Communication between neocortex and hippocampus during sleep in rodents

Abstract

Both neocortical and hippocampal networks organize the firing patterns of their neurons by prominent oscillations during sleep, but the functional role of these rhythms is not well understood. Here, we show a robust correlation of neuronal discharges between the somatosensory cortex and hippocampus on both slow and fine time scales in the mouse and rat. Neuronal bursts in deep cortical layers, associated with sleep spindles and delta waves͞ slow rhythm, effectively triggered hippocampal discharges related to fast (ripple) oscillations. We hypothesize that oscillation-mediated temporal links coordinate specific information transfer between neocortical and hippocampal cell assemblies. Such a neocortical-hippocampal interplay may be important for memory consolidation.T he means by which ensembles of neurons interact with each other for an effective transfer and storage of information are not well understood. It is generally believed that network oscillatory rhythms within and across structures support these functions (1, 2). One current working hypothesis is that information transfer at the hippocampal-neocortical interface in sleep-wake cycle is involved in the encoding and consolidation of memories (3-12). The oscillatory patterns in these structures are fundamentally different in states of waking and sleep (13-15). Attentive, exploratory behavior is characterized by neocortical fast gamma activity and hippocampal theta͞gamma oscillations (16-18). The most prominent hippocampal pattern during slow wave sleep is a transient burst of CA3-CA1 pyramidal cells associated with a sharp wave in stratum (str.) radiatum and fast field oscillation (140-to 200-Hz ripple) in the CA1 pyramidal layer (19-21). Sleep patterns of the neocortex include thalamocortical sleep spindles (12-18 Hz) and delta waves (1-4 Hz) (13,22). Whether and how these macroscopic rhythms support the coding, transfer, and consolidation of information is not understood.Recently, it has been suggested that hippocampal ripples and sleep spindles in the prefrontal cortex are temporally linked on the scale of Ϸ1 s (23). Whether neurons of the hippocampus and neocortex are involved in a more specific spatiotemporal interaction during sleep remains to be explored. To address this issue, we used multisite recording of unit and field activity in the hippocampus and somatosensory cortex. The somatosensory cortex was chosen because it is the most prominent source of sensory information in the rat (24), and, unlike the prefrontal cortex (25), it does not receive monosynaptic input from the hippocampus. Here, we demonstrate temporal coupling of neuronal activity between the somatosensory cortex and hippocampus on both slow and fine time scales and show that neocortical activity can time the occurrence of hippocampal sharp waves and ripples. Such coupling may assist linking neocortical and hippocampal cell assemblies during slow wave sleep. Materials and MethodsTen male mice (six progeny of C57B6͞J and 129S6͞SvEvTac hybrid mice and four connexin36 knockout; ref. 26;...

Interaction between neocortical and hippocampal networks via slow oscillations

“…Slow oscillation was soon shown also in the human EEG during sleep (Achermann and Borbely, 1997;Amzica and Steriade, 1997;Molle et al, 2002), indicating its crucial importance for neocortical function. An important aspect of slow oscillation is its ability to temporally organize other cortical patterns, such as sleep spindles, gamma oscillations and K complexes (Achermann and Borbely, 1997;Amzica and Steriade, 1997;Molle et al, 2002;Steriade and Amzica, 1998a;Mukovski et al, 2006) and hippocampal sharp wave ripples (Sirota et al, 2003).…”

Targeted memory reactivation of newly learned words during sleep triggers REM-mediated integration of new memories and existing knowledge

“…Tamminen et al (2010Tamminen et al ( , 2013 showed that this integration was associated with sleep spindle activity. This suggests that sleep-associated neural replay may be involved in lexical integration, given that sleep spindles are temporally correlated with the occurrence of hippocampal ripples (Siapas & Wilson, 1998;Sirota et al, 2003), which reflect hippocampal replay of newly acquired memories (Girardeau et al, 2009). …”

Development of large-scale functional networks over the lifespan

“…Increasing evidence suggests that the neuronal interaction between hippocampus and neocortex also plays an important role in memory formation (Jutras et al, 2009;Sirota et al, 2003) and memory functions degrade after damage to the hippocampus (Manns et al, 2003;Zola et al, 2000). Interestingly, we found that the left and right temporal lobes turn out to be the driving forces for the highfrequency overconnectivity in older age, which is directly related to cognitive decline.…”