Week6

MANUSCRIPT ID

• Sleep after spatial learning promotes covert reorganization of brain activity

Pierre Orban, Geraldine Rauchs, Evelyne Balteau, Christian Degueldre, Andre Luxen, Pierre Maquet, & Phillipe Peigneux

• Abstract:

Sleep promotes the integration of recently acquired spatial memories into cerebral networks for the long term. In this study, we examined how sleep deprivation hinders this consolidation process. Using functional MRI, we mapped regional cerebral activity during place-finding navigation in a virtual town, immediately after learning and 3 days later, in subjects either allowed regular sleep (RS) or totally sleep-deprived (TSD) on the first posttraining night. At immediate and delayed retrieval, place-finding navigation elicited increased brain activity in an extended hippocamponeocortical network in both RS and TSD subjects. Behavioral performance was equivalent between groups. However, striatal navigation-related activity increased more at delayed retrieval in RS than in TSD subjects. Furthermore, correlations between striatal response and behavioral performance, as well as functional connectivity between the striatum and the hippocampus, were modulated by posttraining sleep. These data suggest that brain activity is restructured during sleep in such a way that navigation in the virtual environment, initially related to a hippocampus-dependent spatial strategy, becomes progressively contingent in part on a response-based strategy mediated by the striatum. Both neural strategies eventually relate to equivalent performance levels, indicating that covert reorganization of brain patterns underlying navigation after sleep is not necessarily accompanied by overt changes in behavior.

• Keywords:

functional MRI; hippocampus; sleep deprivation; memory consolidation; striatum

MANUSCRIPT DETAILS

   * Introduction/Aims 

Spatial learning- flexible relationships between environmental cues

• Encoding and initial maintenance = Medial temporal lobe (hippocampus) dependent
• With training/practice = also partly striatum (caudate) mediated

Sleeping brain may actively process freshly acquired memories Support role in a gradual consolidation process

Hypothesis = Sleep deprivation after spatial learning will hinder reorganization of cortical activity underlying memory consolidation

   * Method 

Subjects: 24 healthy adults (12 male, 12 female)

• Regular Sleep (RS)- 6 males, 6 females
• Total Sleep Deprived (TSD)- 6 males, 6 females

Navigation Task: Virtual environment- Walking along streets in a complex town

• 3 distinct districts- visual backgrounds, objects along streets
• 1 target (identified)
• 10 starting points (not identified)

Setup: Regular sleep group- training, immediate retrieval (day1), 3 nights normal sleep, delayed retrieval (day4) Regular sleep group- training, immediate retrieval (day1), total sleep deprivation (night1), 2 nights normal sleep, delayed retrieval (day4)

Imaging Parameters: (with standard preprocessing)

• Structural T1-weighted MR
• BOLD Echo Planar Imaging

   * Results

Navigational Performance:

• No significant main effect of group (RS vs. TSD) or session (Immediate vs. Delayed), no interaction in a 2 way ANOVA
• Both groups learned and remembered
• Total sleep deprivation did not alter delayed retrieval performance

Increased BOLD response during place finding: (both groups, both times)

• Hippocampus + surrounding cortex
• Occipital
• Parietal
• Frontal
• Cerebellar

Brain activity positively correlates with performance: (both groups, both times)

• Positive correlation- Right hippocampus activity (corrected p-value)and navigation performance (distance from target)

Changes in activation between Immediate and Delayed Retrieval: Increased activation at Delayed (vs. immediate)

• Caudate
• Superior parietal lobule
• Middle cingulate
• Temporal
• Precuneus
• Frontal

Decreased activation at Delayed

• Hippocampus complex

Sleep modifies reorganization of brain activity at delayed retrieval: RS activation > TSD activation

• Caudate
• Insula
• Precentral gyrus
• Middle temporal gyrus

Group x Performance interaction in right caudate at delayed retrieval

• RS: positive (higher activity – improved place finding)
• TSD: negative (lower activity – improved place finding)

   * Discussion and Conclusion:

Striatal activity was increased at delayed retrieval for RS versus TSD subjects Post-training sleep modulated:

• Functional connectivity- hippocampus and caudate
• Linear relationship- striatal activity and navigational accuracy

Sleep-associated changes in brain activity where accompanied by equivalent performance