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. Author manuscript; available in PMC: 2018 Jan 22.
Published in final edited form as: Exp Aging Res. 2015;41(3):259–271. doi: 10.1080/0361073X.2015.1021644

Negative Arousal Increases the Effects of Stimulus Salience in Older Adults

Matthew R Sutherland 1, Mara Mather 1
PMCID: PMC5777218  NIHMSID: NIHMS934344  PMID: 25978446

Abstract

Background/Study Context

Stimuli compete for mental representation, with salient stimuli attracting more attention than less salient stimuli. In a recent study, we found that presenting an emotionally negative arousing sound before briefly showing an array of letters with different levels of salience increased the reporting of the more salient letters but decreased reporting of the less salient letters (Sutherland & Mather, 2012). In the current study we examined whether negative arousal produces similar effects on attention in older adults.

Methods

Data from 55 older adults (61–80 years; M = 70.7; SD = 5.1) were compared with those from 110 younger adults (18–29 years; M = 20.3; SD = 2.3) from Sutherland and Mather (2012). Neutral or negative arousing sound clips were played before a brief presentation of eight letters, three of which were presented in a darker font than the others to create a group of high and low salience targets. Next, participants recalled as many of the letters as they could. At the end of the study, participants rated the emotional arousal and the valence of the sounds.

Results

Higher ratings of emotional arousal for the sounds predicted a greater advantage for high salience letters in recall. This influence of arousal did not significantly differ by age.

Conclusion

The effects of negative arousal on subsequent attention were similar in older adults as in younger adults. Moreover, the results support arousal-biased competition theory (Mather & Sutherland, 2011), which predicts that emotional arousal amplifies the effects of stimulus salience in attention and memory.

Keywords: emotional arousal, salience, short-term memory, aging

Introduction

Certain objects attract attention because they possess features that sharply contrast with the features of other objects, giving the impression that they “pop out” and capture attention (Fecteau & Munoz, 2006; Itti & Koch, 2000). For example, orange traffic cones strongly contrast with the grayish-black asphalt roads on which they are placed, producing a salient contrast for drivers to easily detect. In the brain, representations of different objects in a scene compete for attention (Desimone & Duncan, 1995). The winner is the object with highest perceptual contrast. This is why an orange traffic cone placed on the side of the road is more noticeable than a black trash bag.

A number of studies suggest that the effects of visual salience decline in older age. For instance, the ability to detect perceptual contrasts (Bennet, Sekuler, & Sekuler, 2007; Flaubert, 2002; Habak & Faubert, 2000) and the targets in visual search tasks (Madden, 2007) declines. Moreover, physiological responses to emotional stimuli also diminish with age (Gavazzeni, Wiens, & Fischer, 2008; Levenson, Carstensen, Friesen, & Ekman, 1991), suggesting that the impact of emotion on attention in older adults may also decline. Nevertheless, there is evidence that emotionally arousing stimuli continue to attract increased attention in older adults. For example, both older and younger adults are quicker at detecting a target hidden among distracters if the target is emotionally arousing (Hahn, Carlson, Singer, & Gronlund, 2006; Leclerc & Kensinger, 2008; Mather & Knight, 2006), suggesting that objects resembling motivationally relevant stimuli, like frowning faces and slithering snakes, attract attention and produce effects similar to visual salience. Attention biases towards emotion-eliciting stimuli have been attributed to emotional salience (Todd, Cunninghan, Anderson, & Thompson, 2012), which can dominate attention even in the presence of perceptually salient distracters (Niu, Todd, & Anderson, 2012).

