Bilateral saccadic eye movements and tactile stimulation, but not auditory stimulation, enhance memory retrieval
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, : 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, . 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, . More importantly, subjects in the experimental condition recalled more items than subjects in the control condition, F(1, 51) = 4.2, p = .045, . 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, . 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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2021, European Journal of Trauma and DissociationCitation Excerpt :As a consequence, brain interaction between both hemispheres should be improved and higher brain areas responsible for cognitive reassessment should be activated. In studies comparing parameters of memory retrieval, bilateral-alternating stimulation worked better than bilateral-simultaneous and bilateral-continuous stimulation (Manfield, 2001; Nieuwenhuis et al., 2013; Servan-Schreiber, Schooler, Dew, Carter, & Bartone, 2006) and alternation from right to left was better than alternation from up to down (e.g. horizontal vs. vertical eye-movements; Christman, Garvey, Propper, & Phaneuf, 2003; Parker, Parkin, & Dagnall, 2013). Other authors, in contrast, observed comparable effects for vertical and horizontal eye-movements (Gunter & Bodner, 2008, experiment 2; Hornsveld et al., 2011).
Horizontal eye movements foster approach to negative pictures but do not change emotional valence: A dopaminergic regulation hypothesis
2021, New Ideas in PsychologyCitation Excerpt :EMDR mostly requires the client to perform large horizontal eye movements by following the back-and-forth motion of the therapist's hand, while visualizing their anxious memories. In the more cognitively oriented memory-research domain, Saccade-Induced Retrieval Enhancement (SIRE; Lyle & Martin, 2010) predominantly involves investigating explicit memory performance (e.g., free recall, recognition) for affectively neutral material as a function of eye movements (e.g., Brunyé, Mahoney, Augustyn, & Taylor, 2009; Christman, Garvey, Propper, & Phaneuf, 2003; Lyle & Edlin, 2015; Lyle, Hanaver-Torrez, Hackländer, & Edlin, 2012; Lyle, Logan, & Roediger, 2008; Matzke et al., 2015; Nieuwenhuis et al., 2013; Parker & Dagnall, 2007). Initial SIRE studies acknowledged the link between clinical therapy and cognitive memory research (Christman et al., 2003; Propper & Christman, 2008), but subsequently the domains bifurcated into distinct research specializations and theoretical accounts (also see Phaf, 2017).
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2020, Journal of Affective DisordersCitation Excerpt :Overall, they sustain that symptoms related to traumatic experiences are due to a fault in the processing of stressful memories by different areas of the brain involved in processing emotions, memories, self-perception, attention, REM (rapid eye movement) sleep phase (Rousseau et al., 2019). Bilateral stimulation occurring during EMDR sessions is thought to improve traumatic memories processing by changing functional brain connectivity (Nieuwenhuis et al., 2013), or by favoring physiological changes similar to those observed during the REM (Stickgold et al., 2002) or slow wave sleep (SWS; Pagani et al., 2017) phases; or by reducing the vividness of emotional stimuli by saturating the working memory (Gunter and Bodner, 2008). A recent study by Baek and colleagues in mice suggested that alternating bilateral sensory stimulation (ABS) provides a fear-reducing effect by suppressing the activity of fear-encoding cells and stabilizing inhibitory neurotransmission in a neural circuit including the superior colliculus, the amygdala, and the mediodorsal thalamus with the final effect of attenuating traumatic memories (Baek et al., 2019).