Abstract
There is now converging evidence that the declarative memory system (hippocampus dependent) contributes to sequential motor learning in concert with the procedural memory system (striatum dependent). Because of the competition for shared neuronal resources, introducing a declarative memory task can impair learning of a new motor sequence and interference may occur during the procedural consolidation process. Here, we investigated the extent to which interference effects between memory systems are seen at the retrieval phase of skill learning. Healthy participants were assigned to a control (n = 15) or a declarative condition (n = 15) and trained on a sequence of finger movements (FOS task). Both groups showed similar improvement at the end of the practice session on the first day. Twenty-four hours later, controls were tested solely on the FOS task, while subjects in the declarative condition first engaged in a visuospatial task. Additional offline gains in performance were observed only in the control condition. The introduction of a visuospatial memory task just before retrieval of the motor skill was sufficient to eliminate these gains. This suggests that interference between procedural and declarative memory systems may also occur during subsequent motor recall. It is proposed that the interference effects are linked, in part, to the spatial nature of the motor and declarative tasks, which specifically depends upon hippocampal involvement.
Similar content being viewed by others
References
Albouy G et al (2008) Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 58:261–272
Albouy G et al (2012) Neural correlates of performance variability during motor sequence acquisition. NeuroImage 60:324–331. doi:10.1016/j.neuroimage.2011.12.049
Albouy G, King BR, Maquet P, Doyon J (2013) Hippocampus and striatum: dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus 23:985–1004
Albouy G et al (2015) Maintaining versus enhancing motor sequence memories: respective roles of striatal and hippocampal systems. NeuroImage 108:423–434. doi:10.1016/j.neuroimage.2014.12.049
Bachevalier J, Nemanic S (2008) Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex. Hippocampus 18:64–80. doi:10.1002/hipo.20369
Balas M, Netser S, Giladi N, Karni A (2007a) Interference to consolidation phase gains in learning a novel movement sequence by handwriting: dependence on laterality and the level of experience with the written sequence. Exp Brain Res 180:237–246
Balas M, Roitenberg N, Giladi N, Karni A (2007b) When practice does not make perfect: well-practiced handwriting interferes with the consolidation phase gains in learning a movement sequence. Exp Brain Res 178:499–508
Brashers-Krug T, Shadmehr R, Bizzi E (1996) Consolidation in human motor memory. Nature 382:252–255
Brown RM, Robertson EM (2007) Off-line processing: reciprocal interactions between declarative and procedural memories. J Neurosci 27:10468–10475
Cohen D, Robertson EM (2011) Preventing interference between different memory tasks. Nat Neurosci 14:953–955
Cohen NJ, Squire LR (1980) Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. Science 210:207–210
Cohen D, Pascual-Leone A, Press DZ, Robertson EM (2005) Off-line learning of motor skill memory: a double dissociation of goal and movement. Proc Natl Acad Sci USA 102:18237–18241. doi:10.1073/pnas.0506072102
Coynel D et al (2010) Dynamics of motor-related functional integration during motor sequence learning. NeuroImage 49:759–766
Crane J, Milner B (2005) What went where? Impaired object-location learning in patients with right hippocampal lesions. Hippocampus 15:216–231. doi:10.1002/hipo.20043
DeCoteau WE, Kesner RP (2000) A double dissociation between the rat hippocampus and medial caudoputamen in processing two forms of knowledge. Behav Neurosci 114:1096–1108
Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222. doi:10.1146/annurev.ne.18.030195.001205
Dorfberger S, Adi-Japha E, Karni A (2007) Reduced susceptibility to interference in the consolidation of motor memory before adolescence. PLoS One 2:e240
Doyon J, Benali H (2005) Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol 15:161–167. doi:10.1016/j.conb.2005.03.004
Doyon J, Gaudreau D, Laforce RL Jr, Castonguay M, Bedard PJ, Bedard F, Bouchard JP (1997) Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence. Brain Cogn 34:218–245
Doyon J et al (2009) Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res 199:61–75
Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Ann Rev Psychol 55:51–86
Eckart MT, Huelse-Matia MC, Schwarting RKW (2012) Dorsal hippocampal lesions boost performance in the rat sequential reaction time task. Hippocampus 22:1202–1214. doi:10.1002/hipo.20965
Ertelt D et al (2012) Skill memory escaping from distraction by sleep-evidence from dual-task performance. PLoS One. doi:10.1371/journal.pone.0050983
Fogel SM, Albouy G, Vien C, Popovicci R, King BR, Hoge R, Jbabdi S, Benali H, Karni A, Maquet P, Carrier J, Doyon J (2014) fMRI and sleep correlates of the age-related impairment in motor memory consolidation. Hum Brain Mapp 35(8):3625-3645 .doi:10.1002/hbm.22426
Gagné MH, Cohen H (2016) Interference effects between manual and oral motor skills. Experimental Brain Res 234:845–851
