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Journal of Cognitive Enhancement

, Volume 3, Issue 1, pp 94–103 | Cite as

Exercise and Emotional Memory: a Systematic Review

  • Paul D. LoprinziEmail author
  • Emily Frith
  • Meghan K. Edwards
Mini-Review

Abstract

Memories are often vividly recalled when experienced during an emotional event (i.e., emotional memory). Exercise has been shown to subserve episodic memory function, but its role in influencing emotional memory is less clear. In this systematic review, we discuss the potential underlying mechanisms that subserve emotional memory and summarize an emerging body of research investigating the effects of exercise on emotional memory. We also highlight recommendations for future work in this emerging field of inquiry.

Keywords

Amygdala Cognition Cues Episodic Norepinephrine Perceptual Physical activity 

Notes

Conflict of Interest

The authors declare that they have no conflicts of interest.

References

  1. Bherer, L., Erickson, K. I., & Liu-Ambrose, T. (2013). A review of the effects of physical activity and exercise on cognitive and brain functions in older adults. Journal of Aging Research, 2013, 657508.  https://doi.org/10.1155/2013/657508.Google Scholar
  2. Buchanan, T. W. (2007). Retrieval of emotional memories. Psychological Bulletin, 133(5), 761–779.  https://doi.org/10.1037/0033-2909.133.5.761.Google Scholar
  3. Buchel, C., & Dolan, R. J. (2000). Classical fear conditioning in functional neuroimaging. Current Opinion in Neurobiology, 10(2), 219–223.Google Scholar
  4. Cahill, L. (2003). Similar neural mechanisms for emotion-induced memory impairment and enhancement. Proceedings of the National Academy of Sciences of the United States of America, 100(23), 13123–13124.  https://doi.org/10.1073/pnas.2335833100.Google Scholar
  5. Cahill, L., Babinsky, R., Markowitsch, H. J., & McGaugh, J. L. (1995). The amygdala and emotional memory. Nature, 377(6547), 295–296.  https://doi.org/10.1038/377295a0.Google Scholar
  6. Cahill, L., & McGaugh, J. L. (1998). Mechanisms of emotional arousal and lasting declarative memory. Trends in Neurosciences, 21(7), 294–299.Google Scholar
  7. Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994). Beta-adrenergic activation and memory for emotional events. Nature, 371(6499), 702–704.  https://doi.org/10.1038/371702a0.Google Scholar
  8. Canli, T., Desmond, J. E., Zhao, Z., & Gabrieli, J. D. (2002). Sex differences in the neural basis of emotional memories. Proceedings of the National Academy of Sciences of the United States of America, 99(16), 10789–10794.  https://doi.org/10.1073/pnas.162356599.Google Scholar
  9. Canli, T., Zhao, Z., Brewer, J., Gabrieli, J. D., & Cahill, L. (2000). Event-related activation in the human amygdala associates with later memory for individual emotional experience. Journal of Neuroscience, 20(19), RC99.Google Scholar
  10. Clark, K. B., Naritoku, D. K., Smith, D. C., Browning, R. A., & Jensen, R. A. (1999). Enhanced recognition memory following vagus nerve stimulation in human subjects. Nature Neuroscience, 2(1), 94–98.  https://doi.org/10.1038/4600.Google Scholar
  11. Coyle, J. T. (1977). Biochemical aspects of neurotransmission in the developing brain. International Review of Neurobiology, 20, 65–103.Google Scholar
  12. Ebada, M. E., Latif, L. M., Kendall, D. A., & Pardon, M. C. (2014). Corticosterone protects against memory impairments and reduced hippocampal BDNF levels induced by a chronic low dose of ethanol in C57BL/6J mice. Romanian Journal of Morphology and Embryology, 55(4), 1303–1316.Google Scholar
