Emotion suppression reduces hippocampal activity during successful memory encoding

NeuroImage

Volumn 63, Issue 1, 2012, Pages 525-532

  Binder, Julia ^a,b   de Quervain, Dominique J F ^c   Friese, Malte ^c   Luechinger, Roger ^d   Boesiger, Peter ^d   Rasch, Björn ^a,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b International Normal Aging and Plasticity Imaging Center INAPIC   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d ETH ZURICH   (Switzerland)

Author keywords

Emotion suppression; FMRI; Hippocampus; Memory

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN FUNCTION; COGNITION; DOWN REGULATION; EMOTION; EMOTION SUPPRESSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MEMORY; MEMORY DISORDER; MENTAL PERFORMANCE; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RECALL; VISUAL STIMULATION;

ADULT; AROUSAL; BRAIN MAPPING; EMOTIONS; FEMALE; HIPPOCAMPUS; HUMANS; INHIBITION (PSYCHOLOGY); MEMORY; NEURAL INHIBITION; YOUNG ADULT;

EID: 84864415329     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.07.007     Document Type: Article

References (55)

1. Bonanno G.A., Papa A., Lalande K., Westphal M., Coifman K. The importance of being flexible. Psychol. Sci. 2004, 15:482-487.
2. Cahill L. Why sex matters for neuroscience. Nat. Rev. Neurosci. 2006, 7:477-484.
3. Campbell-Sills L., Barlow D.H., Brown T.A., Hofmann S.G. Effects of suppression and acceptance on emotional responses of individuals with anxiety and mood disorders. Behav. Res. Ther. 2006, 44:1251-1263.
4. Demaree H.A., Robinson J.L., Pu J., Allen J.J.B. Strategies actually employed during response-focused emotion regulation research: affective and physiological consequences. Cogn. Emotion 2006, 20:1248-1260.
5. Demaree H.A., Schmeichel B.J., Robinson J.L., Pu J., Everhart D.E., Berntson G.G. Up- and down-regulating facial disgust: affective, vagal, sympathetic, and respiratory consequences. Biol. Psychol. 2006, 71:90-99.
6. Diekhof E.K., Geier K., Falkai P., Gruber O. Fear is only as deep as the mind allows: a coordinate-based meta-analysis of neuroimaging studies on the regulation of negative affect. NeuroImage 2011, 58:275-285.
7. Dillon D.G., Ritchey M., Johnson B.D., LaBar K.S. Dissociable effects of conscious emotion regulation strategies on explicit and implicit memory. Emotion 2007, 7:354-365.
8. Dolcos F., LaBar K.S., Cabeza R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 2004, 42:855-863.
9. Dunn B.D., Billotti D., Murphy V., Dalgleish T. The consequences of effortful emotion regulation when processing distressing material: a comparison of suppression and acceptance. Behav. Res. Ther. 2009, 47:761-773.
10. Egloff B., Schmukle S.C., Burns L.R., Schwerdtfeger A. Spontaneous emotion regulation during evaluated speaking tasks: associations with negative affect, anxiety expression, memory, and physiological responding. Emotion 2006, 6:356-366.
11. Erk S., von Kalckreuth A., Walter H. Neural long-term effects of emotion regulation on episodic memory processes. Neuropsychologia 2010, 48:989-996.
12. Friston, K.J., Buechel, C., Fink, G.R., Morris, J., Rolls, E., Dolan, R.J., 1997. Psychophysiological and modulatory interactions in Neuroimaging. Neuroimage 6, 218-229.
13. Goldin P.R., McRae K., Ramel W., Gross J.J. The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biol. Psychiatry 2008, 63:577-586.
14. Gross J.J. Antecedent- and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. J. Personal. Soc. Psychol. 1998, 74:224-237.
15. Gross J.J. Emotion regulation: affective, cognitive, and social consequences. Psychophysiology 2002, 39:281-291.
16. Gross J.J. Emotion regulation. Handbook of Emotions 2008, 497-512. Guilford, New York. M. Lewis, J.M. Haviland-Jones, L.F. Barett (Eds.).
17. Gross J.J., Levenson R.W. Emotional suppression - physiology, self-report, and expressive behavior. J. Personal. Soc. Psychol. 1993, 64:970-986.
18. Gross J.J., Levenson R.W. Hiding feelings: the acute effects of inhibiting negative and positive emotion. J. Abnorm. Psychol. 1997, 106:95-103.
19. Gross J.J., Richards J.M., John O.P. Emotion regulation in everyday life. Emotion Regulation in Couples and Families: Pathways to Dysfunction and Health 2006, 13-35. American Psychological Association, Washington, DC. D.K. Snyder, J. Simpson, J.N. Hughes (Eds.).
20. Hayes J.P., Morey R.A., Petty C.M., Seth S., Smoski M.J., McCarthy G., LaBar K.S. Staying cool when things get hot: emotion regulation modulates neural mechanisms of memory encoding. Front. Hum. Neurosci. 2010, 4:230.
21. Heatherton T.F., Wagner D.D. Cognitive neuroscience of self-regulation failure. Trends Cogn. Sci. 2011, 15:132-139.
22. Kalisch R. The functional neuroanatomy of reappraisal: time matters. Neurosci. Biobehav. Rev. 2009, 33:1215-1226.
