Remembered or forgotten stimuli: a functional magnetic resonance imaging study on the effects of emotion

Objective: The first aim of this study is to examine why emotional events enhance memory for preceding stimuli. The second goal is to identify brain regions associated with remembering and forgetting by finding brain activation differences during encoding of remembered and forgotten stimuli. The third goal is to examine which brain areas are activated when studying emotional pictures compared to neutral ones. Method: In each trial, a picture of an object followed by an emotional or neutral picture from the Turkish culture were presented to 15 volunteers. The effect of the succeeding pictures on the remembering of preceding stimuli was examined. The participants studied the stimuli in the magnetic resonance scanner and, meanwhile, brain images were taken. The memory performances of the participants were measured with the recognition test administered one week later. Results: Behavioral results suggest that emotion has no effect on memory for preceding stimuli. Functional magnetic resonance imaging results indicate that remembered stimuli compared to forgotten ones caused more activation in left inferior frontal gyrus and left superior medial gyrus. Emotional pictures create more activation in the - mid-temporal gyrus and supramarginal gyrus compared to neutral images. Conclusion: Brain structures in which activations are observed in remembered stimuli compared to forgotten ones (left inferior frontal gyrus and left superior medial gyrus) are responsible for the semantic elaboration and associative memory formation. Thus, it can be concluded that object pictures are remembered because they are processed more deeply. Besides, activations are observed in the areas known to be related to the processing of emotional face expressions when emotional and neutral pictures are compared.

PDF

___

1. Lee TH, Greening SG, Mather M. Encoding of goal-relevant stimuli is strengthened by emotional arousal in memory. Front Psychol 2015; 6:1173.

2. Nairne JS. Adaptive memory: Evolutionary constraints on remembering. In B. H. Ross (Ed.), The psychology of learning and motivation. Psychology of Learning and Motivation 2010; 53:1-32.

3. Anderson AK, Wais PE, Gabrieli JD. Emotion enhances remembrance of neutral events past. Proc Natl Acad Sci U S A 2006; 103:1599-1604.

4. LaBar KS, Cabeza R. Cognitive neuroscience of emotional memory. Nat Rev Neurosci 2006; 7:54-64.

5. Kensinger EA, Corkin S. Two routes to emotional memory: distinct neural processes for valence and arousal. Proc Natl Acad Sci U S A 2004; 101:3310-3315.

6. Bradley MM, Greenwald MK, Petry MC, Lang PJ. Remembering pictures: pleasure and arousal in memory. J Exp Psychol Learn Mem Cogn 1992; 18:379-390.

7. Kensinger EA, Brierley B, Medford N, Growdon JH, Corkin S. Effects of normal aging and Alzheimer’s disease on emotional memory. Emotion 2002; 2:118-134.

8. Hamann S. Cognitive and neural mechanisms of emotional memory. Trends Cogn Sci 2001; 5:394-400.

9. Murty VP, Ritchey M, Adcock RA, LaBar KS. fMRI studies of successful emotional memory encoding: A quantitative metaanalysis. Neuropsychologia 2010; 48:3459-3469.

10. Markowitsch HJ, Calabrese P, Würker M, Durwen HF, Kessler J, Babinsky R, et al. The amygdala’s contribution to memory--a study on two patients with Urbach-Wiethe disease. Neuroreport 1994; 5:1349-1352.

11. Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL. The amygdala and emotional memory. Nature 1995; 377:295-296.

12. Stefanacci L, Buffalo EA, Schmolck H, Squire LR. Profound amnesia after damage to the medial temporal lobe: A neuroanatomical and neuropsychological profile of patient E. P. J Neurosci 2000; 20:7024-7036.

13. McGaugh JL. Emotional arousal regulation of memory consolidation. Curr Opin Neurobiol 2018; 19:55-60.

14. Dolcos F, LaBar KS, Cabeza R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 2004; 42:855-863.

15. Uncapher MR, Wagner AD. Posterior parietal cortex and episodic encoding: insights from fMRI subsequent memory effects and dual-attention theory. Neurobiol Learn Mem 2009; 91:139-154.

16. Paller KA, Wagner AD. Observing the transformation of experience into memory. Trends Cogn Sci 2002; 6:93-102.

17. Brewer JB, Zhao Z, Desmond JE, Glover GH, Gabrieli JD. Making memories: brain activity that predicts how well visual experience will be remembered. Science 1998; 281:1185-1187.

18. Jia X, Gao C, Wang Y, Han M, Cui L, Guo C. Emotional arousal influences remembrance of goal-relevant stimuli. Emotion 2020; 20:1357-1368.

19. Most SB, Junge JA. Don’t look back: retroactive, dynamic costs and benefits of emotional capture. Vis Cogn 2008; 16:262-278.

20. Finn B, Roediger HL 3rd. Enhancing retention through reconsolidation: negative emotional arousal following retrieval enhances later recall. Psychol Sci 2011; 22:781-786.

21. Dunsmoor JE, Kroes MCW, Murty VP, Braren SH, Phelps EA. Emotional enhancement of memory for neutral information: The complex interplay between arousal, attention, and anticipation. Biol Psychol 2019; 145:134-141.

22. Mather M, Clewett D, Sakaki M, Harley CW. Norepinephrine ignites local hotspots of neuronal excitation: How arousal amplifies selectivity in perception and memory. Behav Brain Sci 2016; 39:e200.

