Experimental Brain Research

, Volume 208, Issue 4, pp 507–517 | Cite as

Offline consolidation of procedural skill learning is enhanced by negative emotional content

  • Amir Homayoun Javadi
  • Vincent Walsh
  • Penelope A. Lewis
Research Article

Abstract

It is now well established that both procedural skills and episodic memories consolidate across periods of offline retention, and most particularly across periods of sleep. Such consolidation has been demonstrated to be more marked for emotional than for neutral episodes, but the interaction between emotionality and the offline consolidation of procedural skills has yet to be investigated. Here, we address this issue by examining the impact of an emotional background context at encoding upon the subsequent consolidation of mirror tracing, a well-studied procedural skill. We also consider the importance of sleep for such consolidation by manipulating the retention interval (over a day, overnight, or over 24 h containing normal sleep). Our data show significantly greater offline improvements in the accuracy of mirror tracing when negative emotional content is present during the training phase when compared to when neutral or positive content is present. Furthermore, consolidation across a night of sleep is associated with faster and more accurate performance than consolidation across a day of wakefulness. These novel findings show that the emotional context in which a procedural skill is learned can impact upon subsequent offline consolidation.

Keywords

Consolidation Procedural memory Procedural learning Emotion Sleep 

Notes

Acknowledgments

We would like to thank Iroise Dumontheil for critical reading of the manuscript and Bahador Bahrami for technical assistance. We would also like to thank the two anonymous reviewers for their constructive comments. PAL is supported by a BBSRC New Investigator award [BB/F003048/1].

