Right Hemisphere Memory Bias Does Not Extend to Involuntary Memories for Negative Scenes

Abstract

Attention is unequally distributed across the visual field. Due to greater right than left hemisphere activation for visuospatial attention, people attend slightly more to the left than the right side. As a result, people voluntarily remember visual stimuli better when it first appears in the left than the right visual field. But does this effect—termed a right hemisphere memory bias—also enhance involuntary memory? We manipulated the presentation location of 100 highly negative images (chosen to increase the likelihood that participants would experience any involuntary memories) in three conditions: predominantly leftward (right hemisphere bias), predominantly rightward (left hemisphere bias), or equally in both visual fields (bilateral). We measured subsequent involuntary memories immediately and for 3 days after encoding. Contrary to predictions, biased hemispheric processing did not affect short- or long-term involuntary memory frequency or duration. Future research should measure hemispheric differences at retrieval, rather than just encoding.

Keywords

Attention emotion hemispheric processing memory

Hemispheric asymmetries—relative differences in activation and function resulting from specialisations in the right and left hemispheres (Ocklenburg et al., 2016)—affect people’s behaviour. Pseudoneglect is one example: Neurotypical people pay slightly more attention to the left than the right side of space (Jewell & McCourt, 2000). Higher memory accuracy for visual stimuli presented in the left versus the right visual field—a right hemisphere (RH) memory bias—suggests pseudoneglect also affects memory (e.g., Dickinson & Intraub, 2009). Here, we examined whether people show a RH memory bias when involuntarily recalling visual stimuli; in this case, highly negative images.

People show a RH memory bias for simple visual stimuli including shapes (Della Sala et al., 2010; Sheremata & Shomstein, 2014) and numbers (Petrini et al., 2009). Della Sala et al. (2010) presented coloured shapes in four quadrants and found participants were more likely to make errors for shapes presented on the right (5,264 errors) than the left (356 errors) side. Replicated online and in-lab, these results suggest people have better memory for shapes presented on the left. This bias also exists for complex stimuli, including object (Kensinger & Choi, 2009; Laeng et al., 2007) and naturalistic (Dickinson & Intraub, 2009; Moeck et al., 2020) images. Dickinson and Intraub (2009) presented scenes, wherein an object was located on the left and right side of each scene, across the visual field for 500 ms. In a surprise recognition memory test, participants displayed 5% higher memory accuracy for left than right side objects.

Together, these findings are consistent, but limited to voluntary memory; participants had to intentionally retrieve the encoded stimuli (e.g., to decide if they had seen an image before, Dickinson & Intraub, 2009). Hemispheric differences in involuntary memory—which come to mind spontaneously without preceding retrieval attempt (e.g., Berntsen, 2010)—have not been investigated. There are two primary reasons to suggest the RH memory bias for voluntary might extend to involuntary memory. First, voluntary and involuntary memories share basic encoding and maintenance mechanisms (Berntsen, 2010); both are enhanced when encoding occurred recently (e.g., Staugaard & Berntsen, 2014) and with emotionally intense stimuli (e.g., N. M. Hall & Berntsen, 2008) that tell a story (Niziurski & Berntsen, 2019). Second, although there is increased activation in the dorsolateral prefrontal cortex during strategic (i.e., voluntary) compared to incidental (i.e., involuntary) retrieval (Kompus et al., 2011), once the retrieval process is initiated a similar neural network underlies both memory types (Habib & Nyberg, 2008; S. A. Hall et al., 2014). This neural network involves the visual cortex and medial temporal, ventral occipitotemporal, and ventral parietal regions (Habib & Nyberg, 2008; S. A. Hall et al., 2014). On the basis of voluntary and involuntary memories sharing encoding and maintenance mechanisms and, once initiated, a similar neural network, we propose that if initially processing visual stimuli with the RH enhances voluntary recall, it should also enhance involuntary recall. It is important to test this idea, because involuntary and voluntary memories occur similarly often (e.g., Rubin & Berntsen, 2009).

