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Experimental Brain Research

, Volume 169, Issue 3, pp 417–426 | Cite as

Two waves of a long-lasting aftereffect of prism adaptation measured over 7 days

  • Y. HatadaEmail author
  • R.C. Miall
  • Y. Rossetti
Research Article

Abstract

Prism adaptation is a useful paradigm to study the integration and reorganization of various sensory modalities involved in sensory–motor tasks. By prolonging the prismatic aftereffect and well-timed observation, we aimed to dissociate the components and mechanisms involved in human prism adaptation by their differential decay and development time courses. Here, we show that a single session of prism adaptation training, combining small increments of prism strength below the subjects’ awareness threshold, during a pointing task with a free walk session with total prism exposure duration of 75 min, generated a surprisingly long-lasting aftereffect. The aftereffect was measured by the magnitude of the proprioceptive shift (assessed by straight-ahead pointing in the dark) for 7 days. An aftereffect was observed, which lasted for more than 6 days, by a single prism adaptation session. The aftereffect did not decay gradually. Unlike previous descriptions, the aftereffect showed two separate time-courses of decay and increase. After a significant initial decay within 6 h, the aftereffect increased again from 1 day up to 3 days. The novel decay and delayed development profile of this adaptation aftereffect suggests two separate underlying neural mechanisms with different time scales. Our experimental paradigms promise to reveal directly the temporal characteristics of early versus late long-term neural plasticity in complex human adaptive behavior.

Keywords

Prism adaptation Aftereffect Visuo–motor Sensory–motor Plasticity 

Notes

Acknowledgements

The authors wish to thank the subjects who participated for this experiment for their patience; A. Koene, S. Lin, C. McManus, C. Michel, L. Pisella, G. Redding, P. Salin for their suggestions and constructive criticisms and P. Revol, C. Urquizar for their technical help. This work was supported by funds from INSERM PROGRES to YR.