23. Kensinger E.A., Clarke R.J., Corkin S. What neural correlates underlie successful encoding and retrieval? A functional magnetic resonance imaging study using a divided attention paradigm. J. Neurosci. 2003, 23:2407-2415.
24. Kim H. Neural activity that predicts subsequent memory and forgetting: a meta-analysis of 74 fMRI studies. NeuroImage 2011, 54:2446-2461.
25. LaBar K.S., Cabeza R. Cognitive neuroscience of emotional memory. Nat. Rev. Neurosci. 2006, 7:54-64.
26. Lang P.J., Bradley M.M., Cuthbert B.N. International affective picture system (IAPS): Affective ratings of pictures and instruction manual 2008, University of Florida, Gainesville, FL.
27. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 2003, 19:1233-1239.
28. Maldjian J.A., Laurienti P.J., Burdette J.H. Precentral gyrus discrepancy in electronic versions of the Talairach atlas. NeuroImage 2004, 21:450-455.
29. McGaugh J.L. Memory - a century of consolidation. Science 2000, 287:248-251.
30. McNally R.J. Psychological mechanisms in acute response to trauma. Biol. Psychiatry 2003, 53:779-788.
31. Murty V.P., Ritchey M., Adcock R.A., LaBar K.S. Reprint of: fMRI studies of successful emotional memory encoding: a quantitative meta-analysis. Neuropsychologia 2011, 49:695-705.
32. Ochsner K.N., Gross J.J. The cognitive control of emotion. Trends Cogn. Sci. 2005, 9:242-249.
33. Ochsner K.N., Gross J.J. Cognitive emotion regulation: insights from social cognitive and affective neuroscience. Curr. Dir. Psychol. Sci. 2008, 17:153-158.
34. Ohira H., Nomura M., Ichikawa N., Isowa T., Iidaka T., Sato A., Fukuyama S., Nakajima T., Yamada J. Association of neural and physiological responses during voluntary emotion suppression. NeuroImage 2006, 29:721-733.
35. Phan K.L., Wager T., Taylor S.F., Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 2002, 16:331-348.
36. Phan K.L., Wager T.D., Taylor S.F., Liberzon I. Functional neuroimaging studies of human emotions. CNS Spectr. 2004, 9:258-266.
37. Phan K.L., Fitzgerald D.A., Nathan P.J., Moore G.J., Uhde T.W., Tancer M.E. Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biol. Psychiatry 2005, 57:210-219.
38. Phillips M., Ladouceur C., Drevets W. A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol. Psychiatry 2008, 13:833-857.
39. Pruessmann K.P., Weiger M., Scheidegger M.B., Boesiger P. SENSE: sensitivity encoding for fast MRI. Magn. Reson. Med. 1999, 42:952-962.
40. Ranganath C., Heller A., Cohen M.X., Brozinsky C.J., Rissman J. Functional connectivity with the hippocampus during successful memory formation. Hippocampus 2005, 15:997-1005.
41. Rasch B., Spalek K., Buholzer S., Luechinger R., Boesiger P., Papassotiropoulos A., de Quervain D.J.-F. A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proc. Natl. Acad. Sci. 2009, 106:19191-19196.
42. Richards J.M. The cognitive consequences of concealing feelings. Curr. Dir. Psychol. Sci. 2004, 13:131-134.
43. Richards J.M., Gross J.J. Composure at any cost? The cognitive consequences of emotion suppression. Pers. Soc. Psychol. Bull. 1999, 25:1033-1044.
44. Richards J.M., Gross J.J. Emotion regulation and memory: the cognitive costs of keeping one's cool. J. Personal. Soc. Psychol. 2000, 79:410-424.
45. Richards J.M., Gross J.J. Personality and emotional memory: how regulating emotion impairs memory for emotional events. J. Res. Personal. 2006, 40:631-651.
46. Schott B.H., Wüstenberg T., Wimber M., Fenker D.B., Zierhut K.C., Seidenbecher C.I., Heinze H.-J., Walter H., Düzel E., Richardson-Klavehn A. The relationship between level of processing and hippocampal-cortical functional connectivity during episodic memory formation in humans 2011.
47. Seger C.A. The basal ganglia in human learning. Neuroscientist 2006, 12(4):285-290.
48. Snyder M. Self-monitoring of expressive behavior. J. Personal. Soc. Psychol. 1974, 30:526-537.
49. Spaniol J., Davidson P.S.R., Kim A.S.N., Han H., Moscovitch M., Grady C.L. Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 2009, 47:1765-1779.
50. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 1992, 99:195-231.
51. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002, 15:273-289.
52. Uncapher M.R., Rugg M.D. Effects of divided attention on fMRI correlates of memory encoding. J. Cogn. Neurosci. 2005, 17:1923-1935.
53. Urry H.L., van Reekum C.M., Johnstone T., Kalin N.H., Thurow M.E., Schaefer H.S., Jackson C.A., Frye C.J., Greischar L.L., Alexander A.L., Davidson R.J. Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J. Neurosci. 2006, 26:4415-4425.
54. van Reekum C.M., Johnstone T., Urry H.L., Thurow M.E., Schaefer H.S., Alexander A.L., Davidson R.J. Gaze fixations predict brain activation during the voluntary regulation of picture-induced negative affect. NeuroImage 2007, 36:1041-1055.
55. Wang S.H., Morris R.G.M. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu. Rev. Psychol. 2010, 61:49-79.