  13. Ferry, B., & McGaugh, J. L. (1999). Clenbuterol administration into the basolateral amygdala post-training enhances retention in an inhibitory avoidance task. Neurobiology of Learning and Memory, 72(1), 8–12.  https://doi.org/10.1006/nlme.1998.3904.Google Scholar
  14. Fryer, S., Hillier, S., Dickson, T., Draper, N., Stoner, L., Winter, D., et al. (2012). Capillary cortisol sampling during high-intensity exercise. International Journal of Sports Medicine, 33(10), 842–845.  https://doi.org/10.1055/s-0032-1311584.Google Scholar
  15. Galvez, R., Mesches, M. H., & McGaugh, J. L. (1996). Norepinephrine release in the amygdala in response to footshock stimulation. Neurobiology of Learning and Memory, 66(3), 253–257.  https://doi.org/10.1006/nlme.1996.0067.Google Scholar
  16. Gold, P. E. (1995). Role of glucose in regulating the brain and cognition. American Journal of Clinical Nutrition, 61(4 Suppl), 987S–995S.Google Scholar
  17. Gomez-Pinilla, F., & Hillman, C. (2013). The influence of exercise on cognitive abilities. Comprehensive Physiology, 3(1), 403–428.  https://doi.org/10.1002/cphy.c110063.Google Scholar
  18. Hajisoltani, R., Rashidy-Pour, A., Vafaei, A. A., Ghaderdoost, B., Bandegi, A. R., & Motamedi, F. (2011). The glucocorticoid system is required for the voluntary exercise-induced enhancement of learning and memory in rats. Behavioural Brain Research, 219(1), 75–81.  https://doi.org/10.1016/j.bbr.2010.12.005.Google Scholar
  19. Hamann, S. (2001). Cognitive and neural mechanisms of emotional memory. Trends in Cognitive Sciences, 5(9), 394–400.Google Scholar
  20. Hamann, S. B., Ely, T. D., Grafton, S. T., & Kilts, C. D. (1999). Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience, 2(3), 289–293.  https://doi.org/10.1038/6404.Google Scholar
  21. Hatfield, T., Spanis, C., & McGaugh, J. L. (1999). Response of amygdalar norepinephrine to footshock and GABAergic drugs using in vivo microdialysis and HPLC. Brain Research, 835(2), 340–345.Google Scholar
  22. Howland, R. H. (2014). Vagus nerve stimulation. Current Behavioral Neuroscience Reports, 1(2), 64–73.  https://doi.org/10.1007/s40473-014-0010-5.Google Scholar
  23. Hu, H., Real, E., Takamiya, K., Kang, M. G., Ledoux, J., Huganir, R. L., & Malinow, R. (2007). Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell, 131(1), 160–173.  https://doi.org/10.1016/j.cell.2007.09.017.Google Scholar
  24. Ida, Y., Tanaka, M., Tsuda, A., Tsujimaru, S., & Nagasaki, N. (1985). Attenuating effect of diazepam on stress-induced increases in noradrenaline turnover in specific brain regions of rats: Antagonism by Ro 15-1788. Life Sciences, 37(26), 2491–2498.Google Scholar
  25. Ikegaya, Y., Nakanishi, K., Saito, H., & Abe, K. (1997). Amygdala beta-noradrenergic influence on hippocampal long-term potentiation in vivo. Neuroreport, 8(14), 3143–3146.Google Scholar
  26. Iwai, E., & Yukie, M. (1987). Amygdalofugal and amygdalopetal connections with modality-specific visual cortical areas in macaques (Macaca fuscata, M. Mulatta, and M. Fascicularis). The Journal of Comparative Neurology, 261(3), 362–387.  https://doi.org/10.1002/cne.902610304.Google Scholar
  27. Jones, E. G., & Powell, T. P. (1970). An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain, 93(4), 793–820.Google Scholar
  28. Kensinger, E. A., & Corkin, S. (2003). Memory enhancement for emotional words: Are emotional words more vividly remembered than neutral words? Memory & Cognition, 31(8), 1169–1180.Google Scholar
  29. Keyan, D., & Bryant, R. A. (2017a). Acute physical exercise in humans enhances reconsolidation of emotional memories. Psychoneuroendocrinology, 86, 144–151.  https://doi.org/10.1016/j.psyneuen.2017.09.019.Google Scholar
