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Erschienen in: Experimental Brain Research 4/2010

01.05.2010 | Research Article

Hippocampal contribution to early and later stages of implicit motor sequence learning

verfasst von: Freja Gheysen, Filip Van Opstal, Chantal Roggeman, Hilde Van Waelvelde, Wim Fias

Erschienen in: Experimental Brain Research | Ausgabe 4/2010

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Abstract

Implicit motor sequence learning refers to an important human ability to acquire new motor skills through the repeated performance of a motor sequence. This learning process is characterized by slow, incremental gains of motor performance. The present fMRI study was developed to better delineate the areas supporting these temporal dynamics of learning. By using the serial color matching paradigm, our study focused on the motor level of sequence learning and tracked the time course of learning-related neural changes. Imaging results showed a significant contribution of the left anterior hippocampus in an early sequence acquisition stage (first scanning session) as well as during a later stage with stabilized learning effects (second scanning session). Hippocampal activation significantly correlated with the behavioral learning process and was affected by a change of the motor sequence. These results suggest a strong involvement of the hippocampus in implicit motor sequence learning. On the other hand, a very extensive and bilateral neural network of parietal, temporal and frontal cortical areas (including SMA, pre-SMA) together with parts of the cerebellum and striatum were found to play a role during random visuo-motor task performance.
Literatur
Zurück zum Zitat Aizenstein HJ, Stenger VA, Cochran J, Clark K, Johnson M, Nebes RD et al (2004) Regional brain activation during concurrent implicit and explicit sequence learning. Cereb Cortex 14:199–208CrossRefPubMed Aizenstein HJ, Stenger VA, Cochran J, Clark K, Johnson M, Nebes RD et al (2004) Regional brain activation during concurrent implicit and explicit sequence learning. Cereb Cortex 14:199–208CrossRefPubMed
Zurück zum Zitat Anastasopoulou T, Harvey N (1999) Assessing sequential knowledge through performance measures: The influence of short-term sequential effects. Q J Exp Psychol A 52:423–448CrossRef Anastasopoulou T, Harvey N (1999) Assessing sequential knowledge through performance measures: The influence of short-term sequential effects. Q J Exp Psychol A 52:423–448CrossRef
Zurück zum Zitat Bar M (2007) The proactive brain: using analogies and associations to generate predictions. Trends Cogn Sci 11:280–289CrossRefPubMed Bar M (2007) The proactive brain: using analogies and associations to generate predictions. Trends Cogn Sci 11:280–289CrossRefPubMed
Zurück zum Zitat Bischoff-Grethe A, Goedert KM, Willingham DT, Grafton ST (2004) Neural substrates of response-based sequence learning using fMRI. J Cogn Neurosci 16:127–138CrossRefPubMed Bischoff-Grethe A, Goedert KM, Willingham DT, Grafton ST (2004) Neural substrates of response-based sequence learning using fMRI. J Cogn Neurosci 16:127–138CrossRefPubMed
Zurück zum Zitat Brasted PJ, Bussey TJ, Murray EA, Wise SP (2003) Role of the hippocampal system in associative learning beyond the spatial domain. Brain 126:1202–1223CrossRefPubMed Brasted PJ, Bussey TJ, Murray EA, Wise SP (2003) Role of the hippocampal system in associative learning beyond the spatial domain. Brain 126:1202–1223CrossRefPubMed