To determine whether people show a RH memory bias for involuntary recall, we manipulated hemispheric activation during encoding using a divided visual field paradigm. We used a large set of negative images to increase the likelihood that participants would experience involuntary memories; people typically remember emotional more vividly than neutral stimuli (Todd et al., 2012). We manipulated which visual field the majority of images appeared in three between-subject conditions: (a) leftward bias (predominantly RH processing), (b) rightward bias (predominantly left hemisphere [LH] processing), and (c) no bias (bilateral processing). We measured the frequency and duration of short-term (immediately after encoding) and the frequency of long-term (for 3 days) involuntary memories. Our primary prediction matched voluntary memory research: Participants in the leftward bias condition would report more short- and long-term involuntary memories compared to participants in the rightward and no bias conditions. Given several studies have investigated hemispheric differences in voluntary memory and found a relatively consistent RH memory bias across a range of stimuli and paradigms, we exclusively focused on involuntary memory in the current study.

A subsidiary aim was to determine whether rapidly presenting negative images is a viable trauma analogue. Although using highly negative images as a trauma analogue is well-supported, prior studies have used presentation times of 1000–6000 ms (Bryant et al., 2013; N. M. Hall & Berntsen, 2008; Krans et al., 2013, 2016; Oulton et al., 2016; Pearson et al., 2012). Thus, whether shorter presentation times (i.e., less than 1,000 ms, here: 250 ms) elicit similar rates and quality (i.e., vivid, distressing) of involuntary memories has not been explored.

Method

Participants

We calculated sample size with Precision for Planning software (Cumming, 2012). When this experiment was collected, this software was unable to estimate sample size for more than two independent groups. Therefore, we generalised the minimum sample size per group (n = 44) from two independent groups (target margin of error = .5, level of confidence = 95, level of assurance = 99) to three (n = 50; N = 150). This generalisation was suitable because planned comparisons were for two groups.

We recruited 170 participants from Flinders University and the community but removed and replaced 20: 3 for not completing the diary and 17 for technical issues.¹ The final sample (N = 150, 69% female, 31% male) were aged 18 to 53 years (M = 23.57, SD = 6.84). Participants had normal or corrected-to-normal vision and were strongly right-handed (M = 9.77, SD = 0.67 on the Flinders Handedness Survey [FLANDERS] (Nicholls et al., 2013), where +10 indicates completely right-handed). We recruited right handers to increase the likelihood that participants would have greater activation in RH than LH regions for visuospatial attention (e.g., Zago et al., 2017). Some studies suggest pseudoneglect—a behavioral index of greater RH than LH activation for visuospatial attention where people attend more to the left than the right side of pre-bisected lines—decreases with age (e.g., Learmonth et al., 2017). While younger adults (e.g., 19–39 years) show robust pseudoneglect, older adults (i.e., aged 60–80) do not (Schmitz & Peigneux, 2011). Therefore, it is possible that the older adults in our sample may not have shown greater RH than LH activation for visuospatial attention. But given only 10% of our sample was aged between 30 and 53 years, and no participants were over 60 years, it seems unlikely that many of our participants did not show greater RH than LH activation for visuospatial attention. The Flinders University Social and Behavioural Research Ethics Committee approved this experiment. Deidentified data and Supplemental Material are available.

Materials

Images

We selected 100 International Affective Picture System images (P. J. Lang et al., 2008), rated 1.31–2.45 on valence (1 = most negative; M = 1.95, SD = .004) and 4.00–7.29 on arousal (9 = most arousing; M = 6.19, SD = .02). We created 5 sets of 20 images (sets matched within 0.012 on valence, 0.045 on arousal) with an even content-distribution (human face, human nonface, animals, inanimate objects) across sets, because content can influence affect ratings (Colden et al., 2008). There were original and mirror-reversed versions of each image, to rule out left–right idiosyncracies (Dickinson & Intraub, 2009). The IAPS images are listed in the Supplemental Material.

We manipulated how many images appeared in each visual field, between-subjects. For participants in the leftward and rightward bias conditions, we presented four sets in the biased (80 images) and one set in the opposite (20 images) visual field. We used an 80:20 ratio, rather than placing all images in the biased visual field, to prevent habituation to presentation location. Image set order and which set appeared in the opposite visual field was counterbalanced, with five versions per condition. For participants in the no bias condition, images appeared equally in the left and right visual fields (50:50 ratio). We created two sets of 50—matched on valence, arousal and category—counterbalanced five times.

