experiments 1 and 2, designed to measure correct recognition of previously presented words (veridical memory) and incorrect recognition of words that were not previously presented (false memory). Based on the results from Experiments 1 and 2, the duration of the pre-test activity was set at 30 seconds and there was no delay between the study and test phases.
Research Questions The purpose of this set of experiments was to determine if younger and older adults benefited from making overt and covert bilateral shifts of attention, and to examine the conditions under which such benefits appear. To reach these goals, the following five questions were addressed: (1) Are there beneficial effects of bilateral eye movements and bilateral (covert) shifts of attention on recognition memory? If yes, are these effects equivalent? (2) If there are beneficial effects on memory, does the duration of bilateral eye movements and attention shifts matter? (3) Do the beneficial effects of eye movements and/or attention shifts depend on the length of delay between study and test? (4) If there are beneficial effects, how do bilateral eye movements and attention shifts improve recognition memory? (5) Do bilateral eye movements and shifts of attention 31
produce equal benefits in younger and older adults? Guided by theories that posit an increase in IHI following bilateral eye movements and those that suggest structural and functional overlap in the systems that control overt and covert shifts of visual attention, it was hypothesized that conditions under which beneficial effects of eye movements are observed, will also be the conditions under which beneficial effects of covert shifts of attention are observed.
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Chapter 4: Experiment 1 This experiment investigated group differences in recognition memory performance following exposure to one of three types of pre-test activity, each lasting 30 seconds – eye movements, attention shifts, or maintenance of central fixation. The effect of delay between study and test (none or 30 minutes) was also examined. Method
Participants A total of 180 right-handed young adults (107 females) were recruited from the undergraduate subject pool in the Department of Psychology at Washington University. Ages ranged from 18 to 23 years (M = 19.54, SD = 1.07) and all participants had normal or corrected to normal vision. Three participants, one each in the eye movement, attention shift and control fixation conditions, were excluded from the data analyses based on false alarm rates greater than 3.0 SD above the mean. All participants were right-handed, as determined by self-report and the Edinburgh Handedness Inventory (Oldfield, 1971). Consent procedures were followed according to the standards outlined by the Washington University Human Research Protection Office. Individuals received one half course credit for each half hour of participation.
Materials Stimuli for the pre-test activity and the verbal recognition task were presented on an Apple iMac G5 computer with a 17 inch display and built-in iSight Camera, using PsyScope X Build 51 software (Cohen, MacWhinney, Flatt, & Provost, 1993). 33
Pre-Test Activity. All participants experienced one of three pre-test activities: they either 1.) made side-to-side eye movements by following a dot flashing in the periphery, 2.) looked straight ahead while a dot flashed side-to-side in the periphery or 3.) looked straight ahead while a dot flashed on and off in the center of the screen (the control condition). The first condition was designed to replicate the type of beneficial eye movements stimuli used in previous studies (Christman et al., 2003; Parker & Dagnall, 2007). The second condition was used to examine the idea that if a similar pattern of memory enhancement is observed following side-to-side shifts of covert attention, then it is possible that the beneficial effects of bilateral eye movements may not require eye movements at all. The eye movement and attention shift stimuli consisted of a black dot (approximately 4º of visual angle) that appeared on a white background. The dot flashed for 500 msec duration, alternating sides on the right and left sides of the display (across approximately 27º of visual angle) over a 30 second period. A small black plus sign remained in the center of the screen at all times. For the control condition (which required maintenance of central fixation), a small black plus sign (identical to the one described for the conditions above) was displayed in the center of the computer monitor and alternated its appearance every 500 msec with a small black circle (approximately 4º of visual angle), also presented centrally, for a total of 30 seconds.