Exposure to an emotional stimulus also has influences on attention that persist in its absence. Once an emotional stimulus is presented, it changes the way subsequently presented neutral objects compete for attention. For example, the ability to detect a solitary neutral stimulus can be enhanced by presenting an emotionally arousing stimulus just beforehand (Bocanegra & Zeelenberg, 2009; Padmala & Pessoa, 2008; Zeelenberg & Bocanegra, 2010), at least if the stimulus has low spatial frequency (Lee, Baek, Lu, & Mather, in press). Moreover, the presentation of an emotional stimulus has also been shown to enhance the ability to identify a neutral target within an array of neutral distracters (Becker, 2009; Olatunji, Ciesielski, Armstrong, & Zald, 2011; Phelps, Ling, & Carrasco, 2006). However, arousal only enhances learning about visual search targets when they are salient “pop-out” targets and not when the targets are very similar to the distracters (Lee, Itti, & Mather, 2012). Thus when attention is biased to a neutral stimulus, emotional arousal can increase this bias. It is well documented that emotionally arousing objects themselves dominate attention, but we have argued that this arousal response continues to influence attention by strengthening preexisting attention biases (Sutherland & Mather, 2012). This means that arousal further amplifies processing of whatever stimulus attracts the most attention—an effect we describe as arousal-biased competition (ABC; Mather & Sutherland, 2011).

Our goal was to examine whether ABC effects are present in older adults. The ability to perceive visual contrasts (Bennet, et al., 2007; Flaubert, 2002; Habak & Faubert, 2000) and to pick out a target among distracters (Madden, 2007) is known to decline with age. Thus one potential prediction was that ABC effects would not be observed in older adults, particularly when attention is biased by visual salience. Declines in the ability to detect perceptual contrasts should weaken biases in attention caused by visual salience, thus interfering with arousal-induced changes that strengthen attention biases. Therefore, according to this interference hypothesis, attention biases driven by perceptual contrasts will not increase due to prior exposure to an emotionally arousing stimulus.

On the other hand, there is also evidence suggesting that ABC effects should be observed in older adults, despite age-related declines in perception and selective attention. For example, like younger adults, older adults continue to show attention biases towards emotionally arousing stimuli (Hahn, et al., 2006; Leclerc & Kensinger, 2008; Mather & Knight, 2006), which suggests that the effects of emotional salience remain stable in later age. Moreover, although older adults tend to be more susceptible than younger adults to distraction from irrelevant neutral stimuli (Guerreiro, Murphy, & Van Gerven, 2010), several studies show that they can be even less distracted than younger adults by negative irrelevant stimuli (Ebner & Johnson, 2010; Thomas & Hasher, 2006; for a review see Mather, 2012), meaning the ability to inhibit attention to emotional stimuli remains relatively stable and perhaps increases in older age. Thus despite declines in visual perception and selective attention, there is evidence showing that interactions between emotion and attention are maintained in later age, meaning there is reason to suspect that in both older and younger adults emotional arousal will similarly enhance subsequent attention biases to neutral stimuli.

To test these competing hypotheses, we measured arousal-biased competition in older adults using the procedure described in Sutherland and Mather (2012), and compared the data from these older adults to the younger adults in Sutherland and Mather (2012). In this design, participants are first exposed to an emotionally arousing sound, which is followed by a brief presentation of eight letters (see Figure 1). The goal is to identify all eight letters, however attention is biased to a perceptually salient subset of the letters that appear in a darker font that contrasts more with the white background than the other letters. Thus the dark letters function as high salience stimuli and the lighter letters as low salience stimuli. The difference between neutral and emotionally arousing conditions in the number of dark letters detected and the number of light letters detected provides a measure of attention bias, allowing a direct test of our competing hypotheses.

Figure 1.

Figure 1

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Schematic depiction of the experimental procedure.

Methods

Participants

Fifty-five older adults (27 female) participated for a small monetary compensation. Older adults were recruited through the University of Southern California Healthy Minds database and ranged from 61 – 80 (M = 70.7, SD = 5.1) years in age, and had from 12 – 28 (M = 16.4, SD = 3.1) years of education with a vocabulary aptitude (Brown, Fishco, & Hanna, 1993) ranging from 0.24 – 0.96 (M = 0.73, SD = 0.17). On scales from 1 – 10 they ranged from 1 – 9 (M = 4.0, SD = 2.2) in self-reported stress, and from 4 – 9 (M = 7.2, SD = 1.3) in subjective measures of health. As reported in Sutherland and Mather (2012), 110 younger adults (80 female) were recruited through the USC undergraduate research subject pool and were run in two separate experiments (see Experiment 1 and Condition 1 of Experiment 2 from Sutherland and Mather, 2012). They ranged from 18 – 29 (M = 20.3, SD = 2.3) in years of age, and on a scale from 1 – 10 reported subjective levels of stress ranging from 1 – 9 (M = 4.2, SD = 2.0).

