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

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Pages (from-to)423-434
Number of pages12
JournalNeuroImage
Volume108
DOIs
StatePublished - 1 Mar 2015

Bibliographical note

Funding Information:
This study was supported by grants from the Canadian Institutes of Health and Research (CIHR; MOP97830 ) as well as the Ministry of Economic Development, Innovation and Exportation of Quebec (MDEIE; PSR-SIIRI-704 ) to JD. Postdoctoral support for GA came from Fyssen Foundation and CIHR. The authors thank Pr. Pierre Maquet for his valuable insights on the design and on the interpretation of the results. We also thank Laura Ray, Louis Patenaude-Veilleux, Amel Bouyoucef and Frederic Jeay for their technical support.

Publisher Copyright:
© 2014 Elsevier Inc.

Keywords

  • Hippocampus
  • Memory consolidation
  • Motor sequence learning
  • Sleep
  • Striatum

ASJC Scopus subject areas

  • Neurology
  • Cognitive Neuroscience

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