The influence of emotive visual stimulation and anxiety on attention biases and memory Rosa Angela Fabio (rafabio@unime.it) Department of Cognitive Science, University of Messina, via Concezione, 6/8, Messina, Italy Daniela Palato (dpalato@unime.it) Department of Cognitive Science, University of Messina, via Concezione, 6/8, Messina, Italy Antonino Errante (aerrante@libero.it) Department of Neuroscience, University of Parma, via Volturno, 39, Parma, Italy Alessandra Falzone (alessandra.falzone@unime.it) Department of Cognitive Science, University of Messina, via Concezione, 6/8, Messina, Italy Antonino Pennisi (apennisi@unime.it) Department of Cognitive Science, University of Messina, via Concezione, 6/8, Messina, Italy Abstract function and episodic memory across various anxiety disorders (Airaksinen, Larsson and Forsell, 2005). The Literacy: Many studies have been showing that anxious precise impact of anxiety on cognition is, however, unclear. individuals display attention biases including preferential In general, anxiety sensitizes sensory cortical systems to engagement, difficulty in disengagement, or attention innocuous environmental stimuli. More conclusive evidence avoidance. Research in patients suggests that pathological that anxiety enhances sensory- perceptual processing comes anxiety may specifically impair spatial short-term and long- from studies that include intrinsically salient stimuli. Facial term episodic memory. Recently, many authors have emphasized the role of aversive stimulation on attention, displays of emotion have been heavily-used in this regard working memory and anxiety. Purpose: The present study (Haxby et al., 2000; Phillips et al., 2003). Clinical investigated the influence of anxiety on memory and populations shows comparable biases toward aversive attention, to contribute to our understanding of the anxiety relative to appetitive face across behavioral and neural effects on cognitive function. Methods: 130 students were dimensions (Blair et al., 2008; Roy et al., 2008), as do included in this study (57 male and 73 female). Procedure: individuals with increased dispositional anxiety (Cools et Each subject completed the State-Trait Anxiety Inventory (STAI). After this measure, only 41 participants with the al., 2005; Telzer et al., 2008). A wealth of research highest (n=21) and the lowest (n=20) levels of anxiety demonstrates that anxious individuals display an attention complete the Trail Making Test A-B, Attentive Matrices bias towards threatening sources of information, and this Test, Babcock Story Recall Test and Short-Term Visual effect is less consistent or typically not observed in non- Memory Test. Results: Less anxious participants showed anxious individuals (Bar-Haim et al., 2007; Mogg and best memory capacity and less attention biases than more Bradley, 1998). However, more recent studies have anxious participants. demonstrated qualitatively different types of biases, Keywords: anxiety; attention; emotive stimulation; including preferential engagement, difficulty in memory. disengagement, or attention avoidance (Cisler and Koster, 2010; Sheppes et al., 2013). There is substantial evidence that biases are not inflexible, but are, in fact, very plastic Introduction and strongly influenced by environmental stressors (Bar- Haim et al., 2010; Wald et al., 2013). The attention control theory posits that anxiety disrupts two central executive Some authors have argued that anxiety impairs the ability functions related to attention control: inhibition and to think and concentrate, suggesting that the interaction shifting. Inhibition refers to the ability to inhibit or regulate between emotion and cognition may elucidate the dominant or automatic responses. Shifting refers to the debilitating nature of pathological anxiety (Vytal et al., adaptive ability to shift attention between tasks depending 2012). Some of the prominent cognitive problems on context. Eysenck and colleagues (2007) discuss these associated with anxiety are correlate to impaired attention functions in terms of top-down and bottom-up processing. mechanisms. Anxious people complain of being easily Anxiety impairs inhibition in that anxiety weakens the distracted and have difficulty concentrating. Population- degree to which inhibitory mechanisms can regulate based studies have reported impairments in executive 593 automatic responses; that is, anxiety weakens top-down different level of anxiety shows different capacity of regulatory control. Research using the spatial cueing task immediate memory and recall; (3) visual stimulation has invariably demonstrated difficulty in disengagement through movies with emotional content influences the among anxious individuals (Amir et. al., 2003; Fox et. al., immediate visual memory in more anxious subjects. The 2001; Van Damme et al., 2006); moreover, research using assumption was that the more anxious subjects have poor the visual search task has almost invariably demonstrated memory performance after watching movies with emotional difficulty in disengagement among anxious individuals contents. (Lipp and Waters, 2007; Rinck et al., 2005). With regard to memory, anxiety has a selective effect that is dependent Materials and Methods on the modality (spatial or verbal), difficulty, and task type (working memory or