State-dependent spike timing relationships between hippocampal and prefrontal circuits during sleep

By Casimir Wierzynski, E. Lubenov, Ming Gu, Athanassios Siapas. 2009

294 citations recorded by the source corpus.

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, which are key determinants of synaptic changes, are not well 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 non-linear: 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 serve as an atomic unit of hippocampal-prefrontal communication during SWS, and that the coupling between prefrontal and hippocampal areas is highly attenuated during REM sleep.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

High-density, long-lasting, and multi-region electrophysiological recordings using polymer electrode arrays (2018, result): “We confirmed previous reports of mPFC and NAc modulation (Lansink et al., 2009; Tang et al., 2017; Wierzynski et al., 2009): 19 of 61 mPFC (13 positively, 6 negatively) (p < 1.”
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning (2015, background): “At the tens of milliseconds timescale, SPW-Rs are often phase-locked to spindle cycles (Sirota et al., 2003; M€olle et al., 2006; Clemens et al., 2007; Wierzynski et al., 2009), an indication of thalamocortical influence on the timing of SPW-Rs.”
Sleep Is for Forgetting (2017, background): “Wilson and others (Wilson and McNaughton, 1994; Kudrimoti et al., 1999) have found that the highly correlated neuronal firing resulting from spatial learning on a maze decreases across the first 20 – 40 min of the start of SWA.”
Memory consolidation. (2015, background): “Additionally, if sharp-wave ripples are followed by neocortical spindles, secondary larger waves of increased firing rates can be observed in the cortex (Wierzynski et al. 2009).”
How Memory Replay in Sleep Boosts Creative Problem-Solving (2018, background): “As discussed above, activity in the hippocampus and neocortex is not so tightly synchronized in REM [34,42] and this lack of hippocampal input to the neocortex combines with random activation via PGO waves and high levels of plasticity to set the scene for the formation of novel connections between ”
Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep. (2020, background): “Studies show ripple-spindle locking (Clemens et al. 2007, Mölle et al. 2006, Sirota et al. 2003, Wierzynski et al. 2009); a recent work reported phase-locking between SWR, SO and spindles (Latchoumane et al. 2017), and their nesting within hippocampus (Staresina et al. 2015).”
Regional slow waves and spindles in human sleep. (2011, unknown): “The apparent discrepancy with (Wierzynski et al., 2009) is most likely related to the fact that our data represent a different neuronal population in the mPFC where neuronal activity is highly modulated by slow waves (compare to their Figure 1), but differences in species and electrode locations…”
Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus (2009, unknown): “…after the path is complete and can be coherent with activity in neocortical and striatal areas (Chrobak and Buzsá ki, 1996; Ji and Wilson, 2007; Wierzynski et al., 2009; Peyrache et al., 2009; Lansink et al., 2009), reactivation could help link a specific path with reward information encoded…”