Zurück zum Zitat Cave CB, Squire LR (1992) Intact and long-lasting repetition priming in amnesia. J Exp Psychol Learn Mem Cogn 18:509–520CrossRefPubMed Cave CB, Squire LR (1992) Intact and long-lasting repetition priming in amnesia. J Exp Psychol Learn Mem Cogn 18:509–520CrossRefPubMed
Zurück zum Zitat Chun MM, Phelps EA (1999) Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage. Nat Neurosci 2:844–847CrossRefPubMed Chun MM, Phelps EA (1999) Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage. Nat Neurosci 2:844–847CrossRefPubMed
Zurück zum Zitat Colgin LL, Moser EI, Moser MB (2008) Understanding memory through hippocampal remapping. Trends Neurosci 31:469–477CrossRefPubMed Colgin LL, Moser EI, Moser MB (2008) Understanding memory through hippocampal remapping. Trends Neurosci 31:469–477CrossRefPubMed
Zurück zum Zitat Curran T (1997) Higher-order associative learning in amnesia: evidence from the serial reaction time task. J Cogn Neurosci 9:522–533CrossRef Curran T (1997) Higher-order associative learning in amnesia: evidence from the serial reaction time task. J Cogn Neurosci 9:522–533CrossRef
Zurück zum Zitat Destrebecqz A, Cleeremans A (2001) Can sequence learning be implicit? New evidence with the process dissociation procedure. Psychon Bull Rev 8:343–350PubMed Destrebecqz A, Cleeremans A (2001) Can sequence learning be implicit? New evidence with the process dissociation procedure. Psychon Bull Rev 8:343–350PubMed
Zurück zum Zitat Destrebecqz A, Peigneux P, Laureys S, Degueldre C, Del Fiore G, Aerts J et al (2005) The neural correlates of implicit and explicit sequence learning: interacting networks revealed by the process dissociation procedure. Learn Mem 12:480–490CrossRefPubMed Destrebecqz A, Peigneux P, Laureys S, Degueldre C, Del Fiore G, Aerts J et al (2005) The neural correlates of implicit and explicit sequence learning: interacting networks revealed by the process dissociation procedure. Learn Mem 12:480–490CrossRefPubMed
Zurück zum Zitat Doyon J, Bellec P, Amsel R, Penhune V, Monchi O, Carrier J et al (2009) Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res 199:61–75CrossRefPubMed Doyon J, Bellec P, Amsel R, Penhune V, Monchi O, Carrier J et al (2009) Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res 199:61–75CrossRefPubMed
Zurück zum Zitat Fortin NJ, Agster KL, Eichenbaum HB (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5:458–462PubMed Fortin NJ, Agster KL, Eichenbaum HB (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5:458–462PubMed
Zurück zum Zitat Gheysen F, Gevers W, De Schutter E, Van Waelvelde H, Fias W (2009) Disentangling perceptual from motor implicit sequence learning with a serial color-matching task. Exp Brain Res 197:163–174CrossRefPubMed Gheysen F, Gevers W, De Schutter E, Van Waelvelde H, Fias W (2009) Disentangling perceptual from motor implicit sequence learning with a serial color-matching task. Exp Brain Res 197:163–174CrossRefPubMed
Zurück zum Zitat Giovanello KS, Verfaellie M, Keane MM (2003) Disproportionate deficit in associative recognition relative to item recognition in global amnesia. Cogn Affect Behav Neurosci 3:186–194CrossRefPubMed Giovanello KS, Verfaellie M, Keane MM (2003) Disproportionate deficit in associative recognition relative to item recognition in global amnesia. Cogn Affect Behav Neurosci 3:186–194CrossRefPubMed
Zurück zum Zitat Grafton ST, Hazeltine E, Ivry R (1995) Functional mapping of sequence learning in normal humans. J Cogn Neurosci 7:497–510CrossRef Grafton ST, Hazeltine E, Ivry R (1995) Functional mapping of sequence learning in normal humans. J Cogn Neurosci 7:497–510CrossRef