long-term memory). Research in Participants patients suggests that pathological anxiety may specifically Data were collected from a sample of 130 participants of impair spatial short-term memory performance; patients both sexes. All subjects were assessed for trait anxiety with different anxiety disorders show deficits in spatial (State-Trait Anxiety Inventory). Subjects with an average working memory, but not verbal working memory level of anxiety (n=90) were excluded from successive performance or verbal working memory capacity (Kizilbash analysis. The remaining participants were 41 (28 et al. , 2002; Boldrini et al., 2005). In contrast, dispositional women and 13 men), aged 19 to 40 years (M=23.8, anxiety is frequently associated with reduced working SD=3.83), divided into two groups. In group 1 were memory capacity but not performance, as captured by digit included 20 participants, aged from 19 to 32 years old span measures or increased reaction time on verbal and (M=22.9, SD=2.77), with trait-anxiety scores below 46 spatial short-term memory tasks (Derakshan and Eysenck, (Less-anxious: M=36.8, SD=2). In group 2 were included 1998; Richards et al., 2000). Some works showed that, in 21 participants, aged from 19 to 40 years old (M=24.7, contrast with certain short-term memory tasks, patients with SD=4.52), with trait- anxiety scores above 46 (More- anxiety disorders are not impaired in long-term memory anxious: M=48, SD=2.87). A significant difference was (Kizilbash et al., 2002; Boldrini et al., 2005). However, found in these two groups t(39)=-14.4, p=<.001. The some studies on anxiety patients showed impairment in sample was counterbalanced for gender and age. long- term episodic memory (Asmundson et al., 1994; Airaksinen et al., 2005). Different emotional reactions can be induced by the presentation of visual stimuli with Instruments affective content. Emotional stimuli are processed and linked with cognitive functions, such as attention and The State-Trait Anxiety Inventory (STAI; Spielberger, memory. Stimuli with emotional content are best recovered Gorsuch and Lushene, 1970). The STAI presents anxiety in tests of recall and recognition than stimuli without scales divided into state-trait, rendering the class of emotional content. The same is true for attention (La-Bar anxiety identifiable (i.e., situational [provoked or and Phelps, 1998; Ochsner, 2000; Kensinger and Corkin, momentary] or trait [more permanent]). The STAI also 2003). Recently, the influence of aversive stimulation on presents standards for these two factors, as well as for the attention, working memory and anxiety was verified by entire scale (single factor with 20 items; Cronbach a = .79) Giron and Martins (2010). This study was conducted with and enables distinctions between men and women (Giron 366 participants of both sexes. Two DVD films, one and De Almeida, 2010). containing aversive stimuli and one containing neutral The Trial Making Test (TMT, A-B; Reitan, 1958) is a stimuli, were administrating. After viewing the DVD, widely used paper and pencil task that evaluates the anxiety, working memory, and attention were assessed. executive functions, dual-task attention, cognitive Concomitant with the increase in anxiety were deficits in flexibility and working memory. The TMT consists of working memory and deficits in selective attention in the two parts: on TMT Part A subjects have to connect group that was exposed to the aversive scenes. No gender numbers from 1 to 25, which are randomly spread over a differences were observed. These results suggests that sheet of paper, in ascending numerical order. On part B, aversive visual stimuli increase anxiety and decrease participants are asked to connect randomly spread numbers attention and working memory performance. Considering (from 1 to 13) and letters (from A to L) in alternating the current evidence of the relationship between numeric and alphabetical order (1-A-2-B-3-C-…-13-L). In cognition and the processing of emotional stimuli, the case of an error the examiner draws the attention of the present study investigated the influence of anxiety on participant to the error, so that the participant completes memory and attention, to contribute to our understanding of the task without errors (at the expense of additional time). the anxiety effects on cognitive function. In particular, the TMT performance was calculated taking the time needed goals of the present study were to determine whether (1) the to perform TMT-B minus time needed for TMT-A. This level of anxiety is a predictor of attention biases and delta TMT value ‘‘removes’’ eventual bias due to interfere with two central executive functions related to differences in upper extremity motor speed, simple attention control: inhibition and shifting; (2) subjects with sequencing, visual scanning, and psychomotor functioning. The Attentive Matrices Test (Spinnler and Tognoni, 1987). 