Cognitive, Affective, & Behavioral Neuroscience

, Volume 14, Issue 4, pp 1327–1339 | Cite as

Distinct parietal sites mediate the influences of mood, arousal, and their interaction on human recognition memory



The two dimensions of emotion, mood valence and arousal, have independent effects on recognition memory. At present, however, it is not clear how those effects are reflected in the human brain. Previous research in this area has generally dealt with memory for emotionally valenced or arousing stimuli, but the manner in which interacting mood and arousal states modulate responses in memory substrates remains poorly understood. We investigated memory for emotionally neutral items while independently manipulating mood valence and arousal state by means of music exposure. Four emotional conditions were created: positive mood/high arousal, positive mood/low arousal, negative mood/high arousal, and negative mood/low arousal. We observed distinct effects of mood valence and arousal in parietal substrates of recognition memory. Positive mood increased activity in ventral posterior parietal cortex (PPC) and orbitofrontal cortex, whereas arousal condition modulated activity in dorsal PPC and the posterior cingulate. An interaction between valence and arousal was observed in left ventral PPC, notably in a parietal area distinct from the those identified for the main effects, with a stronger effect of mood on recognition memory responses here under conditions of relative high versus low arousal. We interpreted the PPC activations in terms of the attention-to-memory hypothesis: Increased arousal may lead to increased top-down control of memory, and hence dorsal PPC activation, whereas positive mood valence may result in increased activity in ventral PPC regions associated with bottom-up attention to memory. These findings indicate that distinct parietal sites mediate the influences of mood, arousal, and their interplay during recognition memory.


Emotion Recollection Parietal cortex Prefrontal cortex 

Supplementary material

13415_2014_266_Fig6_ESM.jpg (174 kb)
Supplementary Fig. 1

FEAT model and contrast specification for quadrupled t test design. (JPEG 174 kb)

13415_2014_266_MOESM1_ESM.tif (127 kb)
High resolution image (TIFF 127 kb)