Verbal Recognition Task. Similar to the methods employed by Parker and Dagnall (2007) in a study which found beneficial effects of eye movements on 34
recognition memory, the present study employed 20 of the 24 word lists developed by Roediger and McDermott (1995) for a task now commonly referred to as the DeeseRoediger-McDermott (DRM) procedure. In this paradigm, participants are exposed to lists of semantically related words during a study session and when tested later, consistently report having seen related but non-presented words from each list (Roediger & McDermott, 1995). For example, participants studied the words “table, sit, legs, seat, couch, desk, recliner, sofa, wood, cushion, swivel, stool, sitting, rocking and bench”. On a subsequent recognition test, participants often report having seen the critical, but nonpresented word “chair”. This finding of reliable verbal false memory production has been replicated numerous times and demonstrated in tests of recall (Watson, Bunting, Poole, & Conway, 2005), recognition (Gallo, Roediger, & McDermott, 2001) and even under conditions when participants are explicitly warned against such false memories (Gallo, Roberts, and Seamon, 1997). In the current experiment there was a study phase consisting of 10 DRM word lists composed of 15 related words each (see Appendix for complete lists). The study phase was followed by a 90 word test phase. The test list included 40 words from the study phase, taken from serial positions 1, 5, 10, and 15 of each list – a direct replication of Parker and Dagnall’s (1997) methods. The test list also included 40 non-studied words, taken from the same serial positions of 10 additional non-presented DRM word lists. Importantly, the test list included 10 “critical lures” which were the strong semantic associates of the 10 thematically related and previously studied word lists.
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Handedness Survey. In order to assess handedness, participants completed the Edinburgh Handedness Inventory (Oldfield, 1971). In this brief survey, participants gave a self-reported rating of their level of handedness for the following ten everyday activities; writing, drawing, throwing, using scissors, using a toothbrush, using a spoon, using a knife, using a broom (upperhand), striking a match and opening a box. Following Lyle et al.’s (2008) methods, participants circled ratings for each item on a twenty point scale, ranging from “Always Left” (-10) to “Always Right” (+10) with “No Preference” represented at the midpoint (0). Measured in this way, scores on this scale could range from -100 (strongly left handed) to +100 (strongly right handed).
Procedure Testing time for most participants in Experiment 1 was either one half hour or one hour (depending on random assignment to delay condition). Participants were tested at individual computer stations (with dividers between each station) in groups of up to 12 per session. They were seated approximately 22 inches from the computer monitor and asked to face the center of the display. Participants were told that the built-in iSight camera (located in the top center of the display) would capture a digital video throughout the experiment in order to monitor compliance with the task instructions. They were shown the recording in progress as the explanation was given. There were four phases during the computer portion of experiment and participants encountered them in the following order – study, delay, pre-test activity and test. Immediately following the experiment, participants completed a paper and pencil
36
version of the Edinburgh Handedness Inventory and filled out a short demographic survey. The instructions for the study phase asked participants to “Please study the following words by saying them softly to yourself, as you may see them again at the end of this experiment”. During this phase, 10 DRM word lists of 15 words each were presented. Individual words appeared in black letters on a white background in the center of the screen for two seconds each. A blank white screen appeared between word lists for three seconds. The order of words within each list was the same for all participants, however list order was randomized. After all 150 study words were presented (about 6 minutes), participants were assigned to one of two delay groups; no delay (immediate condition) or a 30 minute delay (delay condition). Following the study phase, participants in the immediate condition completed 30 seconds of a pre-test activity (described below) and then immediately moved on to the test phase of the experiment; participants in the delay condition went to a nearby waiting room for one half hour before completing the pre-test activity and test phase. Participants in the delay condition were not given instructions about what to do during the delay (other than to stay in the building), and most participants chose made phone calls or completed schoolwork. After the 30 minute delay, participants returned to their computer stations, completed 30 seconds of a pre-test activity (described below) and then completed the test phase of the experiment. All participants were randomly assigned to one of three pre-test activity conditions – eye movements, attention shifts or control fixation. Individuals assigned to the eye movement condition were instructed to follow the dot with their eyes, while 37