594 Three identical arrays of 130 digits, disposed on 13 lines of 10 items each, which are presented in succession. The Results task of the subject is to try to identify, and barrage with a pencil, the stimuli target, among all the other distracters. Anxiety measures The Babcock Story Recall Test (Babcock, 1930) was Table 1 shows the mean STAI scores for both groups. used to examine verbal recall. The subjects were asked to Independent t-tests revealed that the groups differed immediately recall a story just read to them, then after the significantly on state-trait-anxiety levels, t(39)= -14.4, story was read to them again, recall it 10 min later. p=<.001. Scoring was based on 21 memory units, with allowances for immediate recall and penalties for missing information. Scores can range 0–21. Tab.1 Means and standard deviations of anxiety measures. The Short-Term Visual Memory Test. Four DVD Anxiety levels movies, one including neutral content (a men while Groups M SD sweeping), one about generosity (a selfless act of a child), Group 1 36,85 2,01 one showing the fighting between university students Less-Anxious and police (adverse) and another showing a child dancing Group 2 48,05 2,87 More-Anxious (funny), were used for both groups. A pilot study was carried out with 38 independent students of both sexes to examine the emotional valence of the content of the 4 visual stimulation. The content of the movies was suitable for what was proposed, considering that the movie with Trail Making Test adverse content (visual stimulation with unpleasant We examined the time of execution of the Trail Making emotions) was identified correctly as adverse by the 100% Test (Part A, Part B and B-A Score) in more anxious/less of the participants, the neutral movie was identified as anxious groups of subjects. The third phase was calculate “normal” by the 92% of participants, the movie about by subtracting the Part A Score from the Part B Score. A generosity was related to the some ethic topic and the 2(Group: More-Anxious, Less Anxious) x 3(TMT parts: funny movie was rated as “funny” by 93% of participants A, B, B-A) ANOVA with repeated measures revealed a (with classifications on rating-scale). The duration of each significant effect of the variable “TMT Parts” F(2, visual stimulation was 60 ss. The Visual Memory Test is 78)=413.49, p=<.0001. Also, the interaction Groups x composed of 7 item-questions regarding details of the TMT Part was significant F(2,78)=3.08, p=.05. This last movies (28 items). This test evaluates short- term visual analysis suggesting that results of TMT for More Anxiety memory. Group were different from those for Less Anxiety Group. In particular, on the average, the More Anxious Group and Less Anxious Group did not differ in TMT-A execution Procedure F(1,39)=2.52, p=.12. Instead, the two groups shows The application was taken in a public university. significant difference in the execution of TMT-B, According to schedules provided by teachers, the tests F(1,39)=12.8, p=.001, and in Part B-A comparison, were applied at the beginning of the classes or, sometimes, F(1,39)=8.48, p=.006. at the end of these. Following the heterogeneous elements of this study, the tests were diversified by selecting Attentive matrices Test different courses and, in each one of them, applied in their The attentive matrices test allows for the assessment of own classrooms. The students present in the class were two performance measures: speed (response times) and invited to participate. After they agreed, they completed a accuracy (number of counting errors). Two ANOVA with demographic questionnaire and signed a consent form. repeated measure on speed and accuracy were conducted. Each subject completed the state-anxiety scale of the A 2(Groups: More Anxious, Less Anxious) x 3(Matrices STAI, and was tested individually. After this measure, 1,2,3) ANOVA with repeated measure on the last only 41 participants with the highest and the lowest factors, using the accuracy as dependent variable, showed levels of anxiety complete the other four tasks (Trail a significant effect of the Phases F(2,78)=7856.4, Making Test A-B, Attentive Matrices Test, Babcock Story p=.<0001. Also, the variable between subject “Groups” Recall Test and Short-Term Visual Memory Test). To show a significant effect F(1,39)=60.04, p=<.0001. assess the visual short-term memory, four movies were Furthermore, the interaction Phases of Attentive Matrices x shown to the participants. After, participants answered Groups show an effect F(2,78)=4.49, p=.001. This data questions regarding the details of the movies. indicate that scores of more anxious subject were lower than less anxious participants in all conditions, and decreased for more complex task. After, reaction time in Attentive Matrices Tasks were analyzed. A 2(Group: More Anxious, Less Anxious) x 3(Matrices 1,2,3) 595 ANOVA with repeated measure on the last factors, using biases, than more anxious participant. Also, the group with the reaction times as dependent variable, showed a high level of anxiety showed a limitation in various significant effect of variable “Phases” F(2,78)=38.3, attention and mnestic performance, both accuracy of p=<.0001. Moreover, the result were different for more responses and reaction time speed. Overall results show low anxious and less anxious participant F(1,39)=13.84, concentration, slower reaction and execution time and lower p=.001. Finally, a main effect of the interaction Groups x accuracy in more anxious subject, performed attention task Phases was found F(2,78)=13.29, p<=.001. This as the Attentive Matrices Test by Spinnler and Tognoni interaction evidence that non-anxious subject were faster in (1987) or Trail Making Test