References

  1. Adams JA (1987) Historical review and appraisal of research on the learning, retention, and transfer of human motor skills. Psychol Bull 101:41–74CrossRefGoogle Scholar
  2. Adolphs R (2008) Fear, faces, and the human amygdala. Curr Opin Neurobiol 18:166–172CrossRefPubMedGoogle Scholar
  3. Adolphs R, Tranel D, Damasio H, Damasio A (1995) Fear and the human amygdala. J Neurosci 15:5879–5891PubMedGoogle Scholar
  4. Bradley M, Lang P (1994) Measuring emotion: the self-assessment manikin and the semantic differential. J Behav Ther Exp Psychiatry 25:49–59CrossRefPubMedGoogle Scholar
  5. Bremner J, Soufer R, McCarthy G, Delaney R, Staib L, Duncan J, Charney D (2001) Gender differences in cognitive and neural correlates of remembrance of emotional words. Psychopharmacol Bull 35:55PubMedGoogle Scholar
  6. Brown R, Kulik J (1977) Flashbulb memories. Cognition 5:73–99CrossRefGoogle Scholar
  7. Burton L, Rabin L, Vardy S, Frohlich J, Wyatt G, Dimitri D, Constante S, Guterman E (2004) Gender differences in implicit and explicit memory for affective passages. Brain Cogn 54:218–224CrossRefPubMedGoogle Scholar
  8. Cahill L (2000) Neurobiological mechanisms of emotionally influenced, long-term memory. Prog Brain Res 126:29CrossRefPubMedGoogle Scholar
  9. Cahill L, Alkire M (2003) Epinephrine enhancement of human memory consolidation: interaction with arousal at encoding. Neurobiol Learn Mem 79:194–198CrossRefPubMedGoogle Scholar
  10. Cahill L, Gorski L, Belcher A, Huynh Q (2004) The influence of sex versus sex-related traits on long-term memory for gist and detail from an emotional story. Conscious Cogn 13:391–400CrossRefPubMedGoogle Scholar
  11. Chikama M, McFarland N, Amaral D, Haber S (1997) Insular cortical projections to functional regions of the striatum correlate with cortical cytoarchitectonic organization in the primate. J Neurosci 17:9686–9705PubMedGoogle Scholar
  12. Cohen D, Robertson E (2007) Motor sequence consolidation: constrained by critical time windows or competing components. Exp Brain Res 177:440–446CrossRefPubMedGoogle Scholar
  13. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Lüthi A (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757–771CrossRefPubMedGoogle Scholar
  14. Ferry A, Ongur D, An X, Price J (2000) Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J Comp Neurol 425:447–470CrossRefPubMedGoogle Scholar
  15. Fischer S, Hallschmid M, Elsner AL, Born J (2002) Sleep forms memory for finger skills. Proc Natl Acad Sci 99:11987–11991CrossRefPubMedGoogle Scholar
  16. Fogel S, Smith C, Cote K (2007) Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav Brain Res 180:48–61CrossRefPubMedGoogle Scholar
  17. Gabrieli JDE, Corkin S, Mickel SF, Growdon JH (1993) Intact acquisition and long-term retention of mirror-tracing skill in Alzheimer’s disease and in global amnesia. Behav Neurosci 107:899CrossRefPubMedGoogle Scholar
  18. Gabrieli JDE, Stebbins GT, Singh J, Willingham DB, Goetz CG (1997) Intact mirror-tracing and impaired rotary-pursuit skill learning in patients with Huntington’s disease: evidence for dissociable memory systems in skill learning. Neuropsychology 11:272–281CrossRefPubMedGoogle Scholar
  19. Gais S, Born J (2004) Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci USA 101:2140–2144CrossRefPubMedGoogle Scholar
  20. Gazzaniga M (2004) The cognitive neurosciences. Bradford Books, Cambridge, MAGoogle Scholar
  21. Göder R, Boigs M, Braun S, Friege L, Fritzer G, Aldenhoff J, Hinze-Selch D (2004) Impairment of visuospatial memory is associated with decreased slow wave sleep in schizophrenia. J Psychiatr Res 38:591–599CrossRefPubMedGoogle Scholar
  22. Göder R, Scharffetter F, Aldenhoff J, Fritzer G (2007) Visual declarative memory is associated with non-rapid eye movement sleep and sleep cycles in patients with chronic non-restorative sleep. Sleep Med 8:503–508CrossRefPubMedGoogle Scholar
  23. Groenewegen H, Berendse H (1994) Anatomical relationships between the prefrontal cortex and the basal ganglia in the rat. In: Thierry A-M (ed) Motor and cognitive functions of the prefrontal cortex. Springer, Berlin, pp 51–77Google Scholar
  24. Gujar N, McDonald S, Nishida M, Walker M (2010) A role for REM sleep in recalibrating the sensitivity of the human brain to specific emotions. Cereb Cortex. doi:10.1093/cercor/bhq064
  25. Haber S (2003) Integrating cognition and motivation into the basal ganglia pathways of action. In: Bedard MA, Agid Y, Chouinard S, Fahn S, Korczyn AD, Lesperance P (eds) Mental and behavioral dysfunction in movement disorders. Humana Press, New Jersey, pp 35–50Google Scholar
  26. Haber S, Kunishio K, Mizobuchi M, Lynd-Balta E (1995) The orbital and medial prefrontal circuit through the primate basal ganglia. J Neurosci 15:4851–4867PubMedGoogle Scholar