References

  1. Baizer JS, Kralj-Hans I, Glickstein M (1999) Cerebellar lesions and prism adaptation in macaque monkeys. J Neurophysiol 81:1960–1965PubMedGoogle Scholar
  2. Boyden ES, Katoh A, Raymond JL (2004) Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci 27:581–609PubMedCrossRefGoogle Scholar
  3. Butler AJ, Fink GR, Dohle C, Wunderlich G, Tellmann L, Seitz RJ, Zilles K, Freund HJ (2004) Neural mechanisms underlying reaching for remembered targets cued kinesthetically or visually in left or right hemispace. Hum Brain Mapp 21:165–177PubMedCrossRefGoogle Scholar
  4. Caithness G, Osu R, Bays P, Chase H, Klassen J, Kawato M, Wolpert DM, Flanagan JR (2004) Failure to consolidate the consolidation theory of learning for sensorimotor adaptation tasks. J Neurosci 24:8662–8671PubMedCrossRefGoogle Scholar
  5. Calabria M, Michel C, Honoré J, Guillaume A, Pisella L, Luauté, Rode G, Boisson D, Rossetti Y (2004) Prism adaptation and the lack of awareness in spatial neglect. European Congress of Neuropsychology, 18–20 April, ModenaGoogle Scholar
  6. Choe CS, Welch RB (1974) Variables affecting the intermanual transfer and decay of prism adaptation. J Exp Pshychol 102:1076–1084CrossRefGoogle Scholar
  7. Chklovskii DB, Mel BW, Svoboda K (2004) Cortical rewiring and information storage. Nature 431:782–788PubMedCrossRefGoogle Scholar
  8. Clower DM, Hoffman JM, Votaw JR, Faber TL, Woods RP, Alexander GE (1996) Role of posterior parietal cortex in the recalibration of visually guided reaching. Nature 383:618–621PubMedCrossRefGoogle Scholar
  9. Clower DM, West RA, Lynch JC, Strick PL (2001) The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci 21:6283–6291PubMedGoogle Scholar
  10. Clower DM, Dum RP, Strick PL (2005) Basal ganglia and cerebellar inputs to ‘AIP’. Cereb Cortex 15:913–920 (Epub 2004 Sep 30)Google Scholar
  11. Colent C, Pisella L, Bernieri C, Rode G, Rossetti Y (2000) Cognitive bias induced by visuo-motor adaptation to prisms: a simulation of unilateral neglect in normal individuals? Neuroreport 11:1899–1902PubMedCrossRefGoogle Scholar
  12. Farne A, Rossetti Y, Toniolo S, Ladavas E (2002) Ameliorating neglect with prism adaptation: visuo-manual and visuo-verbal measures. Neuropsychologia 40:718–729PubMedCrossRefGoogle Scholar
  13. Goedert KM, Willingham DB (2002) Patterns of interference in sequence learning and prism adaptation inconsistent with the consolidation hypothesis. Learn Mem 9:279–292PubMedCrossRefGoogle Scholar
  14. Goldberg, Taub E, Berman AJ, et al (1967) Decay of prism after-effect and interlimb transfer of adaptation. Paper presented at the meeting of Eastern Psychological Association, Boston, AprilGoogle Scholar
  15. Hamilton CR, Bossom J (1964) Decay of prism aftereffects. J Exp Psychol 67:148–150PubMedCrossRefGoogle Scholar
  16. Hatada Y, Rossetti Y (2004a) Long-lasting prism-adaptation aftereffects: Shift in open-loop midsagittal pointing involves more than just visual and proprioceptive components. Perception 33(Suppl):140Google Scholar
  17. Hatada Y, Rossetti Y (2004b) Prism adaptation generates a very long-lasting directionally biased proprioceptive shift in healthy subjects. Soc Neurosci Abstr 524.12Google Scholar
  18. Hatada Y, Wu F, Silverman R, Schacher S, Goldberg DJ (1999) En passant synaptic varicosities form directly from growth cones by transient cessation of growth cone advance but not of actin-based motility. J Neurobiol 41:242–251PubMedCrossRefGoogle Scholar
  19. Hatada Y, Wu F, Sun ZY, Schacher S, Goldberg DJ (2000) Presynaptic morphological changes associated with long-term synaptic facilitation are triggered by actin polymerization at preexisting varicosities. J Neurosci 20:RC82PubMedGoogle Scholar
  20. Hay J, Pick HL Jr (1966) Visual and proprioceptive adaptation to optical displacement of the visual stimulus. J Exp Psychol 71:150–158PubMedCrossRefGoogle Scholar
  21. Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Putz B, Yoshioka T, Kawato M (2000) Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403:192–195PubMedCrossRefGoogle Scholar
  22. Ingram H, van Donkelaar P, Cole J, Vercher JL, Gauthier G, Miall RC (2000) The role of proprioception and attention in a visuomotor adaptation task. Exp Brain Res 132:114–126PubMedCrossRefGoogle Scholar
  23. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143–1195PubMedGoogle Scholar
  24. Jakobson LS, Goodale MA (1989) Trajectories of reaches to prismatically-displaced targets: evidence for “automatic” visuomotor recalibration. Exp Brain Res 78:575–587PubMedCrossRefGoogle Scholar
  25. Kagerer FA, Contreras-Vidal JL, Stelmach GE (1997) Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115(3):557–561PubMedCrossRefGoogle Scholar
  26. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038PubMedCrossRefGoogle Scholar
  27. Klapp ST, Nordell SA, Hoekenga KC, Patton CB (1974) Long-lasting aftereffect of brief prism exposure. Percept Psychophys 15:399–400Google Scholar