Materials

Emotional arousal was manipulated using a set of 40 audio recordings selected from the International Affective Digital Sound (IADS) system (Bradley & Lang, 2007) (see Table 1). The letters were presented in Arial font and consisted of two different contrast levels. The low contrast letters had an RGB value of 204 204 204; the high contrast letters had an RGB value of 102 102 102. The letter ‘I’ was not displayed on any trial, as it too closely resembled the lower case letter ‘L’. Each letter was simultaneously presented around the fixation cross, forming a circular array that subtended 11.08° × 14.58° of visual arc. Which letters were presented, and their respective contrast levels were randomly selected on a trial-by-trial basis.

Table 1.

Library numbers for IADS stimuli.

Stimulus Type IADS Library Numbers
Negative Arousing 106 115 134 244 255 260 276 279 282 283
289 292 420 501 600 624 626 711 712 730
Neutral 102 113 130 132 170 225 246 250 252 322
358 373 375 377 382 701 708 720 723 728
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Procedure

Five practice trials preceded the main experiment. Every trial began with a 4-second presentation of a fixation-cross, followed by a 6-second audio recording presented via headphones (see Figure 1). Once the recording ended, there was a brief delay, followed by the presentation of the 8-letter array. The inter-stimulus interval (ISI) separating the end of the sound and the presentation of the letters ranged from 750 – 3000 milliseconds (ms). This was done to discourage participants from directly fixating on any of the letters by making their exact presentation time unknown. The letters were presented for 200 ms, and participants were immediately cued to report the letters they saw via key press. Recall was self-paced. The fixation cross remained on the screen until recall began, and participants were directed to focus on it throughout the entire trial.

Once the experiment ended, participants rated the valence and arousal level of all 40 sounds. The rating was self-paced, and the valence and arousal scales ranged from 1–9. A valence rating of 1 indicated extremely negative (9 being most positive), while an arousal rating of 1 indicated no arousal (9 being the highest). Once the ratings were completed, participants were debriefed and then excused from the study.

Results

We started by examining just the older adults’ data. To examine whether exposure to negative arousing sounds increased the bias to report high salience letters, hierarchical linear model (HLM) analyses were used to predict the number of letters recalled on a given trial, based on each participant’s valence rating and arousal rating of the sound presented on that trial. With this approach both the within-subject variance and the between-subject variance of the predictors are modeled. Both emotional arousal ratings and valence ratings were centered on the group mean. Three separate dependent measures were calculated—the number of high salience letters recalled, the number of low salience letters recalled and difference scores (high salience – low salience). Difference scores were the primary dependent measure of interest, as this score can detect simultaneous increases and decreases in recall of either letter type. However we also modeled high salience recall and low salience recall separately, to see if effects manifested as increases in recall of high salience letters only, or as decreases in recall of low salience letters only. In all three models we entered the group-centered mean decibel level (dB) of every sound as a predictor to adjust the shared variance between the physical intensity of the sounds and the subjective emotional arousal they elicit. Since greater difference scores reflect stronger visual salience effects in attention, we hypothesized that higher arousal ratings and lower valence ratings would predict greater difference scores on a trial-by-trial basis, while adjusting for the shared variance of the dB levels of the sounds. We also hypothesized that the mean dB predictor would not reach significance.