Positive Affect Negative Affect Schedule

We used the Positive Affect Negative Affect Schedule (PANAS; Watson et al., 1988) to index emotional intensity during encoding. Participants rated (1 = very slightly or not at all, 5 = extremely) how 10 positive (e.g., excited) and 10 negative (e.g., scared) words reflected their current mood before and after image exposure. Internal consistency was high for the positive affect (α = .90) and negative affect (α = .98) subscales.

Involuntary Memory Measures

We used a 5-min thought-monitoring phase (Oulton et al., 2016) to measure short-term involuntary memory frequency and duration. Participants thought about anything they liked and responded when an involuntary thought or image about the photos came to mind. They pressed and held the spacebar until it passed. We chose this frequency-based thought-monitoring phase, rather than one where participants describe each involuntary memory as it arises, to keep the monitoring phase length consistent across participants, prevent task switching between monitoring and describing, and stop participants avoiding pressing the key due to the effort required to describe each memory. After the 5-min monitoring phase, participants described the most frequently experienced image and rated how often they found themselves thinking about the images (1 = almost never, 5 = very frequently), distress associated with the memories (1 = not at all distressing, 5 = extremely distressing), how vivid the memories were (1 = not at all vivid, 5 = extremely vivid), and how hard they tried to push the memories out of their mind (suppression: 1 = not at all, 5 = completely).

Participants recorded long-term involuntary memories in a 3-day paper diary. They provided a brief description, the time/place the memory occurred, and whether it was a thought, image, or thought/image.

Procedure

After providing informed consent, participants completed the FLANDERS and the PANAS. They then rated current depression, anxiety, and stress symptoms, and self-reported how often they experience involuntary thoughts about different topics (e.g., finance) in everyday life (see Supplemental Material). Next, participants encoded the images: Each image appeared for 250 ms, 5 times, with 1,250 ms encoding time per image. To maximise contralateral processing and avoid changes in visual angle (Bourne, 2006), we used a chin rest 500 mm from the screen. Participants were instructed to look at a fixation cross² while the images (14.93° × 11.19°) appeared in their left and right visual fields (2.3° from the fixation cross, 1.7° from the screen’s edge). Participants then did another PANAS, followed by the thought-monitoring phase and memory ratings. Paper diary instructions concluded the 20-min session.

The diary phase began after participants left the lab. A text message reminded participants to log their entries online at 18:00 each day, to increase compliance and ensure we did not lose data from unreturned paper diaries. If participants forgot to record involuntary memories as they occurred, they only reflected on 1 day, reducing retrospective reporting biases. After three days, participants returned their diary, received payment ($20AUD) or course credit, and were debriefed.

Results and Discussion

We first determined whether rapidly presenting negative images elicited sufficient involuntary memories to test our primary prediction. On average participants reported 9.96 (SD = 9.47) involuntary memories in the 5-min thought-monitoring phase,³ each lasting approximately 2.16 s (SD = 3.27). Participants who experienced short-term involuntary memories (N = 131) rated these memories as relatively vivid (M = 2.84, SD = 1.09), moderately distressing (M = 2.57, SD = 1.19), and tried hard to push these memories out of their mind (suppression: M = 3.58, SD = 1.22). These ratings were similar to Oulton et al. (2016) mean vividness (3.14), distress (2.80), and suppression (3.27) ratings with 2,500 ms image presentation time. Involuntary memories also occurred after participants left the lab (diary phase: M = 2.46, SD = 2.40). Most diary involuntary memories contained imagery (image only: 37%, thought and image: 36%, thought only: 27%). Therefore, rapidly presenting negative images elicited high-quality involuntary memories, sufficient to test our primary prediction.