  27. Haegelen C, Rouaud T, Darnault P, Morandi X (2009) The subthalamic nucleus is a key-structure of limbic basal ganglia functions. Med Hypotheses 72:421–426CrossRefPubMedGoogle Scholar
  28. Hamann S, Canli T (2004) Individual differences in emotion processing. Curr Opin Neurobiol 14:233–238CrossRefPubMedGoogle Scholar
  29. Heimer L, Switzer R, Hoesen G (1982) Ventral striatum and ventral pallidum: components of the motor system. Trends Neurosci 5:83087CrossRefGoogle Scholar
  30. Hoddes E, Zarcone V, Smythe H, Phillips R, Dement WC (1973) Quantification of sleepiness: a new approach. Psychophysiology 10:431–436CrossRefPubMedGoogle Scholar
  31. Hornung O, Regen F, Danker-Hopfe H, Schredl M, Heuser I (2007) The relationship between REM sleep and memory consolidation in old age and effects of cholinergic medication. Biol Psychiatry 61:750–757CrossRefPubMedGoogle Scholar
  32. Hornung O, Regen F, Warnstedt C, Anghelescu I, Danker-Hopfe H, Heuser I, Lammers C (2008) Declarative and procedural memory consolidation during sleep in patients with borderline personality disorder. J Psychiatr Res 42:653–658CrossRefPubMedGoogle Scholar
  33. Kandel ER, Schwartz JH, Jessell TM (2000) Principles of neural science. McGraw-Hill, Health Professions Division, New YorkGoogle Scholar
  34. Kensinger E, Garoff-Eaton R, Schacter D (2006) Memory for specific visual details can be enhanced by negative arousing content. J Mem Lang 54:99–112CrossRefGoogle Scholar
  35. Kleinsmith L, Kaplan S (1963) Paired-associate learning as a function of arousal and interpolated interval. J Exp Psychol 65:190–193CrossRefPubMedGoogle Scholar
  36. Kloepfer C, Riemann D, Nofzinger E, Feige B, Unterrainer J, O’Hara R, Sorichter S, Nissen C (2009) Memory before and after sleep in patients with moderate obstructive sleep apnea. J Clin Sleep Med 5:540PubMedGoogle Scholar
  37. LaBar K, Cabeza R (2006) Cognitive neuroscience of emotional memory. Nat Rev Neurosci 7:54–64CrossRefPubMedGoogle Scholar
  38. LaBar K, Phelps E (1998) Arousal-mediated memory consolidation: role of the medial temporal lobe in humans. Psychol Sci 9:490–493CrossRefGoogle Scholar
  39. Laureys S, Peigneux P, Perrin F, Maquet P (2002) Sleep and motor skill learning. Neuron 35:5–7CrossRefPubMedGoogle Scholar
  40. LeDoux J (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184CrossRefPubMedGoogle Scholar
  41. Levonian E (1972) Retention over time in relation to arousal during learning: an explanation of discrepant results. Acta Psychol 36:290–321CrossRefGoogle Scholar
  42. Maddock R (1999) The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain. Trends Neurosci 22:310–316CrossRefPubMedGoogle Scholar
  43. Maquet P, Laureys S, Peigneux P, Fuchs S, Petiau C, Phillips C, Aerts J, Del Fiore G, Degueldre C, Meulemans T, Luxen A, Franck G, Van Der Linden M, Smith C, Cleeremans A (2000) Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci 3:831–836CrossRefPubMedGoogle Scholar
  44. Maren S (2008) Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. Eur J Neurosci 28:1661CrossRefPubMedGoogle Scholar
  45. Marshall L, Molle M, Hallschmid M, Born J (2004) Transcranial direct current stimulation during sleep improves declarative memory. J Neurosci 24:9985–9992CrossRefPubMedGoogle Scholar
  46. McGaugh J (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1–28CrossRefPubMedGoogle Scholar
  47. McGaugh J, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205–210CrossRefPubMedGoogle Scholar
  48. Milner B (1962) Les troubles de la memoire accompagnant des lesions hippocampiques bilaterales. In: Passant P (ed) Centre de la Recherche Scientifique. Physiologie de l’hippocampe. Paris, pp 257–272Google Scholar
  49. Morecraft R, van Hoesen G (1992) Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: evidence for somatotopy in areas 24c and 23c. J Comp Neurol 322(4):471–489CrossRefPubMedGoogle Scholar
  50. Morecraft R, Van Hoesen G (1998) Convergence of limbic input to the cingulate motor cortex in the rhesus monkey. Brain Res Bull 45:209–232CrossRefPubMedGoogle Scholar
  51. Nishida M, Walker M (2007) Daytime naps, motor memory consolidation and regionally specific sleep spindles. PloS One 2:e341CrossRefPubMedGoogle Scholar
  52. Nishida M, Pearsall J, Buckner R, Walker M (2009) REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb Cortex 19:1158CrossRefPubMedGoogle Scholar
  53. Nissen C, Kloepfer C, Nofzinger E, Feige B, Voderholzer U, Riemann D (2006) Impaired sleep-related memory consolidation in primary insomnia—a pilot study. Sleep 29:1068–1073PubMedGoogle Scholar
  54. Nissen C, Kloepfer C, Feige B, Piosczyk H, Spiegelhalder K, Voderholzer U, Riemann D (2010) Sleep-related memory consolidation in primary insomnia. J Sleep Res. doi:10.1111/j.1365-2869.2010.00872.x
  55. Ochsner K (2000) Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. J Exp Psychol Gen 129:242–261CrossRefPubMedGoogle Scholar