Zurück zum Zitat Hazeltine E, Grafton ST, Ivry R (1997) Attention and stimulus characteristics determine the locus of motor-sequence encoding—a PET study. Brain 120:123–140CrossRefPubMed Hazeltine E, Grafton ST, Ivry R (1997) Attention and stimulus characteristics determine the locus of motor-sequence encoding—a PET study. Brain 120:123–140CrossRefPubMed
Zurück zum Zitat Honda M, Deiber MP, Ibanez V, Pascual-Leone A, Zhuang P, Hallett M (1998) Dynamic cortical involvement in implicit and explicit motor sequence learning—a PET study. Brain 121:2159–2173CrossRefPubMed Honda M, Deiber MP, Ibanez V, Pascual-Leone A, Zhuang P, Hallett M (1998) Dynamic cortical involvement in implicit and explicit motor sequence learning—a PET study. Brain 121:2159–2173CrossRefPubMed
Zurück zum Zitat Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273:1399–1402CrossRefPubMed Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273:1399–1402CrossRefPubMed
Zurück zum Zitat Lieberman MD, Chang GY, Chiao J, Bookheimer SY, Knowlton BJ (2004) An event-related fMRI study of artificial grammar learning in a balanced chunk strength design. J Cogn Neurosci 16:427–438CrossRefPubMed Lieberman MD, Chang GY, Chiao J, Bookheimer SY, Knowlton BJ (2004) An event-related fMRI study of artificial grammar learning in a balanced chunk strength design. J Cogn Neurosci 16:427–438CrossRefPubMed
Zurück zum Zitat Loftus GR, Masson MEJ (1994) Using confidence-intervals in within-subject designs. Psychon Bull Rev 1:476–490 Loftus GR, Masson MEJ (1994) Using confidence-intervals in within-subject designs. Psychon Bull Rev 1:476–490
Zurück zum Zitat Muller RA, Kleinhans N, Pierce K, Kemmotsu N, Courchesne E (2002) Functional MRI of motor sequence acquisition: effects of learning stage and performance. Cogn Brain Res 14:277–293CrossRef Muller RA, Kleinhans N, Pierce K, Kemmotsu N, Courchesne E (2002) Functional MRI of motor sequence acquisition: effects of learning stage and performance. Cogn Brain Res 14:277–293CrossRef
Zurück zum Zitat Nissen MJ, Bullemer P (1987) Attentional requirements of learning—evidence from performance-measures. Cogn Psychol 19:1–32CrossRef Nissen MJ, Bullemer P (1987) Attentional requirements of learning—evidence from performance-measures. Cogn Psychol 19:1–32CrossRef
Zurück zum Zitat O’Keefe J (1999) Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus 9:352–364CrossRefPubMed O’Keefe J (1999) Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus 9:352–364CrossRefPubMed
Zurück zum Zitat Orban P, Peigneux P, Lungu O, Albouy G, Breton E, Laberenne F et al (2010) The multifaceted nature of the relationship between performance and brain activity in motor sequence learning. Neuroimage 49:694–702CrossRefPubMed Orban P, Peigneux P, Lungu O, Albouy G, Breton E, Laberenne F et al (2010) The multifaceted nature of the relationship between performance and brain activity in motor sequence learning. Neuroimage 49:694–702CrossRefPubMed
Zurück zum Zitat Packard MG, Knowlton BJ (2002) Learning and memory functions of the basal ganglia. Annu Rev Neurosci 25:563–593CrossRefPubMed Packard MG, Knowlton BJ (2002) Learning and memory functions of the basal ganglia. Annu Rev Neurosci 25:563–593CrossRefPubMed
Zurück zum Zitat Peigneux P, Maquet P, Meulemans T, Destrebecqz A, Laureys S, Degueldre C et al (2000) Striatum forever, despite sequence learning variability: a random effect analysis of PET data. Hum Brain Mapp 10:179–194CrossRefPubMed Peigneux P, Maquet P, Meulemans T, Destrebecqz A, Laureys S, Degueldre C et al (2000) Striatum forever, despite sequence learning variability: a random effect analysis of PET data. Hum Brain Mapp 10:179–194CrossRefPubMed
