State-Dependent Spike-Timing Relationships between Hippocampal and Prefrontal Circuits during Sleep

Cortico-hippocampal interactions during sleep are believed to reorganize neural circuits in support of memory consolidation. However, spike-timing relationships across cortico-hippocampal networks—key determinants of synaptic changes—are poorly understood. Here we show that cells in prefrontal corte...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2009-02, Vol.61 (4), p.587-596
Main Authors: Wierzynski, Casimir M., Lubenov, Evgueniy V., Gu, Ming, Siapas, Athanassios G.
Format: Article
Language:English
Subjects:
Algorithms
Analysis of Variance
Animals
Electroencephalography
Electrophysiology
Hippocampus - physiology
Hypotheses
Male
Nerve Net - physiology
Prefrontal Cortex - physiology
Rats
Rats, Long-Evans
SIGNALING
Sleep
Sleep - physiology
Sleep Stages
Sleep, REM - physiology
Standard deviation
SYSBIO
SYSNEURO
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Summary:Cortico-hippocampal interactions during sleep are believed to reorganize neural circuits in support of memory consolidation. However, spike-timing relationships across cortico-hippocampal networks—key determinants of synaptic changes—are poorly understood. Here we show that cells in prefrontal cortex fire consistently within 100 ms after hippocampal cells in naturally sleeping animals. This provides evidence at the single cell-pair level for highly consistent directional interactions between these areas within the window of plasticity. Moreover, these interactions are state dependent: they are driven by hippocampal sharp-wave/ripple (SWR) bursts in slow-wave sleep (SWS) and are sharply reduced during REM sleep. Finally, prefrontal responses are nonlinear: as the strength of hippocampal bursts rises, short-latency prefrontal responses are augmented by increased spindle band activity and a secondary peak ∼100 ms later. These findings suggest that SWR events are atomic units of hippocampal-prefrontal communication during SWS and that the coupling between these areas is highly attenuated during REM sleep.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2009.01.011