  56. Payne JD, Stickgold R, Swanberg K, Kensinger EA (2008) Sleep preferentially enhances memory for emotional components of scenes. Psychol Sci 19(8):781–788CrossRefPubMedGoogle Scholar
  57. Phelps E (2004) Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 14:198–202CrossRefPubMedGoogle Scholar
  58. Plihal W, Born J (1997) Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci 9:534–547CrossRefGoogle Scholar
  59. Plihal W, Pietrowsky R, Born J (1999) Dexamethasone blocks sleep induced improvement of declarative memory. Psychoneuroendocrinology 24:313–331CrossRefPubMedGoogle Scholar
  60. Prehn-Kristensen A, Göder R, Chirobeja S, Breßmann I, Ferstl R, Baving L (2009) Sleep in children enhances preferentially emotional declarative but not procedural memories. J Exp Child Psychol 104:132–139CrossRefPubMedGoogle Scholar
  61. Press D, Casement M, Pascual-Leone A, Robertson E (2005) The time course of off-line motor sequence learning. Cogn Brain Res 25:375–378CrossRefGoogle Scholar
  62. Richardson M, Strange B, Dolan R (2004) Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nat Neurosci 7:278–285CrossRefPubMedGoogle Scholar
  63. Robertson E, Cohen D (2006) Understanding consolidation through the architecture of memories. Neuroscientist 12:261CrossRefPubMedGoogle Scholar
  64. Robertson E, Pascual-Leone A, Miall R (2004) Current concepts in procedural consolidation. Nat Rev Neurosci 5:576–582CrossRefPubMedGoogle Scholar
  65. Roozendaal B, McEwen B, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10:423–433CrossRefPubMedGoogle Scholar
  66. Rouleau I, Decary A, Chicoine A, Montplaisir J (2002) Procedural skill learning in obstructive sleep apnea syndrome. Sleep 25:401–411PubMedGoogle Scholar
  67. Sah P, Westbrook R, Luthi A (2008) Fear conditioning and long-term potentiation in the amygdala what really is the connection? Ann N Y Acad Sci 1129:88CrossRefPubMedGoogle Scholar
  68. Sanes JN, Dimitrov B, Hallett M (1990) Motor learning in patients with cerebellar dysfunction. Brain 113:103CrossRefPubMedGoogle Scholar
  69. Schabus M, Hödlmoser K, Gruber G, Sauter C, Anderer P, Klösch G, Parapatics S, Saletu B, Klimesch W, Zeitlhofer J (2006) Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur J Neurosci 23:1738–1746CrossRefPubMedGoogle Scholar
  70. Seeck-Hirschner M, Baier P, Sever S, Buschbacher A, Aldenhoff J, Göder R (2010) Effects of daytime naps on procedural and declarative memory in patients with schizophrenia. J Psychiatr Res 44:42–47CrossRefPubMedGoogle Scholar
  71. Seymour B, Dolan R (2008) Emotion, decision making, and the amygdala. Neuron 58:662–671CrossRefPubMedGoogle Scholar
  72. Sharot T, Phelps E (2004) How arousal modulates memory: disentangling the effects of attention and retention. Cogn Affect Behav Neurosci 4:294–306CrossRefPubMedGoogle Scholar
  73. Snoddy GS (1920) An experimental analysis of a case of trial and error learning in the human subject. Psychol Rev 124:1–78Google Scholar
  74. Sterpenich V, Albouy G, Boly M, Vandewalle G, Darsaud A, Balteau E, Dang-Vu TT, Desseilles M, D’Argembeau A, Gais S, Rauchs G, Schabus M, Degueldre C, Luxen A, Collette F, Maquet P (2007) Sleep-related hippocampo-cortical interplay during emotional memory recollection. PLoS Biol 5:e282CrossRefPubMedGoogle Scholar
  75. Stickgold R, James LT, Hobson JA (2000) Visual discrimination learning requires sleep after training. Nat Neurosci 3:1237–1238CrossRefPubMedGoogle Scholar
  76. Tamaki M, Matsuoka T, Nittono H, Hori T (2008) Fast sleep spindle (13–15 Hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep 31:204PubMedGoogle Scholar
  77. van der Helm E, Gujar N, Walker M (2010) Sleep deprivation impairs the accurate recognition of human emotions. Sleep 33:335–342PubMedGoogle Scholar
  78. Wagner U, Gais S, Born J (2001) Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn Mem 8:112–119CrossRefPubMedGoogle Scholar
  79. Walker M (2009) The Role of Sleep in Cognition and Emotion. Ann N Y Acad Sci 1156:168–197CrossRefPubMedGoogle Scholar
  80. Walker M, Stickgold R (2004) Sleep-dependent learning and memory consolidation. Neuron 44:121–133CrossRefPubMedGoogle Scholar
  81. Walker E, Tarte R (1963) Memory storage as a function of arousal and time with homogeneous and heterogeneous lists. J Verbal Learn Verbal Behav 2:113–119CrossRefGoogle Scholar
  82. Walker M, Brakefield T, Morgan A, Hobson J, Stickgold R (2002) Practice with sleep makes perfect sleep-dependent motor skill learning. Neuron 35:205–211CrossRefPubMedGoogle Scholar
  83. Zimmermann P, Fimm B (1995) Test for attentional performance (TAP). PsyTest, Herzogenrath, GermanyGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Amir Homayoun Javadi
    • 1
  • Vincent Walsh
    • 1
  • Penelope A. Lewis
    • 1
    • 2
  1. 1.Institute of Cognitive NeuroscienceUniversity College LondonLondonUK
  2. 2.Neuroscience of Aphasia Research UnitThe University of ManchesterManchesterUK

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