  1. Anderson, A., Wais, P., & Gabrieli, J. D. E. (2006). Emotion enhances remembrance of neutral events past. Proceedings of the National Academy of Sciences, 103, 1599–1604.CrossRefGoogle Scholar
  2. Basso, M. R., Schefft, B. K., Ris, M. D., & Dember, W. N. (1996). Mood and global–local visual processing. Journal of the International Neuropsychological Society, 2, 249–255.PubMedCrossRefGoogle Scholar
  3. Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2003). General multilevel linear modeling for group analysis in FMRI. NeuroImage, 20, 1052–1063.PubMedCrossRefGoogle Scholar
  4. Blood, A. J., Zatorre, R. J., Bermudez, P., & Evans, A. C. (1999). Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nature Neuroscience, 2, 382–387.PubMedCrossRefGoogle Scholar
  5. Cabeza, R., Ciaramelli, E., Olson, I. R., & Moscovitch, M. (2008). The parietal cortex and episodic memory: An attentional account. Nature Reviews Neuroscience, 9, 613–625.PubMedCentralPubMedCrossRefGoogle Scholar
  6. Ciaramelli, E., Grady, C., Levine, B., Ween, J., & Moscovitch, M. (2010). Top-down and bottom-up attention to memory are dissociated in posterior parietal cortex: Neuroimagingand and neuropsychological evidence. Journal of Neuroscience, 30, 4943–4956.PubMedCrossRefGoogle Scholar
  7. Ciaramelli, E., Grady, C. L., & Moscovitch, M. (2008). Top-down and bottom-up attention to memory: A hypothesis (AtoM) on the role of the posterior parietal cortex in memory retrieval. Neuropsychologia, 46, 1828–1851.PubMedCrossRefGoogle Scholar
  8. Ciavarro, M., Ambrosini, E., Tosoni, A., Committeri, G., Fattori, P., & Galletti, C. (2013). rTMS of medial parieto-occipital cortex interferes with attentional reorienting during attention and reaching tasks. Journal of Cognitive Neuroscience, 25, 1453–1462.PubMedCrossRefGoogle Scholar
  9. Corbetta, M., Kincade, J. M., Ollinger, J. M., McAvoy, M. P., & Shulman, G. L. (2000). Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nature Neuroscience, 3, 292–297.PubMedCrossRefGoogle Scholar
  10. Corson, Y., & Verrier, N. (2007). Emotions and false memories: Valence or arousal? Psychological Science, 18, 208–211. doi:10.1111/j.1467-9280.2007.01874.x PubMedCrossRefGoogle Scholar
  11. Davidson, P. S., Anaki, D., Ciaramelli, E., Cohn, M., Kim, A. S., Murphy, K. J., & Levine, B. (2008). Does lateral parietal cortex support episodic memory? Evidence from focal lesion patients. Neuropsychologia, 46, 1743–1755. doi:10.1016/j.neuropsychologia.2008.01.011 PubMedCentralPubMedCrossRefGoogle Scholar
  12. Demeter, E., Hernandez-Garcia, L., Sarter, M., & Lustig, C. (2011). Challenges to attention: A continuous arterial spin labeling (ASL) study of the effects of distraction on sustained attention. NeuroImage, 54, 1518–1529.PubMedCentralPubMedCrossRefGoogle Scholar
  13. Denkova, E., Dolcos, S., & Dolcos, F. (2013a). The effect of retrieval focus and emotional valence on the inferior frontal cortex activity during autobiographical recollection. Frontiers in Behavioral Neuroscience, 7, 192.PubMedCentralPubMedGoogle Scholar
  14. Denkova, E., Dolcos, S., & Dolcos, F. (2013b). The effect of retrieval focus and emotional valence on the medial temporal lobe activity during autobiographical recollection. Frontiers in Behavioral Neuroscience, 7, 109.PubMedCentralPubMedGoogle Scholar
  15. Dolcos, F., LaBar, K. S., & Cabeza, R. (2004). Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: An event-related fMRI study. NeuroImage, 23, 64–74. doi:10.1016/j.neuroimage.2004.05.015 PubMedCrossRefGoogle Scholar
  16. Finn, B., & Roediger, H. L., III. (2011). Enhancing retention through reconsolidation: Negative emotional arousal following retrieval enhances later recall. Psychological Science, 22, 781–786. doi:10.1177/0956797611407932 PubMedCrossRefGoogle Scholar
  17. Gasper, K., & Clore, G. L. (2002). Attending to the big picture: Mood and global versus local processing of visual information. Psychological Science, 13, 34–40. doi:10.1111/1467-9280.00406 PubMedCrossRefGoogle Scholar
  18. Grabenhorst, F., & Rolls, E. T. (2011). Value, pleasure and choice in the ventral prefrontal cortex. Trends in Cognitive Sciences, 15, 56–67.PubMedCrossRefGoogle Scholar
  19. Greene, C. M., Bahri, P., & Soto, D. (2010). Interplay between affect and arousal in recognition memory. PLoS ONE, 5, e11739. doi:10.1371/journal.pone.0011739 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Han, S., Jiang, Y., Gu, H., Rao, H., Mao, L., Cui, Y., & Zhai, R. (2004). The role of human parietal cortex in attention networks. Brain, 127, 650–659. doi:10.1093/brain/awh071 PubMedCrossRefGoogle Scholar