23. Swallow KM, Atir S. The role of value in the attentional boost effect. Q J Exp Psychol (Hove) 2019; 72:523-542.

24. Schmidt SR, Schmidt CR. Inattentional blindness and the von Restorff effect. Mem Cognit 2015; 43:151-163.

25. Talmi D, Anderson AK, Riggs L, Caplan JB, Moscovitch M. Immediate memory consequences of the effect of emotion on attention to pictures. Learn Mem 2008; 15:172-182.

26. Lang PJ, Bradley MM, Cuthbert BN. International affective picture system (IAPS): technical manual and affective ratings. NIMH Center for the Study of Emotion and Attention 1997; 1:39-58.

27. Snodgrass JG, Vanderwart M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J Exp Psychol Hum Learn 1980; 6:174-215.

28. Schneider W, Eschman A, Zuccolotto A. E-Prime: user's guide. http://psy.swan.ac.uk/staff/lucignoli/E-Prime/ ReferenceGuideV2_2012.pdf. Accessed May 1, 2020.

29. Craik FIM, Lockhart RS. Levels of processing: a framework for memory research. JVLVB 1972; 11:671-684.

30. Adolphs R, Cahill L, Schul R, Babinsky R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn Mem 1997; 4:291-300.

31. O’Carroll RE, Drysdale E, Cahill L, Shajahan P, Ebmeier KP. Stimulation of the noradrenergic system enhances and blockade reduces memory for emotional material in man. Psychol Med 1999; 29:1083-1088.

32. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996; 29:162-173.

33. Koo TK, Li MY. A Guideline of selecting and reporting ıntraclass correlation coefficients for reliability research. J Chiropr Med 2016; 15:155-163.

34. Snodgrass JG, Corwin J. Pragmatics of measuring recognition memory: applications to dementia and amnesia. J Exp Psychol Gen 1988; 117:34-50.

35. Nasaruddin NH, Yusoff AN, Kaur S. Brain activation in response to randomized visual stimulation as obtained from conjunction and differential analysis: an fMRI study. J Phys Conf Ser 2014; 546:012003.

36. Vytal K, Hamann S. Neuroimaging support for discrete neural correlates of basic emotions: a voxel-based meta-analysis. J Cogn Neurosci 2010; 22:2864-2885.

37. Sabatinelli D, Fortune EE, Li Q, Siddiqui A, Krafft C, Oliver WT, et al. Emotional perception: meta-analyses of face and natural scene processing. Neuroimage 2011; 54:2524-2533.

38. Milner D, Goodale M. The visual brain in action. New York, NY: Oxford University Press, 2006.

39. Rosen HJ, Wilson MR, Schauer GF, Allison S, Gorno-Tempini ML, Pace-Savitsky C, et al. Neuroanatomical correlates of impaired recognition of emotion in dementia. Neuropsychologia 2006; 44:365-373.

40. Rossion B, Caldara R, Seghier M, Schuller AM, Lazeyras F, Mayer E. A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 2003; 126:2381-2395.

41. Haxby JV, Hoffman EA, Gobbini MI. The distributed human neural system for face perception. Trends Cogn Sci 2000; 4:223-233.

42. Reed CL, Caselli RJ. The nature of tactile agnosia: a case study. Neuropsychologia 1994; 32:527-539.

43. Alat Z. News coverage of violence against women: The Turkish case. Feminist Media Studies 2006; 6:295-314.

44. Sogut F. Turkish cinema and violence: a research on the presentation of violence in recent Turkish films. Atatürk University Institute of Fine Arts Journal 2020; 26:246-257.

45. Arcan E. Interrupted social peace: Hate speech in Turkish media. The IAFOR Journal of Media, Communication and Film 2013; 1:43-56.

46. Ayranci U, Kosgeroglu N, Gunay Y. Determining the violence rating in the movies displayed at the time the children watch television most. Anadolu Psikiyatri Derg 2004; 5:133-140.

47. Bradley MM, Lang PJ, Cuthbert BN. Emotion, novelty, and the startle reflex: habituation in humans. Behav Neurosci 1993; 107:970-980.

48. Cahill L, Haier RJ, Fallon J, Alkire MT, Tang C, Keator D, et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc Natl Acad Sci U S A 1996; 93:8016-8021.

49. Prince SE, Daselaar SM, Cabeza R. Neural correlates of relational memory: successful encoding and retrieval of semantic and perceptual associations. J Neurosci 2005; 25:1203-1210.

50. Prince SE, Tsukiura T, Cabeza R. Distinguishing the neural correlates of episodic memory encoding and semantic memory retrieval. Psychol Sci 2007; 18:144-151.

51. Christianson SA. Emotional stress and eyewitness memory: a critical review. Psychol Bull 1992; 112:284-309.

52. Ritchey M, Bessette-Symons B, Hayes SM, Cabeza R. Emotion processing in the aging brain is modulated by semantic elaboration. Neuropsychologia 2011;49:640-650.

53. Kirchhoff BA, Schapiro ML, Buckner RL. Orthographic distinctiveness and semantic elaboration provide separate contributions to memory. J Cogn Neurosci 2005; 17:1841-1854.

54. Cansino S, Maquet P, Dolan RJ, Rugg MD. Brain activity underlying encoding and retrieval of source memory. Cereb Cortex 2002; 12:1048-1056.