keeping their head steady, as it moved back and forth across the display. Participants in attention shift condition were instructed to maintain fixation on the plus sign at the center of the screen, while participants in the control fixation condition were instructed to maintain central fixation as the small plus sign and dot alternated appearing (flashed) every 500 msec in the center of the display. Compliance with these directions was monitored through the use of video recorded through the computer’s built-in camera. A review of the videos revealed that all participants complied with the pre-test activity instructions. Immediately after the 30 s pre-test activity, all participants completed a recognition test. The test phase began with a set of onscreen instructions asking participants to decide if individual words were among those in the previously studied lists. If a word was recognized as having been previously seen, participants were instructed to press the “s” key (for seen); if a word had not been seen, they were instructed to press the “u” key (for unseen). Responding was self-paced. The test phase word list consisted of 90 words, including 40 that were previously seen, 40 that were unseen and 10 unseen critical lures. The order of presentation of words in the test list was randomized for each participant. The dependent variables for this study included correct recognition of previously presented words (hits), false alarms to non-presented critical lures, and false alarms to unrelated non-presented words. The signal detection measure d’ was calculated in two ways. The first was d’ true (verbatim memory) and the second was d’ false (gist-based memory). Higher d’ true scores indicated greater recognition accuracy and took into account both correct hits and correct rejections of non-presented words (false alarms). Following the method described 38
by Parker & Dagnall (2007) and Koutstaal & Schacter (1997), d’ false was used as a measure of gist-based responding, with “seen” responses to unseen critical lures considered hits, and “seen” responses to unrelated, non-presented words considered false alarms. Higher d’ false scores indicated a greater reliance on gist-based memory, based on a high proportion of “seen” responses to unseen but related critical lures relative to the proportion of “seen” responses to non-presented, unrelated words2. The criterion measure β was calculated to assess response bias for both verbatim (β true) memory and gist-based (β false) memory. Higher values of β correspond to a more conservative response criteria (saying that a test item was “seen” on the study list). Because the distributions of β were positively skewed, they were log transformed for all analyses.
Results and Discussion For all analyses, alpha was set at .05. For all measures, group means were analyzed in 2 (delay: none or 30 minutes) X 3 (pre-test activity: control, eye movements or attention shifts) between-subjects ANOVAs. Table 1 provides a summary of the means and SDs for each measure, across all conditions.
2
For participants with a false alarm rate of 0, a standard correction to a .05 alarm rate was used when calculating d’ values.
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Table 1 Mean (SD) proportion of hits, false alarms, accuracy (d') and response bias (log β) as a function of pre-test activity and delay condition following 30 seconds of pre-test activity.
Pre-Test Activity Eye
Attention
Central
Movements
Shifts
Fixation
Measure No Delay Hits
0.75
(0.13)
0.77
(0.10)
0.74
(0.15)
FA critical
0.58a (0.19)
0.64b (0.23)
0.75a,b (0.22)
FA non-critical
0.15
(0.10)
0.16
(0.12)
0.19
(0.12)
d' true
1.90
(0.57)
1.90
(0.62)
1.72
(0.42)
log β true
0.45
(0.74)
0.36
(0.86)
0.20
(0.90)
d' false
1.41a (0.70)
1.56
(0.76)
1.70a (0.64)
log β false
0.62 a (0.70)
0.47b (0.80)
0.10a,b (0.90)
30 Minute Delay Hits
0.71
(0.17)
0.68
(0.16)
0.70
(0.17)
FA critical
0.60
(0.23)
0.65
(0.21)
0.67
(0.20)
FA non-critical
0.17
(0.11)
0.19
(0.14)
0.22
(0.14)
d' true
1.63
(0.75)
1.49
(0.64)
1.50
(0.71)
log β true
0.30
(0.63)
0.40
(0.68)
0.26
(0.64)
d' false
1.27
(0.72)
1.48
(0.64)
1.43
(0.81)
log β false
0.36
(0.72)
0.35
(0.72)
0.23
(0.71)
Note. Means in a row sharing subscripts are significantly different (p < .05). 40
Hits Hits were defined as the proportion of words correctly identified as previously seen on the original 150 word study list. There was a main effect of delay on correct recognition, F(1, 171) = 5.67, p < .05, ηp2 = .03, with more hits in the no delay condition (M = .75, SD = .13) than the 30 minute delay condition (M = .70, SD = .16). Unlike the beneficial effects of eye movements on correct recognition reported by Parker and Dagnall (2007), there was no effect of pre-test activity on hits, (F < 1) in this study. As seen in Figure 2, there was no interaction between delay and pre-test activity (F < 1).