by Reitan (1958). Furthermore, the first task of attentive matrices and their these subjects were less able in Babcock Story Recall performance decreased in successive phases. Instead, more Test (1930), both immediate and delayed recall tasks. anxious subject performance was lower in all phases. Moreover, less anxious participant were more skilled in Visual memory Test. Their performance was better in all Memory performance visual stimulations conditions, even after viewing movies The impact of anxiety on cognitive function was with high level of emotional contents (as the aggressive investigate used the Babcock Story Recall Test. Data were and funny movies). In particular, the performance of analyzed by a 2(Group: More Anxious, Less Anxious) x anxious subjects in Trail Making test was lower compared 2(Phases: immediate recall, delayed recall) ANOVA with to less anxious participant, only in the second phase of test. repeated measures, using the second factor as between Instead, in the first phase no significant difference was subject variable. A main effect of Phases (immediate found. This data can be interpreted as due to different task vs. delayed recall) was found F(1,39)=7, p=<.01. This demands. Indeed, the second part of this test requires a great data indicate a high performance in immediate recall cognitive load on selective attention and working memory, compared to delayed recall task for both groups. Also that impairs the more anxious subjects performance. Even the variable Groups show a significant effect F(1, in Attentive matrices test, performances of anxious subject 39)=46.58, p=<.0001. Indeed, both mnestic index were were lower than less anxious participants in all conditions, lower in more anxiety subjects compared to non-anxious and decreased for more complex task (third matrices). Both participant. speed (response times) and accuracy (number of counting errors) less anxious group of subject show a better result. Movies Vision and Memory parameter An interesting data was that less anxious subject were The hypothesis was that stimulation through movies with faster in the first task of attentive matrices and their emotional content influences the immediate visual memory performance decreased in successive phases, instead more in anxious subjects. A 2(Group: More Anxious, Less anxious subject performance was lower in all phases. Anxious) x 4(category of movie: neutral, generosity, According with others evidence, this data confirm that adverse, funny) ANOVA with repeated measure on the anxiety influence many attention biases towards threatening last factor show a main effect of Groups F(1,39)=38.01, sources of information, engagement and disangagement of p=<.0001. Also the variable Category present a significant attention (Cisler and Koster, 2010; Sheppes et al., 2013; effect F(3,117)=4.59, p=<.004. Finally, the interaction Bar-Haim et al., 2007; Mogg and Bradley, 1998; Williams Groups x Category of Movies was significant F(3, et al., 1996). With regard to memory, anxiety has a 117)=3.25, p=<.02. This data suggested that after vision selective effect that is dependent on modality (spatial or of movies with emotive contents, the performance of more verbal), difficulty, and task type (working memory or long- anxious subject was poor compared to less anxious term memory). In this study, performances of more participants. anxious/less anxious subjects in memory tests showed different pattern of execution, with a high performance in Discussion and Conclusions immediate recall compared to delayed recall task for both groups. However, both mnestic index were lower in more anxiety subjects compared to less anxious participant. This Anxiety is known to play an important role in the evidence confirm that more anxious persons show functions of memory and attention (i. e. Bar-Haim et al., impairment in long-term episodic memory (Lucas et al., 2007; Mogg and Bradley, 1998; Kizilbash et al., 2002; 1991; Asmundson et al., 1994; Cohen et al., 1996; Boldrini et al., 2005). The present findings support the Airaksinen et al., 2005). However, further analysis should assumption that anxiety and emotion stimulation influences be performed to estimate the impact of anxiety on short attention and memory. Indeed, mental function performance term verbal memory. The role of visual stimulation was is directly linked to the different levels of anxiety explored in this study toward a visual memory test, after experienced and the strategies adopted by each individual to the vision of movies with emotive or neutral contents. deal with this function (Gable, Reis and Elliot, 2000; Leen- Precedent evidences shows that visual stimuli with Feldner et al., 2007). The comparison between two groups of emotional contents are best recovered in tests of recall and subjects with different levels of anxiety, respectively more recognition than stimuli without emotional content (La-Bar anxious and less anxious, evidence that less anxious and Phelps, 1998; Ochsner, 2000; Kensinger and Corkin, participants showed best memory capacity and less attention 596 2003). In our study we assessed the visual memory using population- based samples: evidence of episodic memory movies with ecological situations. In fact, precedent studies dysfunction. 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