These data allow us to address the subsidiary aim of investigating rapid presentation as a viable trauma analogue. We compared our short-term involuntary memory rate—9.95 over 5-min or 1.99 per minute—to two other studies that have assessed involuntary memories for negative images using a monitoring phase (Krans et al., 2016; Oulton et al., 2016). With the same 5-min monitoring phase, Oulton et al. (2016) reported just 1.82 involuntary memories (averaged across conditions). A one-sample t-test against 1.82 confirmed our rate was significantly higher than Oulton et al., t(143) = 10.31, p < . 001. With a 2-min monitoring phase, Krans et al. (2016) reported 2.45 involuntary memories per minute. A one-sample t-test on participants per minute involuntary memory rate, against 2.45, showed Krans et al. rate was significantly higher than ours, t(143) = –2.90, p = .004. However, Krans et al. preceded the monitoring phase with a task (presenting blurred versions of some encoded images) designed to provoke thoughts about the images. Given we did not include any provocation task, the similarity in ours and Krans et al. involuntary memory rate suggests our paradigm elicited a high number of involuntary memories.

Our short-term involuntary memory rate was also comparable to trauma film studies. For example, the average involuntary memory rate from four studies that all used a 5-min thought-monitoring phase to measure involuntary memories for a highly negative sexual assault film segment (from Irreversible) is 7.83; calculated from the control condition of three studies (Kubota et al., 2015; Nixon et al., 2007, 2009) and collapsed across all participants from one study (Wilksch & Nixon, 2010). A one-sample t-test against 7.83 revealed this average was lower than our 5-min involuntary memory rate, t(143) = 2.70, p = .008. Our long-term involuntary memory frequency (2.46 over 3 days) was also similar to prior research, relative to diary length (N. M. Hall & Berntsen, 2008: 2.18 over 5 days; Oulton et al., 2016: 3.50 over 7 days), suggesting this paradigm boosts short-term involuntary memory frequency without sacrificing long-term involuntary memory frequency. Therefore, rapidly presenting negative images is a viable trauma analogue that could be used alone or—to further increase involuntary memory frequency—alongside a provocation task (as used by Krans et al., 2016). Our rapid image presentation paradigm makes a useful addition to trauma analogue research, which is often limited by low involuntary memory frequency (James et al., 2016). Eliciting high involuntary memory frequency with images makes this paradigm particularly appealing; images are easier to manipulate and offer greater content variation than trauma films (Pearson et al., 2012).

Having established that our paradigm elicited sufficient involuntary memories, we next investigated whether biased hemispheric processing at encoding affected involuntary memory frequency and duration. To test evidence for the null hypothesis, we report Bayes factors (BF₁₀) obtained in JASP (JASP Team, 2020) with default Cauchy prior (Rouder et al., 2009). We interpret BF₁₀ according to Wetzels et al.’s (2011) ranges. We used a one-way analysis of variance (ANOVA) to compare involuntary memory frequency in the leftward, rightward, and no bias conditions. Contrary to expectations, we found no significant difference in involuntary memory frequency by presentation bias, F(2, 141) = .67, p = .52, ŋ² = .009 (Table 1). A Bayesian ANOVA indicated substantial support for the null hypothesis (BF₁₀ = 0.12), suggesting participants in all three conditions experienced similar involuntary memory frequency. Presentation bias also did not influence participants ratings of how often they found themselves thinking about the images, F(2, 128) = 1.06, p = .35, ŋ² = .02, with substantial support for the null hypothesis (BF₁₀ = 0.20). There were no significant differences in average (F(2, 129) = .69, p = .50, ŋ² = .01) or cumulative (i.e., total time over the monitoring phase; F(2, 129) = .97, p = .38, ŋ² = .01) involuntary memory duration.⁴ For both average (BF₁₀ = 0.12) and cumulative (BF₁₀ = 0.17) duration, we found substantial support for the null hypothesis. These findings suggest predominantly RH processing does not enhance the frequency and duration of short-term involuntary memories for highly negative images.

Table 1.

Frequency and Duration of Immediate Involuntary Memories.