Zurück zum Zitat Rauch SL, Whalen PJ, Savage CR, Curran T, Kendrick A, Brown HD et al (1997) Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Hum Brain Mapp 5:124–132CrossRefPubMed Rauch SL, Whalen PJ, Savage CR, Curran T, Kendrick A, Brown HD et al (1997) Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Hum Brain Mapp 5:124–132CrossRefPubMed
Zurück zum Zitat Reber PJ, Squire LR (1994) Parallel brain systems for learning with and without awareness. Learn Mem 1:217–229PubMed Reber PJ, Squire LR (1994) Parallel brain systems for learning with and without awareness. Learn Mem 1:217–229PubMed
Zurück zum Zitat Ryan JD, Althoff RR, Whitlow S, Cohen NJ (2000) Amnesia is a deficit in relational memory. Psychol Sci 11:454–461CrossRefPubMed Ryan JD, Althoff RR, Whitlow S, Cohen NJ (2000) Amnesia is a deficit in relational memory. Psychol Sci 11:454–461CrossRefPubMed
Zurück zum Zitat Sakai K, Hikosaka O, Miyauchi S, Sasaki Y, Fujimaki N, Pütz B (1999) Presupplementary motor area activation during sequence learning reflects visuo-motor association. J Neurosci 19:1–6 Sakai K, Hikosaka O, Miyauchi S, Sasaki Y, Fujimaki N, Pütz B (1999) Presupplementary motor area activation during sequence learning reflects visuo-motor association. J Neurosci 19:1–6
Zurück zum Zitat Schendan HE, Searl MM, Melrose RJ, Stern CE (2003) An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 37:1013–1025CrossRefPubMed Schendan HE, Searl MM, Melrose RJ, Stern CE (2003) An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 37:1013–1025CrossRefPubMed
Zurück zum Zitat Schwarb H, Schumacher EH (2009) Neural evidence of a role for spatial response selection in the learning of spatial sequences. Brain Res 1247:114–125CrossRefPubMed Schwarb H, Schumacher EH (2009) Neural evidence of a role for spatial response selection in the learning of spatial sequences. Brain Res 1247:114–125CrossRefPubMed
Zurück zum Zitat Seidler RD, Purushotham A, Kim SG, Ugurbil K, Willingham D, Ashe J (2002) Cerebellum activation associated with performance change but not motor learning. Science 296:2043–2046CrossRefPubMed Seidler RD, Purushotham A, Kim SG, Ugurbil K, Willingham D, Ashe J (2002) Cerebellum activation associated with performance change but not motor learning. Science 296:2043–2046CrossRefPubMed
Zurück zum Zitat Seidler RD, Purushotham A, Kim SG, Ugurbil K, Willingham D, Ashe J (2005) Neural correlates of encoding and expression in implicit sequence learning. Exp Brain Res 165:114–124CrossRefPubMed Seidler RD, Purushotham A, Kim SG, Ugurbil K, Willingham D, Ashe J (2005) Neural correlates of encoding and expression in implicit sequence learning. Exp Brain Res 165:114–124CrossRefPubMed
Zurück zum Zitat Shanks DR, Green RE, Kolodny J (1994) A critical examination of the evidence for nonconcious (implicit) learning. In: Umilta C, Moscovitch M (eds) Attention and performance XV: conscious and nonconscious information processing. MIT Press, Cambridge, pp 837–860 Shanks DR, Green RE, Kolodny J (1994) A critical examination of the evidence for nonconcious (implicit) learning. In: Umilta C, Moscovitch M (eds) Attention and performance XV: conscious and nonconscious information processing. MIT Press, Cambridge, pp 837–860
Zurück zum Zitat Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306CrossRefPubMed Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306CrossRefPubMed
Zurück zum Zitat Stadler MA, Frensch PA (eds) (1998) Handbook of implicit learning. Sage, Thousand Oaks Stadler MA, Frensch PA (eds) (1998) Handbook of implicit learning. Sage, Thousand Oaks