Overall the HLM results supported our predictions. Arousal ratings predicted difference scores in the expected direction (see Table 2A), showing that the bias to recall high salience letters increased with higher levels of emotional arousal.1 The valence ratings did not reach significance. Next we examined whether the increase in difference scores was driven by participants recalling more high salience letters, or by recalling fewer low salience letters on trials that were more arousing. The results show that increases in difference scores associated with emotional arousal appear to be driven by increases in recall of high salience letters, as emotional arousal ratings predicted greater recall of high salience letters (see Table 2B) but had no significant influence on recall of low salience letters (see Table 2C). Similarly, the valence rating predictor did not reach significance in either model. The mean dB predictor did not reach significance in all three models.

Table 2.

Hierarchical linear model (HLM) analysis of older adults (n = 55) using the arousal ratings (1 = least arousing, 9 = most arousing) of the sounds, the valence ratings of the sounds (1 = most negative, 5 = neutral, 9 = most positive), as well as the mean dB (physical intensity) of the sounds to predict (A) difference scores (high salience minus low salience), (B) the number of high salience letters recalled and (C) the number of low salience letters recalled.

A. Difference Scores (High Salience minus Low Salience)
Effect b SE t df p
Intercept 0.3413636 0.1175486 2.90 54 <0.01
Arousal Rating 0.0360472 0.0167557 2.15 2142 0.032
Valence Rating −0.0281695 0.0149569 −1.88 2142 0.060
Mean dB 0.0000373 0.0019003 0.02 2142 0.984
B. High Salience Recall
Effect b SE t df p
Intercept 1.4927273 0.0669241 22.31 54 <0.001
Arousal Rating 0.0176652 0.0089641 1.97 2142 0.049
Valence Rating −30.0132682 0.0080017 −31.66 2142 0.097
Mean dB 0.0002447 0.0010166 0.24 2142 0.810
C. Low Salience Recall
Effect b SE t df p
Intercept 1.1513636 0.0703259 16.37 54 <0.001
Arousal Rating −30.0183819 0.0095889 −31.92 2142 0.055
Valence Rating 0.0149013 0.0085595 1.74 2142 0.082
Mean dB 0.0002074 0.0010875 0.19 2142 0.849
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To more directly examine the influence of age on attention biases associated with emotional arousal, we pooled these data with data reported in Sutherland and Mather (2012) and re-ran all three models. However this time we included participant’s age group as a predictor. Corroborating the findings of our previous models, it was observed that greater arousal ratings predicted greater difference scores—an effect that was driven by increases in recall of high salience letters, for arousal ratings did predict greater high salience recall (see Table 3B), but had no significant influence on recall of low salience letters (see Table 3C). Age predicted smaller difference scores and age also predicted high salience recall and low salience recall separately and in a negative direction, suggesting that the bias to recall high salience letters was smaller in older adults and that they recall fewer letters overall regardless of salience level. And age did not interact with arousal or valence ratings in predicting difference scores, or in predicting high salience or low salience recall (see Table 4).

Table 3.

Hierarchical linear model (HLM) analysis of older adults (n = 55) and younger adults (n = 110) using the arousal ratings (1 = least arousing, 9 = most arousing) of the sounds, the valence ratings of the sounds (1 = most negative, 5 = neutral, 9 = most positive), and age group as well as the mean dB (physical intensity) of the sounds to predict (A) difference scores (high salience minus low salience), (B) the number of high salience letters recalled and (C) the number of low salience letters recalled.

A. Difference Scores (High Salience minus Low Salience)
Effect b SE t df p
Intercept 0.0911364 0.0686337 1.33 164 >0.05
Arousal Rating 0.0203270 0.0089708 2.27 6432 0.024
Valence Rating −0.0160107 0.0094667 −1.69 6432 0.091
Mean dB 0.0008306 0.0011471 0.72 6432 0.469
Age 0.2502273 0.0686337 3.65 163.08 <0.001
B. High Salience Recall
Effect b SE t df p
Intercept 1.6700000 0.0363861 45.90 164 <0.001
Arousal Rating 0.0140457 0.0047339 2.97 6432 0.003
Valence Rating −0.0086282 0.0049956 −1.73 6432 0.084
Mean dB 0.0004343 0.0006053 0.72 6432 0.473
Age −0.1772727 0.0363861 −4.87 163.07 <0.001
C. Low Salience Recall
Effect b SE t df p
Intercept 1.5788636 0.0460084 34.32 164 <0.001
Arousal Rating −0.0062813 0.0054185 −1.16 6432 0.246
Valence Rating 0.0073825 0.0057181 1.29 6432 0.197
Mean dB −0.0003963 0.0006929 −0.57 6432 0.567
Age −0.4275000 0.0460084 −9.29 163.07 <0.001
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Table 4.