Galea JM, Albert NB, Ditye T, Miall RC (2010) Disruption of the dorsolateral prefrontal cortex facilitates the consolidation of procedural skills. J Cogn Neurosci 22:1158–1164. doi:10.1162/jocn.2009.21259
Grafton ST, Hazeltine E, Ivry R (1995) Functional mapping of sequence learning in normal humans. J Cogn Neurosci 7:497–510
Grafton ST, Hazeltine E, Ivry RB (2002) Motor sequence learning with the nondominant left hand: a PET functional imaging study. Exp Brain Res 146:369–378. doi:10.1007/s00221-002-1181-y
Hardwick RM, Rottschy C, Miall RC, Eickhoff SB (2013) A quantitative meta-analysis and review of motor learning in the human brain. NeuroImage 67:283–297. doi:10.1016/j.neuroimage.2012.11.020
Karni A (1996) The acquisition of perceptual and motor skills: a memory system in the adult human cortex. Cogn Brain Res 5:39–48
Karni A, Sagi D (1993) The time course of learning a visual skill. Nature 365:250–252
Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377:155–158
Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, Ungerleider LG (1998) The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci USA 95:861–868
Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341. doi:10.1146/annurev.neuro.23.1.315
Keisler A, Shadmehr R (2010) A shared resource between declarative memory and motor memory. J Neurosci 30:14817–14823. doi:10.1523/jneurosci.4160-10.2010
Kesner RP, Bolland BL, Dakis M (1993) Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp Brain Res 93:462–470. doi:10.1007/BF00229361
Korman M, Doyon J, Doljansky J, Carrier J, Dagan Y, Karni A (2007) Daytime sleep condenses the time course of motor memory consolidation. Nat Neurosci 10:1206–1213
Kichka M (1978) Tel-aviv Traffic. https://www.pinterest.com/pin/426082814716780323/. Accessed 04 July 2016
Krakauer JW, Shadmehr R (2006) Consolidation of motor memory. Trends Neurosci 29:58–64
Lehericy S, Benali H, Van De Moortele PF, Pelegrini-Issac M, Waechter T, Ugurbil K, Doyon J (2005) Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proc Natl Acad Sci USA 102:12566–12571
Lohse KR, Wadden K, Boyd LA, Hodges NJ (2014) Motor skill acquisition across short and long time scales: a meta-analysis of neuroimaging data. Neuropsychologia 59:130–141. doi:10.1016/j.neuropsychologia.2014.05.001
Lundbye-Jensen J, Petersen TH, Rothwell JC, Nielsen JB (2011) Interference in ballistic motor learning: specificity and role of sensory error signals. PLoS One 6:e17451
Maquet P et al (2000) Experience-dependent changes in changes in cerebral activation during human REM sleep. Nat Neurosci 3:831–836
Morehead JR, Butcher PA, Taylor JA (2011) Does fast learning depend on declarative mechanisms? J Neurosci 31:5184–5185. doi:10.1523/jneurosci.0040-11.2011
O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175
Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9:1465–1472
Peigneux P, Melchior G, Schmidt C, Dang-Vu T, Boly M, Laureys S, Maquet P (2004) Memory processing during sleep mechanisms and evidence from neuroimaging studies. Psychol Belg 44:121–142
Poldrack RA, Packard MG (2003) Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 41:245–251
Poldrack RA, Rodriguez P (2004) How do memory systems interact? Evidence from human classification learning. Neurobiol Learn Mem 82:324–332
Rieckmann A, Fischer H, Bäckman L (2010) Activation in striatum and medial temporal lobe during sequence learning in younger and older adults: relations to performance. NeuroImage 50:1303–1312. doi:10.1016/j.neuroimage.2010.01.015
Robertson EM (2012) New insights in human memory interference and consolidation. Curr Biol 22:R66–R71
Robertson EM, Pascual-Leone A, Miall RC (2004) Current concepts in procedural consolidation. Nat Rev Neurosci 5:576–582
Steele CJ, Penhune VB (2010) Specific Increases within Global Decreases: A Functional Magnetic Resonance Imaging Investigation of Five Days of Motor Sequence Learning. J Neurosci 30(24):8332–8341. doi:10.1523/JNEUROSCI.5569-09.2010
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 37:1013–1025
Shadmehr R, Brashers-Krug T (1997) Functional stages in the formation of human long-term motor memory. J Neurosci 17:409–419
Smith ML, Milner B (1981) The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19:781–793. doi:10.1016/0028-3932(81)90090-7
Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231
Tibi R, Eviatar Z, Karni A (2013) Fact retrieval and memory consolidation for a movement sequence: bidirectional effects of ‘unrelated’ cognitive tasks on procedural memory. PLoS One 8:e80270
Walker MP, Brakefield T, Hobson JA, Stickgold R (2003) Dissociable stages of human memory consolidation and reconsolidation. Nature 425:616–620
Zach N, Inbar D, Grinvald Y, Vaadia E (2012) Single neurons in M1 and premotor cortex directly reflect behavioral interference. PLoS One 7:e32986
Acknowledgments
We thank Jean Bégin for his help with the statistical analyses. This study was funded by a grant from FQRNT (Québec).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gagné, MH., Cohen, H. Interference effects between memory systems in the acquisition of a skill. Exp Brain Res 234, 2883–2891 (2016). https://doi.org/10.1007/s00221-016-4690-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-016-4690-9