  28. Kurata K, Hoshi E (1999) Reacquisition deficits in prism adaptation after muscimol microinjection into the ventral premotor cortex of monkeys. J Neurophysiol 81:1927–1938Google Scholar
  29. Lackner JR, Lobovits D (1977) Adaptation to displaced vision: evidence for prolonged after-effects. Q J Exp Psychol 29(1):65–69PubMedCrossRefGoogle Scholar
  30. Martin KC, Kosik KS (2002) Synaptic tagging—who’s it? Nat Rev Neurosci 3:813–820PubMedCrossRefGoogle Scholar
  31. Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain 119:1183–1198PubMedCrossRefGoogle Scholar
  32. Maviel T, Durkin TP, Menzaghi F, Bontempi B (2004) Sites of neocortical reorganization critical for remote spatial memory. Science 305:96–99PubMedCrossRefGoogle Scholar
  33. Michel C (2003) Les effets consécutifs cognitifs de l’adaptation prismatique visuo-manuelle: de la pseudonégligence à la négligence. Unpublished PhD thesis, Université Claude Bernard Lyon, VilleurbanneGoogle Scholar
  34. Oblinger MM, Lasek RJ (1985) Selective regulation of two axonal cytoskeletal networks in dorsal root ganglion cells. In: O’Lague P (ed) UCLA Symposium on Molecular and Cellular Biology, vol 24, New York, pp135–143Google Scholar
  35. Pisella L, Rode G, Farne A, Boisson D, Rossetti Y (2002) Dissociated long lasting improvements of straight-ahead pointing and line bisection tasks in two hemineglect patients. Neuropsychologia 40:327–334PubMedCrossRefGoogle Scholar
  36. Pisella L, Rossetti Y, Michel C, Rode G, Boisson D, Pelisson D, Tilikete C (2005) Ipsidirectional impairment of prism adaptation after unilateral lesion of anterior cerebellum. Neurology 65:150–152PubMedCrossRefGoogle Scholar
  37. Redding GM, Wallace B (1985) Perceptual-motor coordination and adaptation during locomotion: determinants of prism adaptation in hall exposure. Percept Psychophys 38:320–330PubMedGoogle Scholar
  38. Redding GM, Wallace B (1996) Adaptive spatial alignment and strategic perceptual-motor control. J Exp Psychol Hum Percept Perform 22:379–394PubMedCrossRefGoogle Scholar
  39. Redding GM, Wallace B (1997a) Prism adaptation during target pointing from visible and nonvisible starting locations. J Mot Behav 29:119–130PubMedCrossRefGoogle Scholar
  40. Redding GM, Wallace B (1997b) Adaptive spatial alignment. Lawrence Erlbaum, Hillsdale, NJGoogle Scholar
  41. Redding GM, Wallace B (2002) Strategic calibration and spatial alignment: a model from prism adaptation. J Mot Behav 34:126–138PubMedGoogle Scholar
  42. Redding GM, Wallace B (2003) Dual prism adaptation: calibration or alignment? J Mot Behav 35(4):399–408PubMedGoogle Scholar
  43. Redding GM, Wallace B (2005) Prism adaptation and unilateral neglect: review and analysis. Neuropsychologia (in press) (Epub ahead of print)Google Scholar
  44. Redding GM, Rossetti Y, Wallace B (2005) Applications of prism adaptation: a tutorial in theory and method. Neurosci Biobehav Rev 29:431–444PubMedCrossRefGoogle Scholar
  45. Robertson EM, Pascual-Leone A, Press DZ (2004) Awareness modifies the skill-learning benefits of sleep. Curr Biol 14:208–212PubMedGoogle Scholar
  46. Rossetti Y, Rode G, Pisella L, Farne A, Li L, Boisson D, Perenin MT (1998) Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect. Nature 395:166–169PubMedCrossRefGoogle Scholar
  47. Sutton MA, Masters SE, Bagnall MW, Carew TJ (2001) Molecular mechanisms underlying a unique intermediate phase of memory in aplysia. Neuron 31:143–154PubMedCrossRefGoogle Scholar
  48. Takehara K, Kawahara S, Kirino Y (2003) Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci 23:9897–9905PubMedGoogle Scholar
  49. Taub E, Goldberg LA (1973) Prism adaptation: control of intermanual transfer by distribution of practice. Science 180:755–757PubMedCrossRefGoogle Scholar
  50. Taub E, Ellman SJ, Berman AJ (1966) Deafferentation in monkeys: effect on conditioned grasp response. Science 151:593–594PubMedCrossRefGoogle Scholar
  51. Walker MP, Stickgold R (2004) Sleep-dependent learning and memory consolidation. Neuron 44:121–133PubMedCrossRefGoogle Scholar
  52. Welch RB (1978) Perceptual modification: adaptating to altered sensory environments. Academic, New York, NYGoogle Scholar
  53. Welch RB (1986) Adaptation of space perception. In Boff KR, Kaufman L, Thomas JR (eds) Handbook of perception and human performance, vol 1: sensory processes and perception. Wiley, Chichester, NY, pp24.1–24.45Google Scholar
  54. Weiner MJ, Hallett M, Funkenstein HH (1983) Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology 33:766–772PubMedGoogle Scholar
  55. Yin PB, Kitazawa S (2001) Long-lasting aftereffects of prism adaptation in the monkey. Exp Brain Res 141:250–253PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Institute of Cognitive NeuroscienceUniversity College LondonLondonUK
  2. 2.Behavioural Brain Sciences, PsychologyUniversity of BirminghamBirminghamUK
  3. 3.Espace et ActionUMR-S 534 INSERM-UCBLBronFrance
  4. 4.Institut Fédératif des Neurosciences de LyonLyon Cedex 03France

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