Elsevier

Brain and Cognition

Volume 81, Issue 1, February 2013, Pages 52-56
Brain and Cognition

Bilateral saccadic eye movements and tactile stimulation, but not auditory stimulation, enhance memory retrieval

https://doi.org/10.1016/j.bandc.2012.10.003Get rights and content

Abstract

Recent research has shown superior memory retrieval when participants make a series of horizontal saccadic eye movements between the memory encoding phase and the retrieval phase compared to participants who do not move their eyes or move their eyes vertically. It has been hypothesized that the rapidly alternating activation of the two hemispheres that is associated with the series of left–right eye movements is critical in causing the enhanced retrieval. This hypothesis predicts a beneficial effect on retrieval of alternating left–right stimulation not only of the visuomotor system, but also of the somatosensory system, both of which have a strict contralateral organization. In contrast, this hypothesis does not predict an effect, or a weaker effect, on retrieval of alternating left–right stimulation of the auditory system, which has a much less lateralized organization. Consistent with these predictions, we replicated the horizontal saccade-induced retrieval enhancement (Experiment 1) and showed that a similar retrieval enhancement occurs after alternating left–right tactile stimulation (Experiment 2). Furthermore, retrieval was not enhanced after alternating left–right auditory stimulation compared to simultaneous bilateral auditory stimulation (Experiment 3). We discuss the possibility that alternating bilateral activation of the left and right hemispheres exerts its effects on memory by increasing the functional connectivity between the two hemispheres. We also discuss the findings in the context of clinical practice, in which bilateral eye movements (EMDR) and auditory stimulation are used in the treatment of post-traumatic stress disorder.

Highlights

► A 30-s series of alternating left–right saccades improves episodic memory retrieval. ► So does alternating left–right tactile but not auditory stimulation. ► The results suggest the effect is mediated by enhanced interhemispheric interaction.

Introduction

Previous research has revealed intrigu′ing relationships between saccadic eye movements and memory. First, rapid eye movements (REMs) during sleep, of which the majority are in the horizontal direction (Hansotia et al., 1990), are critical for memory consolidation (Poe, Walsh, & Bjorness, 2010). Second, during demanding memory retrieval, people tend to make more saccades than during simple retrieval (Ehrlichman, Micic, Sousa, & Zhu, 2007). Third, patients with post-traumatic stress disorder, which is characterized by prolonged and inappropriate recurrence of traumatic memories, can be treated with a therapy called eye-movement desensitization reprocessing (EMDR). This treatment involves having the patient think about his traumatic memories while simultaneously moving his eyes back and forth between left and right. In many patients, repetition of the procedure gradually changes the traumatic (sensory) memory into a more (verbal) declarative memory, while at the same time reducing emotional arousal and avoidance. Meta-analyses indicate that EMDR is equally effective as cognitive-behavioral therapy and superior to other therapies (Bisson et al., 2007, Bradley et al., 2005, Seidler and Wagner, 2006). Other studies have reported that horizontal eye movements performed during retrieval also decrease the vividness and distress of emotional autobiographical memories in healthy adults (e.g., van den Hout, Muris, Salemink, & Kindt, 2001). These three real-life phenomena suggest that horizontal saccades are important for efficient consolidation and retrieval of memories, and some researchers have speculated that the phenomena may be intimately related (Stickgold, 2002).

Here, we focus on a fourth phenomenon, dubbed saccade-induced retrieval enhancement (Lyle & Martin, 2010), that was discovered in a series of laboratory studies and that ultimately may cast light on the mechanisms underlying the real-life phenomena described above. In these studies (reviewed in Christman and Propper, 2010, Propper and Christman, 2008), cognitive psychologists found that a brief period of bilateral saccadic eye movements, prior to the retrieval phase of a memory experiment, improves memory retrieval in a wide array of tasks, including recall and recognition of words (Christman et al., 2003, Lyle et al., 2008, Parker et al., 2008, Samara et al., 2011), recall of early childhood memories (Christman, Propper, & Brown, 2006), recognition of details in a visual event narrative (Lyle and Jacobs, 2010, Parker et al., 2009), and recall and recognition of landmark shape and location information (Bruyné et al., 2009, Parker et al., 2008). In these studies, the critical eye-movement procedure was similar to that used in EMDR: participants watched a dot that alternately appeared on the left and right side of the screen, changing position twice per second. This procedure was compared with a control condition, in most studies consisting of vertical saccadic eye movements or a centrally presented dot changing color twice per second.

The goal of the current study was to examine if the beneficial effect on memory retrieval is specific for eye movements or generalizes to other types of bilateral stimulation. This question is partly motivated by clinical practice: Over the past decade, EMDR therapists have started to replace eye movements with other forms of alternating left–right sensory stimulation, in particular auditory or tactile stimuli (Shapiro, 1994, Shapiro, 2002). For example, a recent survey suggested that in around 50% of all EMDR sessions, eye movements have been replaced by binaural stimulation (van den Hout et al., 2011). Although there have been no large controlled studies of clinical efficacy, recent studies have found some evidence that these other forms of alternating left–right stimulation can reduce subjective distress in patients with post-traumatic stress disorder (Servan-Schreiber, Schooler, Dew, Carter, & Bartone, 2006) and reduce the vividness of negative memories in healthy volunteers (although this effect was inferior to that of eye movements; van den Hout et al., 2011).