Zurück zum Zitat Stevens M, Lammertyn J, Verbruggen F, Vandierendonck A (2006) Tscope: a C library for programming cognitive experiments on the MS Windows platform. Behav Res Methods 38:280–286PubMed Stevens M, Lammertyn J, Verbruggen F, Vandierendonck A (2006) Tscope: a C library for programming cognitive experiments on the MS Windows platform. Behav Res Methods 38:280–286PubMed
Zurück zum Zitat Takashima A, Nieuwenhuis ILC, Jensen O, Talamini LM, Rijpkema M, Fernandez G (2009) Shift from hippocampal to neocortical centered retrieval network with consolidation. J Neurosci 29:10087–10093CrossRefPubMed Takashima A, Nieuwenhuis ILC, Jensen O, Talamini LM, Rijpkema M, Fernandez G (2009) Shift from hippocampal to neocortical centered retrieval network with consolidation. J Neurosci 29:10087–10093CrossRefPubMed
Zurück zum Zitat Thomas KM, Hunt RH, Vizueta N, Sommer T, Durston S, Yang YH et al (2004) Evidence of developmental differences in implicit sequence learning: an fMRI study of children and adults. J Cogn Neurosci 16:1339–1351CrossRefPubMed Thomas KM, Hunt RH, Vizueta N, Sommer T, Durston S, Yang YH et al (2004) Evidence of developmental differences in implicit sequence learning: an fMRI study of children and adults. J Cogn Neurosci 16:1339–1351CrossRefPubMed
Zurück zum Zitat Toni I, Krams M, Turner R, Passingham RE (1998) The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 8:50–61CrossRefPubMed Toni I, Krams M, Turner R, Passingham RE (1998) The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 8:50–61CrossRefPubMed
Zurück zum Zitat Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289CrossRefPubMed Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289CrossRefPubMed
Zurück zum Zitat van der Graaf FHCE, de Jong BM, Maguire RP, Meiners LC, Leenders KL (2004) Cerebral activation related to skills practice in a double serial reaction time task: striatal involvement in random-order sequence learning. Cogn Brain Res 20:120–131CrossRef van der Graaf FHCE, de Jong BM, Maguire RP, Meiners LC, Leenders KL (2004) Cerebral activation related to skills practice in a double serial reaction time task: striatal involvement in random-order sequence learning. Cogn Brain Res 20:120–131CrossRef
Zurück zum Zitat Van Opstal F, Verguts T, Orban GA, Fias W (2008) A hippocampal—parietal network for learning an ordered sequence. Neuroimage 40:333–341CrossRefPubMed Van Opstal F, Verguts T, Orban GA, Fias W (2008) A hippocampal—parietal network for learning an ordered sequence. Neuroimage 40:333–341CrossRefPubMed
Zurück zum Zitat Van Opstal F, Fias W, Peigneux P, Verguts T (2009) The neural representation of extensively trained ordered sequences. Neuroimage 47:367–375CrossRefPubMed Van Opstal F, Fias W, Peigneux P, Verguts T (2009) The neural representation of extensively trained ordered sequences. Neuroimage 47:367–375CrossRefPubMed
Zurück zum Zitat Vaquero JMM, Jimenez L, Lupianez J (2006) The problem of reversals in assessing implicit sequence learning with serial reaction time tasks. Exp Brain Res 175:97–109CrossRefPubMed Vaquero JMM, Jimenez L, Lupianez J (2006) The problem of reversals in assessing implicit sequence learning with serial reaction time tasks. Exp Brain Res 175:97–109CrossRefPubMed
Metadaten
Titel
Hippocampal contribution to early and later stages of implicit motor sequence learning
verfasst von
Freja Gheysen
Filip Van Opstal
Chantal Roggeman
Hilde Van Waelvelde
Wim Fias
Publikationsdatum
01.05.2010
Verlag
Springer-Verlag
Erschienen in
Experimental Brain Research / Ausgabe 4/2010
Print ISSN: 0014-4819
Elektronische ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-010-2186-6

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