Maintaining vs. enhancing motor sequence memories: respective roles of striatal and hippocampal systems

Genevieve Albouy; Stuart Fogel; Bradley R King; Samuel Laventure; Habib Benali; Avi Karni; Julie Carrier; Edwin M Robertson; Julien Doyon

doi:10.1016/j.neuroimage.2014.12.049

Maintaining vs. enhancing motor sequence memories: respective roles of striatal and hippocampal systems

Neuroimage. 2015 Mar:108:423-34. doi: 10.1016/j.neuroimage.2014.12.049. Epub 2014 Dec 23.

Authors

Genevieve Albouy¹, Stuart Fogel², Bradley R King¹, Samuel Laventure¹, Habib Benali³, Avi Karni⁴, Julie Carrier⁵, Edwin M Robertson⁶, Julien Doyon⁷

Affiliations

¹ Functional Neuroimaging Unit, C.R.I.U.G.M., Montreal, QC, Canada; Psychology Department, University of Montreal, Montreal, QC, Canada.
² Functional Neuroimaging Unit, C.R.I.U.G.M., Montreal, QC, Canada; Psychology Department, University of Montreal, Montreal, QC, Canada; Brain & Mind Institute, Department of Psychology, Western University, London, ON, Canada.
³ Unité Mixte de Recherche-S 678, Institut National de la Santé et de la Recherche Médicale/University of Paris 6, Centre Hospitalier Universitaire Pitié-Salpêtrière, Paris, France.
⁴ Laboratory for Human Brain & Learning, Sagol Department of Neurobiology & E.J. Safra Brain Research Center, University of Haifa, Haifa, Israel.
⁵ Functional Neuroimaging Unit, C.R.I.U.G.M., Montreal, QC, Canada; Psychology Department, University of Montreal, Montreal, QC, Canada; Centre of Advanced Research in Sleep Medicine, Hôpital du Sacré-Coeur de Montreal, Montreal, QC, Canada.
⁶ Harvard Center for Noninvasive Brain Stimulation, Harvard Medical School and Beth Israel Deaconess Medical Center, Neurology Department, Boston, MA, USA.
⁷ Functional Neuroimaging Unit, C.R.I.U.G.M., Montreal, QC, Canada; Psychology Department, University of Montreal, Montreal, QC, Canada. Electronic address: julien.doyon@umontreal.ca.

PMID: 25542533
DOI: 10.1016/j.neuroimage.2014.12.049

Abstract

It is now accepted that hippocampal- and striatal-dependent memory systems do not act independently, but rather interact during both memory acquisition and consolidation. However, the respective functional roles of the hippocampus and the striatum in these processes remain unknown. Here, functional magnetic resonance imaging (fMRI) was used in a daytime sleep/wake protocol to investigate this knowledge gap. Using a protocol developed earlier in our lab (Albouy et al., 2013a), the manipulation of an explicit sequential finger-tapping task, allowed us to isolate allocentric (spatial) and egocentric (motor) representations of the sequence, which were supported by distinct hippocampo- and striato-cortical networks, respectively. Importantly, a sleep-dependent performance enhancement emerged for the hippocampal-dependent memory trace, whereas performance was maintained for the striatal-dependent memory trace, irrespective of the sleep condition. Regression analyses indicated that the interaction between these two systems influenced subsequent performance improvements. While striatal activity was negatively correlated with performance enhancement after both sleep and wakefulness in the allocentric representation, hippocampal activity was positively related to performance improvement for the egocentric representation, but only if sleep was allowed after training. Our results provide the first direct evidence of a functional dissociation in consolidation processes whereby memory stabilization seems supported by the striatum in a time-dependent manner whereas memory enhancement seems linked to hippocampal activity and sleep-dependent processes.

Keywords: Hippocampus; Memory consolidation; Motor sequence learning; Sleep; Striatum.

Publication types

Comparative Study
Research Support, N.I.H., Extramural

MeSH terms

Corpus Striatum / physiology*
Female
Hippocampus / physiology*
Humans
Male
Memory / physiology*
Sleep
Wakefulness
Young Adult

Grants and funding

MOP97830/PHS HHS/United States