  30. Keyan, D., & Bryant, R. A. (2017b). Brief exercise enhances intrusive memories of traumatic stimuli. Neurobiology of Learning and Memory, 141, 9–13.  https://doi.org/10.1016/j.nlm.2017.03.012.Google Scholar
  31. Keyan, D., & Bryant, R. A. (2017c). Role of BDNF val66met polymorphism in modulating exercised-induced emotional memories. Psychoneuroendocrinology, 77, 150–157.  https://doi.org/10.1016/j.psyneuen.2016.12.013.Google Scholar
  32. Labban, J. D., & Etnier, J. L. (2011). Effects of acute exercise on long-term memory. Research Quarterly for Exercise and Sport, 82(4), 712–721.  https://doi.org/10.1080/02701367.2011.10599808.Google Scholar
  33. Lanier, W. L. (1997). The afferentation theory of cerebral arousal. Neuroanesthesia, 27–38.Google Scholar
  34. Lanier, W. L., Iaizzo, P. A., & Milde, J. H. (1989). Cerebral function and muscle afferent activity following intravenous succinylcholine in dogs anesthetized with halothane: The effects of pretreatment with a defasciculating dose of pancuronium. Anesthesiology, 71(1), 87–95.Google Scholar
  35. Lanier, W. L., Iaizzo, P. A., Milde, J. H., & Sharbrough, F. W. (1994). The cerebral and systemic effects of movement in response to a noxious stimulus in lightly anesthetized dogs. Possible modulation of cerebral function by muscle afferents. Anesthesiology, 80(2), 392–401.Google Scholar
  36. LeDoux, J. E. (1992). Brain mechanisms of emotion and emotional learning. Current Opinion in Neurobiology, 2(2), 191–197.Google Scholar
  37. LeDoux, J. E. (1993). Emotional memory systems in the brain. Behavioural Brain Research, 58(1–2), 69–79.Google Scholar
  38. LeDoux, J. E., Farb, C., & Ruggiero, D. A. (1990). Topographic organization of neurons in the acoustic thalamus that project to the amygdala. Journal of Neuroscience, 10(4), 1043–1054.Google Scholar
  39. Loizou, L. A. (1969). Projections of the nucleus locus coeruleus in the albino rat. Brain Research, 15(2), 563–566.Google Scholar
  40. Lupien, S. J., & McEwen, B. S. (1997). The acute effects of corticosteroids on cognition: Integration of animal and human model studies. Brain Research. Brain Research Reviews, 24(1), 1–27.Google Scholar
  41. Magnie, M. N., Bermon, S., Martin, F., Madany-Lounis, M., Suisse, G., Muhammad, W., & Dolisi, C. (2000). P300, N400, aerobic fitness, and maximal aerobic exercise. Psychophysiology, 37(3), 369–377.Google Scholar
  42. Markowitsch, H. J., Calabrese, P., Wurker, M., Durwen, H. F., Kessler, J., Babinsky, R., et al. (1994). The amygdala's contribution to memory--a study on two patients with Urbach-Wiethe disease. Neuroreport, 5(11), 1349–1352.Google Scholar
  43. Marks, W. N., Fenton, E. Y., Guskjolen, A. J., & Kalynchuk, L. E. (2015). The effect of chronic corticosterone on fear learning and memory depends on dose and the testing protocol. Neuroscience, 289, 324–333.  https://doi.org/10.1016/j.neuroscience.2015.01.011.Google Scholar
  44. McGaugh, J. L. (2000). Memory--a century of consolidation. Science, 287(5451), 248–251.Google Scholar
  45. Michalak, J., Rohde, K., & Troje, N. F. (2015). How we walk affects what we remember: Gait modifications through biofeedback change negative affective memory bias. Journal of Behavior Therapy and Experimental Psychiatry, 46, 121–125.  https://doi.org/10.1016/j.jbtep.2014.09.004.Google Scholar
  46. Pacak, K., Palkovits, M., Kvetnansky, R., Fukuhara, K., Armando, I., Kopin, I. J., & Goldstein, D. S. (1993). Effects of single or repeated immobilization on release of norepinephrine and its metabolites in the central nucleus of the amygdala in conscious rats. Neuroendocrinology, 57(4), 626–633.  https://doi.org/10.1159/000126417.Google Scholar