Hierarchical linear model (HLM) analysis of older adults (n = 55) and younger adults (n = 110) using the arousal ratings (1 = least arousing, 9 = most arousing) of the sounds, the valence ratings of the sounds (1 = most negative, 5 = neutral, 9 = most positive), the mean dB (physical intensity) of the sounds, as well as the interactions between age group and arousal ratings and between age and valence ratings to predict difference scores (high salience minus low salience).

Difference Scores (High Salience minus Low Salience)
Effect b SE t df p
Intercept 0.091136 0.068634 1.33 164 >0.05
Arousal Rating 0.026716 0.010263 2.60 6430 0.009
Valence Rating −0.019826 0.009901 −2.00 6430 0.045
Mean dB 0.000880 0.001148 0.77 6430 0.444
Age 0.250227 0.068634 3.65 163.08 <0.001
Age × Arousal Rating 0.010294 0.010179 1.01 6430 0.312
Age × Valence Rating −0.008668 0.009912 −0.88 6430 0.382
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Finally, we modeled the number of incorrect letters reported on each trial. This was done to ensure that participants who were reporting more letters correctly were not also reporting more letters incorrectly, which could negate our interpretation that emotional arousal increases biases to attend to salient stimuli. As expected, arousal ratings and mean dB failed to predict incorrect responses, however the valence rating and age predictors did reach significance (see Table 5). This suggests that when the effects of negative valence are separated from the effects of emotional arousal, negative valence can interfere with selective attention, thus increasing the likelihood of mistaking a possible target for a target that was not actually displayed. However, we also observed that older age had the opposite effect on attention and leads to fewer errors, which suggests that older adults are less susceptible to false recall.

Table 5.

Hierarchical linear model (HLM) analysis using the arousal and valence ratings of the sounds, the mean dB of the sounds and age group as predictors of the number of incorrectly reported letters.

Older and Younger Adults Incorrect Responses
Effect b SE t df p
Intercept 0.5529545 0.0457304 12.09 164 <0.001
Arousal Rating −0.0055707 0.0041893 −1.33 6432 0.184
Valence Rating −0.0092037 0.0044209 −2.08 6432 0.037
Mean dB 0.0004734 0.0005357 0.88 6432 0.377
Age −0.1511364 0.0457304 −3.31 163.06 0.001
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Discussion

In this study we examined emotion-induced attention biases in older and younger adults. More specifically, we examined whether negative arousal increased attention biases to salient stimuli—an effect that has been observed previously in younger adults (Sutherland & Mather, 2012). To do this we separated the emotion-eliciting stimulus from the targets used to measure attention, allowing us to dissociate biases towards emotional objects from other potential influences that emotion may have on attention.

Our goal was to examine whether arousal continues to amplify biased competition processes in later age. Previous research reveals age-related declines on measures of visual perception (Bennet, et al., 2007; Flaubert, 2002; Habak & Faubert, 2000) and visual search (Madden, 2007). Moreover, older adults also show weaker physiological responses to emotional stimuli (Gavazzeni, et al., 2008; Levenson, et al., 1991), suggesting that emotional arousal may have less of an influence on attention in later age. Thus one possible hypothesis was that these age-related declines would interfere with emotion-induced attention biases to subsequently presented stimuli.