  21. Haramati, S., Soroker, N., Dudai, Y., & Levy, D. A. (2008). The posterior parietal cortex in recognition memory: A neuropsychological study. Neuropsychologia, 46, 1756–1766.PubMedCrossRefGoogle Scholar
  22. Isen, A. M., Johnson, M. M., Mertz, E., & Robinson, G. F. (1985). The influence of positive affect on the unusualness of word associations. Journal of Personality and Social Psychology, 48, 1413–1426.PubMedCrossRefGoogle Scholar
  23. Jefferies, L. N., Smilek, D., Eich, E., & Enns, J. T. (2008). Emotional valence and arousal interact in attentional control. Psychological Science, 19, 290–295.PubMedCrossRefGoogle Scholar
  24. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17, 825–841.PubMedCrossRefGoogle Scholar
  25. Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5, 143–156.PubMedCrossRefGoogle Scholar
  26. Judde, S., & Rickard, N. (2010). The effect of post-learning presentation of music on long-term word-list retention. Neurobiology of Learning and Memory, 94, 13–20. doi:10.1016/j.nlm.2010.03.002 PubMedCrossRefGoogle Scholar
  27. Kalpouzos, G., Fischer, H., Rieckmann, A., Macdonald, S. W., & Backman, L. (2012). Impact of negative emotion on the neural correlates of long-term recognition in younger and older adults. Frontiers in Integrative Neuroscience, 6, 74.PubMedCentralPubMedCrossRefGoogle Scholar
  28. Kensinger, E. A., & Corkin, S. (2004). Two routes to emotional memory: Distinct neural processes for valence and arousal. Proceedings of the National Academy of Sciences, 101, 3310–3315. doi:10.1073/pnas.0306408101 CrossRefGoogle Scholar
  29. Kim, H. (2011). Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies. NeuroImage, 54, 2446–2461.PubMedCrossRefGoogle Scholar
  30. Kuhbandner, C., & Pekrun, R. (2013). Affective state influences retrieval-induced forgetting for integrated knowledge. PLoS ONE, 8, e56617. doi:10.1371/journal.pone.0056617 PubMedCentralPubMedCrossRefGoogle Scholar
  31. Lane, A. R., Smith, D. T., Schenk, T., & Ellison, A. (2011). The involvement of posterior parietal cortex in feature and conjunction visuomotor search. Journal of Cognitive Neuroscience, 23, 1964–1972.PubMedCrossRefGoogle Scholar
  32. Liu, D. L., Graham, S., & Zorawski, M. (2008). Enhanced selective memory consolidation following post-learning pleasant and aversive arousal. Neurobiology of Learning and Memory, 89, 36–46.PubMedCrossRefGoogle Scholar
  33. Mather, M. (2007). Emotional arousal and memory binding: An object-based framework. Perspectives on Psychological Science, 2, 33–52. doi:10.1111/j.1745-6916.2007.00028.x CrossRefGoogle Scholar
  34. Mickley Steinmetz, K. R., & Kensinger, E. A. (2009). The effects of valence and arousal on the neural activity leading to subsequent memory. Psychophysiology, 46, 1190–1199. doi:10.1111/j.1469-8986.2009.00868.x PubMedCentralPubMedCrossRefGoogle Scholar
  35. Nielson, K. A., & Arentsen, T. J. (2012). Memory modulation in the classroom: Selective enhancement of college examination performance by arousal induced after lecture. Neurobiology of Learning and Memory, 98, 12–16.PubMedCrossRefGoogle Scholar
  36. Nielson, K. A., & Lorber, W. (2009). Enhanced post-learning memory consolidation is influenced by arousal predisposition and emotion regulation but not by stimulus valence or arousal. Neurobiology of Learning and Memory, 92, 70–79.PubMedCrossRefGoogle Scholar
  37. Ochsner, K. N. (2000). Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. Journal of Experimental Psychology: General, 129, 242–261. doi:10.1037/0096-3445.129.2.242 CrossRefGoogle Scholar
  38. Petrides, M. (2007). The orbitofrontal cortex: Novelty, deviation from expectation, and memory. Annals of the New York Academy of Sciences, 1121, 33–53.PubMedCrossRefGoogle Scholar
  39. Rossi, S., Pasqualetti, P., Zito, G., Vecchio, F., Cappa, S. F., Miniussi, C., & Rossini, P. M. (2006). Prefrontal and parietal cortex in human episodic memory: An interference study by repetitive transcranial magnetic stimulation. European Journal of Neuroscience, 23, 793–800. doi:10.1111/j.1460-9568.2006.04600.x PubMedCrossRefGoogle Scholar
  40. Rowe, G., Hirsh, J. B., & Anderson, A. K. (2007). Positive affect increases the breadth of attentional selection. Proceedings of the National Academy of Sciences, 104, 383–388.CrossRefGoogle Scholar
  41. Sakaki, M., Fryer, K., & Mather, M. (2014). Emotion strengthens high-priority memory traces but weakens low-priority memory traces. Psychological Science, 25, 387–395. doi:10.1177/0956797613504784 PubMedCrossRefGoogle Scholar
  42. Sharot, T., & Yonelinas, A. P. (2008). Differential time-dependent effects of emotion on recollective experience and memory for contextual information. Cognition, 106, 538–547.PubMedCrossRefGoogle Scholar