Figure 2. Proportion of hits as a function of pre-test activity and delay group.
False Alarms (critical) Critical false alarms were defined as non-presented words that were strong semantic associates of words presented during the study phase that were falsely
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recognized as “seen”. As shown in Figure 3, there was a main effect of pre-test activity on false recognition, F(2, 171) = 4.62, p < .05, ηp2 = .05.
Figure 3. Proportion of critical false alarms as a function of pre-test activity and delay group.
Planned comparisons revealed that for participants in the no delay group, eye movements (M = .58, SD = .22) significantly reduced critical false alarms compared to the control condition (M = .75, SD = .22), t(58) = 3.13, p < .01. Importantly, shifts of attention (M = .63, SD = .23) also reduced critical false alarms relative to the control group, t(57) = 1.93, p < .05, and were no different from eye movements, t (57) = -0.10, ns. The finding that making eye movements just before a memory task reduces false memories replicates previous research on recognition (Lyle et al., 2008; Parker & Dagnall, 2007) and recall (Christman et al., 2003, Christman et al, 2004. Christman et al., 42
2006). The current finding extends the nature of these beneficial effects on memory to include covert shifts of attention. There were no significant effects of pre-test activity in the delay condition (F < 1), a somewhat surprising result given reports of the benefits of 30 seconds of bilateral eye movements following delays of 30 minutes (Parker & Dagnall, 2007), 2 weeks (Christman et al., 2003) and even decades (Christman et al., 2006). An inspection of the mean false alarm rate in the present study reveals numerically fewer false alarms in both the eye movement (M = .60) and attention shift (M = .65) conditions, compared to the control condition (M = .67) following a 30 minute delay, however planned comparisons revealed no significant differences between means. False Alarms (non-critical) Non-critical false alarms were defined as unrelated, non-presented words that were reported as “seen” during the study phase. Group means for the proportion of noncritical false alarms were analyzed in the same 2 (delay) X 3 (pre-test activity) ANOVA described for correct recognition. There were no main effects of delay, F(1, 171) = 2.73, p = .10. ηp2 = .02, or pre-test activity, F(2, 171) = 2.01, p < .14. ηp2 = .02, however both effects approached conventional significance. Figure 4 shows that the means for these conditions are in the expected directions, with numerically fewer non-critical false alarms in the eye movement and attention shift groups than the control group, and more false alarms following the 30 minute delay compared to no delay. There was no interaction between delay and pre-test activity for non-critical false alarms (F < 1).
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Figure 4. Proportion of non-critical false alarms as a function of pre-test activity and delay group.
Accuracy (d’) and Response Criteria (β) The signal detection measure d’ true was used to examine accuracy (the ability to discriminate old items from new). There was a main effect of delay on d’ true, with greater accuracy in the no delay (M = 1.84 , SD = .54) than the 30 minute delay condition (M = 1.54, SD = .70), F(1, 165) = 9.67, p < .01, ηp2 = .06. There was no main effect of pre-test activity on d’ true (unlike Christman et al., 2003:Parker & Dagnall, 2007; and Parker, Relph, & Dagnall, 2008), and no interaction between delay and pre-test activity (Fs