On the other hand, there is evidence that interactions between emotion and attention persist in later age. The ability to detect an emotional stimulus hidden among distracters is maintained (Hahn, et al., 2006; Leclerc & Kensinger, 2008; Mather & Knight, 2006), as well as the ability to ignore emotional distracters (Ebner & Johnson, 2010; Mather, 2012; Thomas & Hasher, 2006), which suggests that emotional influences over attention, as well as attention influences over emotion, remain stable in older adults. This led us to hypothesize that like younger adults, older adults would show increased attention biases to highly salient objects following exposure to an emotionally arousing stimulus.

We conducted several HLM analyses to examine this hypothesis. First we examined a group of older adults separately, and then pooled these data with the younger adult sample that was originally reported in Sutherland and Mather (2012). This allowed us to examine the influence of age and emotional arousal on attention to high salience letters. Despite older age predicting an overall decline in the number of targets that were reported, as well as a decline in the bias to recall high salience targets, higher arousal ratings continued to predict greater attention biases to objects with high salience. This suggests that after adjusting for shared variance between arousal ratings and age with respect to biases to recall high salience letters, arousal ratings continued to predict recall of both difference scores and high salience letters, suggesting that emotional arousal enhances selective attention biases produced by differences in perceptual salience similarly in younger and older adults.

But unlike the HLM analyses reported in Sutherland and Mather (2012), we found no significant effect indicating that emotional arousal decreased recall of low salience letters. The difference here was that we included each participant’s age group as a predictor, as well as each individual’s arousal rating for each item. In the previous report, we used established norms to categorize each item. In the current study we used individual responses, as we were concerned about potential age differences in how arousing or negative certain sounds would be. It is not clear why using individual arousal ratings would be less likely to reveal arousal impairment effects for low salient letters than using previous norms to indicate which stimuli fall into which category, but this would be interesting to examine in future research.

Moreover, we also observed that negative valence predicted more false reports of letters, but surprisingly older age had the opposite effect on false recall, as older age predicted fewer falsely reported letters. This finding was unexpected given that older adults have been shown to produce more false memories compared to younger adults (Norman & Schacter, 1997), as they rely more on gist processing than on item processing during memory encoding (Dennis, Kim, & Cabeza, 2007; Tun, Wingfield, Rosen, & Blanchard, 1998). But perhaps this divergence in results is due to the limited number of items that were presented as targets in our experiment, for studies demonstrating greater false recall in older adults used word stimuli to measure memory, which results in more unique items to recall and affords more semantic overlap with related information. However, a direct test of this idea is needed to make any useful interpretations regarding aging and false memory of letters versus words.

Taken together, our results indicate that emotional arousal increases the mental dominance of perceptually salient objects—an effect that shows no decline in older adults. This provides further evidence for ABC theory (Mather & Sutherland, 2011), and suggests that these predictions extend to older adults, at least in terms of how arousal interacts with bottom-up salience to influence memory encoding. In future studies it will be important to manipulate positive emotional arousal in older adults to determine whether it has the same effect as negative arousal on attention to perceptually salient stimuli (for evidence that positive and negative arousal can have similar ABC effects for younger adults, see Sakaki, Fryer, & Mather, in press). Moreover, identifying the neural mechanisms that underlie the behavioral effects of emotional influences on attention, and whether older and younger adults use the same neural mechanisms to achieve the same emotion-induced biases would add significantly to our current understanding of emotion and cognitive aging. But in any case, our results add to a growing body of literature that suggests that emotional processing remains effective in later age despite losses in perception and attention that are associated with cognitive aging.

Footnotes

1

The unstandardized b coefficient of the intercept represents the expected number of high or low salience letters recalled when the predictors are held constant at their own respective means. With each increase (or decrease) of a single unit within a given predictor, the expected number of letters recalled increases (or decreases) by the b coefficient of that predictor. For example, because arousal ratings are centered they have a mean of zero, so as arousal ratings increase or decrease by one unit the expected number of high salience letters recalled (Table 2B) increases or decreases from 1.4927273 by 0.0176652.

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