  43. Shigemune, Y., Abe, N., Suzuki, M., Ueno, A., Mori, E., Tashiro, M., & Fujii, T. (2010). Effects of emotion and reward motivation on neural correlates of episodic memory encoding: A PET study. Neuroscience Research, 67, 72–79. doi:10.1016/j.neures.2010.01.003 PubMedCrossRefGoogle Scholar
  44. Simons, J. S., Peers, P. V., Mazuz, Y. S., Berryhill, M. E., & Olson, I. R. (2010). Dissociation between memory accuracy and memory confidence following bilateral parietal lesions. Cerebral Cortex, 20, 479–485. doi:10.1093/cercor/bhp116 PubMedCentralPubMedCrossRefGoogle Scholar
  45. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143–155.PubMedCrossRefGoogle Scholar
  46. Smith, A. P., Henson, R. N., Dolan, R. J., & Rugg, M. D. (2004). fMRI correlates of the episodic retrieval of emotional contexts. NeuroImage, 22, 868–878.PubMedCrossRefGoogle Scholar
  47. Stanislaw, H., & Todorov, N. (1999). Calculation of signal detection theory measures. Behavior Research Methods, Instruments, & Computers, 31, 137–149. doi:10.3758/BF03207704 CrossRefGoogle Scholar
  48. Tamber-Rosenau, B. J., Esterman, M., Chiu, Y. C., & Yantis, S. (2011). Cortical mechanisms of cognitive control for shifting attention in vision and working memory. Journal of Cognitive Neuroscience, 23, 2905–2919.PubMedCentralPubMedCrossRefGoogle Scholar
  49. Todd, R. M., Talmi, D., Schmitz, T. W., Susskind, J., & Anderson, A. K. (2012). Psychophysical and neural evidence for emotion-enhanced perceptual vividness. Journal of Neuroscience, 32, 11201–11212.PubMedCentralPubMedCrossRefGoogle Scholar
  50. Tsukiura, T., & Cabeza, R. (2011). Remembering beauty: Roles of orbitofrontal and hippocampal regions in successful memory encoding of attractive faces. NeuroImage, 54, 653–660.PubMedCentralPubMedCrossRefGoogle Scholar
  51. Vanlessen, N., Rossi, V., De Raedt, R., & Pourtois, G. (2013). Positive emotion broadens attention focus through decreased position-specific spatial encoding in early visual cortex: Evidence from ERPs. Cognitive, Affective, & Behavioral Neuroscience, 13, 60–79.CrossRefGoogle Scholar
  52. Vilberg, K. L., & Rugg, M. D. (2008). Memory retrieval and the parietal cortex: A review of evidence from a dual-process perspective. Neuropsychologia, 46, 1787–1799. doi:10.1016/j.neuropsychologia.2008.01.004 PubMedCentralPubMedCrossRefGoogle Scholar
  53. Vogt, B. A., & Laureys, S. (2005). Posterior cingulate, precuneal and retrosplenial cortices: Cytology and components of the neural network correlates of consciousness. Progress in Brain Research, 150, 205–217.PubMedCentralPubMedCrossRefGoogle Scholar
  54. Wagner, A. D., Shannon, B. J., Kahn, I., & Buckner, R. L. (2005). Parietal lobe contributions to episodic memory retrieval. Trends in Cognitive Sciences, 9, 445–453. doi:10.1016/j.tics.2005.07.001 PubMedCrossRefGoogle Scholar
  55. Warbrick, T., Reske, M., & Shah, N. J. (2013). Do EEG paradigms work in fMRI? Varying task demands in the visual oddball paradigm: Implications for task design and results interpretation. NeuroImage, 77, 177–185.PubMedCrossRefGoogle Scholar
  56. Woolrich, M. (2008). Robust group analysis using outlier inference. NeuroImage, 41, 286–301.PubMedCrossRefGoogle Scholar
  57. Woolrich, M. W., Behrens, T. E., Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2004). Multilevel linear modelling for FMRI group analysis using Bayesian inference. NeuroImage, 21, 1732–1747.PubMedCrossRefGoogle Scholar
  58. Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. NeuroImage, 14, 1370–1386.PubMedCrossRefGoogle Scholar
  59. Yin, X., Zhao, L., Xu, J., Evans, A. C., Fan, L., Ge, H., & Liu, S. (2012). Anatomical substrates of the alerting, orienting and executive control components of attention: Focus on the posterior parietal lobe. PLoS ONE, 7, e50590. doi:10.1371/journal.pone.0050590 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Young, J. J., & Shapiro, M. L. (2011). The orbitofrontal cortex and response selection. Annals of the New York Academy of Sciences, 1239, 25–32.PubMedCrossRefGoogle Scholar
  61. Zhu, X., Wang, X., Parkinson, C., Cai, C., Gao, S., & Hu, P. (2010). Brain activation evoked by erotic films varies with different menstrual phases: An fMRI study. Behavioural Brain Research, 206, 279–285.PubMedCrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2014

Authors and Affiliations

  • Ciara M. Greene
    • 1
    • 2
  • Oliver Flannery
    • 1
  • David Soto
    • 1
  1. 1.Department of Medicine, Division of Brain SciencesImperial College LondonLondonUK
  2. 2.School of Applied PsychologyUniversity College CorkCorkIreland

Personalised recommendations