Presentation bias condition	Involuntary memory frequency	Average duration (s)	Cumulative duration (s)
Leftward (RH)	8.69 (8.65)	2.48 (3.26)	31.15 (60.30)
Rightward (LH)	10.78 (9.51)	2.32 (3.40)	22.94 (43.00)
None	10.39 (10.29)	1.70 (3.15)	16.74 (38.96)

We next determined whether a RH memory bias affects long-term involuntary memories by comparing involuntary memory frequency by condition during the diary phase. We ran a 3 (day: 1, 2, 3) by 3 (condition: leftward, rightward, none) repeated-measures ANOVA (Figure 1). Presentation bias did not affect long-term involuntary memory frequency, F(2, 146) = 1.29, p = .28, ŋ_p ² = .02, with substantial evidence for the null hypothesis (BF₁₀ = 0.13). In all conditions, involuntary memories decreased at a similar rate, shown by a main effect of time (F(2, 146) = 45.88, p < .001, ŋ_p ² = .32, BF₁₀ > 30) and no interaction between time and presentation bias (F(4, 294) = 2.29, p = .06, ŋ_p ² = .03, BF₁₀ = 0.11). Thus, consistent with the short-term data, biased hemispheric processing did not affect long-term involuntary memory frequency.

Figure 1.

Involuntary memory frequency (95% CIs) per diary day by presentation bias condition.

We found no evidence that a RH memory bias extends to involuntary memory. At first glance, this finding could reflect that voluntary and involuntary memories do not share encoding and maintenance factors in relation to the effect of pseudoneglect on memory. To test this idea, we examined whether our findings can be attributed to factors at encoding affecting voluntary and involuntary memory differently. If so, then an encoding factor known to increase both voluntary and involuntary memory frequency (e.g., N. M. Hall & Berntsen, 2008)—such as emotional intensity—should not be associated with short- and long-term involuntary memories. We operationalised emotional intensity experienced during encoding as change in positive and negative affect (measured by the PANAS) from pre–post image exposure. Change in negative affect correlated positively with short- and long-term involuntary memory frequency and all characteristics ratings (Table 2). Accordingly, change in positive affect negatively correlated with long-term involuntary memory frequency and most characteristic ratings. The correlations were less consistent for positive than negative affect, likely because negative affect items assess feelings elicited by highly negative and arousing images (i.e., subjective distress/displeasure) more than positive affect items (i.e., sadness/lethargy; Watson et al., 1988). Taken together, emotional intensity during encoding was associated with the increased occurrence and severity of involuntary memories in our sample, replicating prior research (N. M. Hall & Berntsen, 2008; Niziurski & Berntsen, 2019). Thus, it is unlikely that our lack of RH memory bias reflects factors at encoding affecting voluntary and involuntary memory differently. Indeed, alternative explanations for why manipulating hemispheric processing during encoding did not lead to any differences in involuntary memories, despite robustly affecting voluntary memory, are also possible.

Table 2.
Correlations [95% CI] Between Emotional Intensity and Involuntary Memory Frequency and Characteristics.

Change in negative affect Change in positive affect

Thought-monitoring task

Involuntary memory frequency .26* [.11, .40] –.08 [–.24, .08]

Self-rated frequency .33* [.17, .47] –.19* [–.34, –.02]

Vividness .31* [.15, .46] –.17 [–.33, .00]

Distress .57* [.45, .68] –.20* [–.36, –.04]

Suppression .32*** [.16, .46] –.19* [–.34, –.02]

Diary phase

Involuntary memory frequency .35*** [.20, .49] –.20* [–.35, –.04]

Vividness .21* [.03, .37] –.18* [–.35, –.002]

Distress .51* [.37, .63] –.24 [–.39, –.06]

Suppression .33* [.17, .48] –.24 [–.40, –.07]

Note. p < . 001. p < . 01. p < . 05.