The execution of lateral eye movements is associated with strong activation of parts of the hemisphere contralateral to the direction of the eye movement (Dean et al., 2004, Kastner et al., 2007)1, which reflects the contralateral organization of the visuomotor system. Ipsilateral activation occurs a bit later (due to the time needed for transcallosal transfer) but is much weaker in magnitude and far more localized. Therefore, a sequence of alternating left–right eye movements results in a pronounced (though not all-or-none) pattern of rapidly alternating activation of the two hemispheres. Christman and colleagues hypothesized that this alternating pattern of hemispheric activation causes the beneficial effect of alternating left–right eye movements on normal memory retrieval, possibly by stimulating the communication between the hemispheres (Christman et al., 2003, Propper and Christman, 2008). According to this hypothesis, alternating left–right tactile stimulation should also enhance memory retrieval, because of the strict contralateral organization of the somatosensory system (Kandel et al., 2000, Nieuwenhuys et al., 2007). Interestingly, Christman’s alternating hemispheric activation hypothesis predicts somewhat different results for alternating left–right auditory stimulation: Although studies consistently show a contralateral dominance of brain activations to monaural stimuli (King and Carlisle, 1995, Langers et al., 2005, Pantev et al., 1986), the contralateral dominance is not nearly as pronounced as in the visuomotor and somatosensory systems. This is because the ascending pathways of the mammalian auditory system project to both the ipsilateral and the contralateral auditory cortices, and hence monaural sound stimuli directly activate both hemispheres (Brodal, 1981). Thus, intermittent left–right auditory stimulation does not activate the two hemispheres in a strictly alternating fashion, and therefore Christman’s hypothesis predicts a smaller or absent effect on memory retrieval.

We conducted three experiments to test these predictions of the alternating hemispheric activation hypothesis. In Experiment 1, we replicated previous studies that examined the effect of bilateral eye movements on memory retrieval. In Experiment 2, we examined the effect of alternating left–right tactile stimulation compared to a control condition with intermittent simultaneous bilateral tactile stimulation. Finally, in Experiment 3, we compared the effects on memory retrieval of intermittent alternating versus simultaneous stimulation of the two ears. In all three experiments, half of the words to be encoded were emotionally aversive, the other half emotionally neutral. This allowed us to explore whether potential beneficial memory effects, usually obtained with neutral material, generalize to the emotional domain. Mixed-handed individuals were excluded from participation because the beneficial effect of eye movements sometimes does not occur in these individuals (Bruyné et al., 2009, Lyle et al., 2008).

Section snippets

Subjects

Fifty students at Leiden University (aged 18–26) participated for course credit or €4.50. All participants were native speakers of Dutch. Handedness was assessed using a modified version of the Edinburgh Handedness Inventory (Oldfield, 1971): Participants indicated the hand they prefer to use for each of 10 activities (e.g., writing, throwing) by choosing “always left” (−10), “usually left” (−5), “no preference (0), “usually right” (+5) or “always right” (+10). This results in scores ranging

Method Experiment 2: Tactile stimulation

Details of the method were the same as in Experiment 1, except as noted below.

Method Experiment 3: Auditory stimulation

Details of the method were the same as in Experiment 1, except as noted below.

Results Experiment 1: Eye movements

Table 2 presents the number of recalled items in the experimental and control conditions. An analysis of variance indicated that subjects recalled more emotional than neutral items, F(1, 48) = 23.0, p < .001, ηp2=.32: the typical emotional superiority effect on memory. More importantly, subjects in the experimental condition recalled more items than subjects in the control condition, F(1, 48) = 4.5, p = .039, ηp2=.09. The interaction between the two factors was not significant, F(1, 48) = 0.2, p = .66.

Results Experiment 2: Tactile stimulation

The results in Experiment 2 were similar to those in Experiment 1. As shown in Table 2, subjects recalled more emotional than neutral items, F(1, 51) = 31.2, p < .001, ηp2=.38. More importantly, subjects in the experimental condition recalled more items than subjects in the control condition, F(1, 51) = 4.2, p = .045, ηp2=.08. The interaction between the two factors was not significant, F(1, 51) = 0.3, p = .58. The two groups did not differ in the number of falsely recalled items, t(51) = 0.9, p = 0.37.

Results Experiment 3: Auditory stimulation

The results in Experiment 3 showed a different pattern than those in Experiments 1 and 2 (see Table 2). As in the previous experiments, subjects recalled more emotional than neutral items, F(1, 73) = 8.4, p = .005, ηp2=.10. However, in this experiment there was no difference between the two conditions in the number of correctly recalled items, F(1, 73) = 0.02, p = .88. The interaction between the two factors was nonsignificant, F(1, 77) = 0.02, p = .89, and the two groups did not differ in the number of

Discussion

The results can be summarized as follows. Experiment 1 replicated previous studies that showed a beneficial effect of horizontal eye movements on memory retrieval (Propper & Christman, 2008), and in particular on word recall (Lyle et al., 2008, Samara et al., 2011). Experiment 2 showed a similar beneficial effect on memory retrieval of alternating left–right tactile stimulation, indicating that the effect generalizes to at least one other modality. However, in Experiment 3, we found that the

Acknowledgments

This work was supported by VIDI Grants from the Netherlands Organization for Scientific Research (S.N., B.M.E. and H.A.S.)

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