Heterogeneity of network and coding states in CA1

Abstract

The hippocampus likely uses temporal coding to represent complex memories via mechanisms such as theta phase precession and theta sequences. Theta sequences are rapid sweeps of spikes from multiple place cells, encoding past or planned trajectories or non-spatial information. Phase precession, the correlation between a place cell's theta firing phase and animal position has been suggested to facilitate sequence emergence. We find that CA1 phase precession varies strongly across cells and environmental contingencies. Phase precession depends on the CA1 network state, and is only present when the medium gamma oscillation (60-90 Hz, linked to Entorhinal inputs) dominates. Conversely, theta sequences are most evident for non-precessing cells or with leading slow gamma (20-45 Hz, linked to CA3 inputs). These results challenge the view that phase precession is the mechanism underlying the emergence of theta sequences and point at a 'dual network states' model for hippocampal temporal code, potentially supporting merging of memory and exogenous information in CA1.

Hippocampal gamma and sharp wave/ripples mediate bidirectional interactions with cortical networks during sleep

“…The instantaneous balance between Slow Gamma and medium gamma may reflect the momentary prevalence of respectively CA3 vs. entorhinal inputs into CA1 (Bragin et al, 1995; Colgin et al, 2009). Correspondingly, a shift between memory retrieval, predictive hippocampal activity and registration and storage of novel cortical inputs may take place (Guardamagna et al, 2021). During sleep, SWR events associated to higher levels of Slow Gamma contain increased replay (Carr et al, 2012).…”

“…Slow Gamma is thought to be related to the routing of information from CA3, a recurrent-rich hippocampal subfield, which for this reason is seen as potentially functioning as an auto-associative memory, and CA1 (Bragin et al, 1995;Colgin et al, 2009). Consistent with this idea, Slow Gamma in wakefulness is related in CA1 with an increase in the predictive features of spatially-related cell activity (Bieri et al, 2014;Cabral et al, 2014;Lasztóczi and Klausberger, 2016) and with the organization of neuronal spiking into ordered sequences (Guardamagna et al, 2021). During sleep, increased Slow Gamma during SWR events correlates with greater replay (Carr et al, 2012).…”

Theta-band phase locking during encoding leads to coordinated entorhinal-hippocampal replay

“…However, this study is the first to show that theta may also play a pivotal, potentially mechanistic, role in the establishment of offline hippocampal-cortical replay synchronisation – a process thought to lie at the heart of long-term memory formation. Given CA1 theta phase locking is thought to underlie the emergence of hippocampal theta sequences(Guardamagna et al, 2022), we hypothesise the dMEC theta phase locking we observed may reflect the emergence of distributed, hippocampal-dMEC theta sequences. As such, cross-structural sequence coupling may underlie the emergence of synchronised hippocampal-dMEC replay and thereby the commission of memories to long-term storage.…”

“…Theta-band oscillations have long been implicated in hippocampal-cortical communication (Jadhav et al, 2016; Jones & Wilson, 2005; Mizuseki et al, 2009; O’Neill et al, 2013) as well as sequence-based plasticity(Drieu et al, 2018; Johnson & Redish, 2007; Muessig et al, 2019). Specifically, phase-locking of CA1 cells to the hippocampal theta-band is thought to underlie the expression of so-called ‘theta-sequences’(Guardamagna et al, 2022) which have been shown to be required for the emergence of hippocampal replay(Drieu et al, 2018). Thus, perhaps the emergence of synergistic hippocampal-dMEC replay is supported by dMEC cells locking similarly to the theta rhythm during encoding?…”

State Dependent Coupling of Hippocampal Oscillations

“…Specifically, during wakefulness, the CA1 region is characterized by cross-frequency coupling between theta and distinct gamma oscillations which exhibit their peak power at distinct phases of ongoing slow oscillations (Belluscio et al, 2012; Buzsáki and Wang, 2012; Colgin et al, 2009; Csicsvari et al, 2003; Scheffer-Teixeira et al, 2012; Yamamoto et al, 2014). The slow, medium and fast gamma oscillations, emerging from stratum radiatum (SR), stratum lacunosum moleculare (SLM) and stratum pyramidale (SP) respectively, are linked to network activity in entorhinal cortex, CA3 and CA1 region respectively (Colgin et al, 2009; Fernández-Ruiz et al, 2017; Guardamagna et al, 2021; Lasztóczi and Klausberger, 2016; Schomburg et al, 2014). During sleep, theta and medium gamma oscillations dominate the REM sleep, whereas delta, spindle frequency band (11-20 Hz, hereafter spindle) and ripples or fast gamma (100-200 Hz), linked to memory consolidation processes, dominate the non-REM sleep (Battaglia et al, 2011; Buzsáki, 1989; Genzel et al, 2014; Roumis and Frank, 2015).…”