  47. Phelps, E. A., LaBar, K. S., & Spencer, D. D. (1997). Memory for emotional words following unilateral temporal lobectomy. Brain and Cognition, 35(1), 85–109.  https://doi.org/10.1006/brcg.1997.0929.Google Scholar
  48. Phelps, E. A., & Sharot, T. (2008). How (and why) emotion enhances the subjective sense of recollection. Current Directions in Psychological Science, 17(2), 147–152.  https://doi.org/10.1111/j.1467-8721.2008.00565.x.Google Scholar
  49. Reisberg, D., & Heuer, F. (1992). Remembering the details of emotional events. In E. Winograd & U. Neisser (Eds.), Affect and Accuracy in Recall: Studies of 'Flashbulb' Memories (pp. 162–190). Cambridge: Cambridge University Press.Google Scholar
  50. Schacter, D. L. (1987). Implicit memory: History and current status. Journal of Experimental Psychology Learning Memory and Cognition, 13, 510–518.Google Scholar
  51. Scudder, M. R., Drollette, E. S., Pontifex, M. B., & Hillman, C. H. (2012). Neuroelectric indices of goal maintenance following a single bout of physical activity. Biological Psychology, 89(2), 528–531.  https://doi.org/10.1016/j.biopsycho.2011.12.009.Google Scholar
  52. Segal, S. K., Cotman, C. W., & Cahill, L. F. (2012). Exercise-induced noradrenergic activation enhances memory consolidation in both normal aging and patients with amnestic mild cognitive impairment. Journal of Alzheimer's Disease, 32(4), 1011–1018.  https://doi.org/10.3233/JAD-2012-121078.Google Scholar
  53. Sherwin, R. S., & Sacca, L. (1984). Effect of epinephrine on glucose metabolism in humans: Contribution of the liver. American Journal of Physiology, 247(2 Pt 1), E157–E165.Google Scholar
  54. Siette, J., Reichelt, A. C., & Westbrook, R. F. (2014). A bout of voluntary running enhances context conditioned fear, its extinction, and its reconsolidation. Learning & Memory, 21(2), 73–81.  https://doi.org/10.1101/lm.032557.113.Google Scholar
  55. Smythies, J. (2005). Section III. The norepinephrine system. International Review of Neurobiology, 64, 173–211.  https://doi.org/10.1016/S0074-7742(05)64003-2.Google Scholar
  56. Tanaka, T., Yokoo, H., Mizoguchi, K., Yoshida, M., Tsuda, A., & Tanaka, M. (1991). Noradrenaline release in the rat amygdala is increased by stress: Studies with intracerebral microdialysis. Brain Research, 544(1), 174–176.Google Scholar
  57. Thomas, M. J., Moody, T. D., Makhinson, M., & O'Dell, T. J. (1996). Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron, 17(3), 475–482.Google Scholar
  58. Tully, K., & Bolshakov, V. Y. (2010). Emotional enhancement of memory: How norepinephrine enables synaptic plasticity. Molecular Brain, 3, 15.  https://doi.org/10.1186/1756-6606-3-15.Google Scholar
  59. Turner, B. H., Mishkin, M., & Knapp, M. (1980). Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. Journal of Comparative Neurology, 191(4), 515–543.  https://doi.org/10.1002/cne.901910402.Google Scholar
  60. Weinberg, L., Hasni, A., Shinohara, M., & Duarte, A. (2014). A single bout of resistance exercise can enhance episodic memory performance. Acta Psychologica, 153, 13–19.  https://doi.org/10.1016/j.actpsy.2014.06.011.Google Scholar
  61. Yang, H. W., Lin, Y. W., Yen, C. D., & Min, M. Y. (2002). Change in bi-directional plasticity at CA1 synapses in hippocampal slices taken from 6-hydroxydopamine-treated rats: The role of endogenous norepinephrine. European Journal of Neuroscience, 16(6), 1117–1128.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Paul D. Loprinzi
    • 1
    Email author
  • Emily Frith
    • 1
  • Meghan K. Edwards
    • 1
  1. 1.Physical Activity Epidemiology Laboratory, Exercise Psychology Laboratory, Department of Health, Exercise Science and Recreation ManagementThe University of MississippiOxfordUSA

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