One explanation is that we focused on encoding, not retrieval. Data from Laeng et al. (2007) suggest the RH voluntary memory bias is driven by processing differences at retrieval. In Laeng et al. participants encoded images centrally or from the right or left visual field. At test, the images encoded from each visual field were presented centrally and vice versa. Although participants showed better memory for images presented in the left than the right visual field overall, this effect was driven by greater sensitivity for the images presented in the left visual field at test, not encoding (Laeng et al., 2007). Future research should investigate hemispheric differences at retrieval by cueing involuntary memories with blurred versions of the encoded images (Krans et al., 2013) in a divided visual field paradigm, or pairing the images with sounds that are then played to the left and right ear at retrieval (e.g., Staugaard & Berntsen, 2014). This type of cueing study overcomes a limitation of our thought-monitoring phase; asking participants to monitor their thoughts encourages a deliberate process that counters the spontaneity of involuntary memories (Niziurski & Berntsen, 2019).

A second explanation for why we did not find a RH memory bias for involuntary memory is because hemispheric differences in dorsolateral prefrontal cortex activity exist for voluntary, but not involuntary, retrieval. The dorsolateral prefrontal cortex is involved in the initial strategic search stage of voluntary memory (Kompus et al., 2011), with the left dorsolateral prefrontal cortex being primarily activated during this process (Habib & Nyberg, 2008; S. A. Hall et al., 2014). However, there is no strategic search for involuntary recall, removing the opportunity to observe hemispheric differences at this retrieval stage. Future research should test this possibility by measuring subsequent voluntary (and involuntary) memory following biased hemispheric processing of visual stimuli. This type of study would also allow us to confirm that our paradigm elicits a right hemisphere memory bias for voluntary memory, rather than relying solely on evidence from prior research that this bias exists.

This experiment has limitations. We required a between-subjects design because we measured immediate involuntary memories with a frequency-based thought-monitoring task suited to a large set of highly negative images. But this task meant we could not determine whether the involuntarily remembered images were originally encoded from the right or the left visual field. It also prevented us from using a within-subjects design that might have been more sensitive to detecting visual field differences. An alternative thought-monitoring task is to ask participants to describe each involuntary memory as it comes to mind (e.g., Oulton & Takarangi, 2018). By coding these descriptions to specific images, we could establish which visual field the remembered image originally appeared. One drawback is that this task requires a smaller set of nonconceptually overlapping images, to ensure matching between descriptions and images (e.g., Chapman et al., 2013). Nonetheless, future research should use this task to investigate whether these findings are consistent when image presentation is manipulated within-subjects. Another limitation is that we relied on recruiting strong right-handers to increase the likelihood that participants had greater RH than LH activation for visuospatial attention. However, recent evidence suggests eye-dominance may be a better predictor than handedness of hemispheric biases in visuospatial attention (Schintu et al., 2020). Future research should recruit participants who show both right-eye dominance and right-handedness, to test whether differences in eye dominance within our sample explains the lack of right hemisphere involuntary memory bias. Finally, due to resource limitations, we relied on eye-tracking data from a prior experiment with longer presentation times to infer that participants can centrally fixate, when instructed (Moeck et al., 2020). However, by not eye-tracking our participants, we are unable to confirm they were continually fixating on the central cross during image presentation.

Conclusion

We sought to determine whether a RH memory bias extends from voluntary to involuntary memory, by biasing hemispheric processing of negative images. Our findings suggest it does not: Counter to expectations, short and long-term involuntary memory frequency did not differ between participants who initially processed the majority of images with the RH, the LH, or bilaterally. In addition, we show a promising new lab paradigm for inducing high rates of involuntary memories for negative images.

	Change in negative affect	Change in positive affect
Thought-monitoring task
Involuntary memory frequency	.26*** [.11, .40]	–.08 [–.24, .08]
Self-rated frequency	.33*** [.17, .47]	–.19* [–.34, –.02]
Vividness	.31*** [.15, .46]	–.17 [–.33, .00]
Distress	.57*** [.45, .68]	–.20* [–.36, –.04]
Suppression	.32*** [.16, .46]	–.19* [–.34, –.02]
Diary phase
Involuntary memory frequency	.35*** [.20, .49]	–.20* [–.35, –.04]
Vividness	.21* [.03, .37]	–.18* [–.35, –.002]
Distress	.51*** [.37, .63]	–.24** [–.39, –.06]
Suppression	.33*** [.17, .48]	–.24** [–.40, –.07]

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Ella K. Moeck

Supplemental Material

Supplemental material for this article is available at

Notes

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