The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme

“Computational models have explored the potential theoretical advantages of such cross-frequency coupling (Lisman & Idiart 1995, Varela et al. 2001, Lisman 2005, Neymotin et al. 2011).”

“Phase coding has also been proposed for fast gammaband oscillations (313, 591).”

“, 2010), in accordance to theoretical models (Lisman, 2005).”

“…is converted into a phase code: the stronger the feature value, the earlier the corresponding units will respond within a given oscillation cycle (O’Keefe and Recce, 1993; Hopfield, 1995; Mehta et al., 2002; Margrie and Schaefer, 2003; Buzsáki and Draguhn, 2004; Lisman, 2005; Fries et al., 2007).”

“Extending this theory, it has been suggested that the theta/gamma code model can work as a working memory buffer for encoding episodic memories (Jensen and Lisman, 2005) and for ordering place and episodic memories Fig.”

“This coding principle is hypothesized to underpin spatial navigation in the rodent hippocampus: within a theta cycle a full sequence of locations, from previously to subsequently visited locations, is represented at a rate of one location per gamma cycle [60,61].”

“While nested codes could offer considerable computational advantages by exploiting the synergy of information at different scales, they have rarely been addressed in experimental work (Hopfield, 1995; Lisman, 2005).”

“Experiences are characterized by repeated and novel sequences.”

“In terms of sensory processing, FBC might reflect a mechanism for distinguishing different kinds of information encoded by overlapping neural networks or for organizing the information conveyed with different timescales (Lisman, 2005).”

“First, spike sequences of neurons within theta cycles are temporally compressed representations of the rat’s spatial trajectories (Dragoi andBuzsáki, 2006; Foster andWilson, 2007; Gupta et al., 2012; Lisman, 2005; Wikenheiser and Redish, 2015;Cei et al., 2014).”

“The nested oscillation model has been suggested to apply more broadly beyond the hippocampus (Lisman, 2005), for instance, for visual representations (VanRullen and Koch, 2003).”

“…tests and parallel animal work confirm the assumption that binge drinking (especially multiple successive detoxifications) can result in brain damage in a variety of regions, including those involved in cognitive control (Loeber et al., 2009; Squeglia et al., 2009; Stephens and Duka, 2008).”

“Another possibility relates to the temporal scale of the hippocampal inputs through chunking (Miller 1956; Newell 1990) or the action of a working memory buffer (Jensen & Lisman 2005).”

“Nested gamma oscillations may enable temporal codes that operate relative to the theta cycle to be superimposed upon firing rate codes (Buzsáki and Wang, 2012; Lisman, 2005).”

“It is thought to reflect coherent neural communication and information encoding (Lisman, 2005; Jensen and Colgin, 2007), and has been hypothesized to support processes including perceptual binding, spatial and temporal memory encoding, and information processing (Lisman, 2005).”

“…(Fries, 2005, 2015), hierarchical nesting as indexed by phase-power-coupling (Jensen and Colgin, 2007; Schroeder et al., 2008), phase precession and phase coding (Lisman, 2005; Schyns et al., 2011; Jensen et al., 2014), and gating by pulsed inhibition (Jensen and Mazaheri, 2010).”

“Rhythmic oscillations are thought to play an important role in binding distributed cell assemblies together (Singer, 1993; Lisman, 2005), raising the possibility that ripple oscillations could coordinate memory replay.”

“This would be consistent with theta activity (and perhaps other forms of cortical rhythmicity) functioning to time the passage of packets of information around cortical loops (Miller, 1991) or perform a range of more complex functions (Worden, 1992; Carpenter and Grossberg, 1993; Hasselmo and Wyble, 1997; Jensen and L…”

“…hippocampal formation, phase precession and the temporal sequence compression it implies when places or events are sequentially experienced is thought to underlie rapid encoding of experience (Skaggs et al., 1996; Lisman, 2005; Dragoi and Buzsáki, 2006; Morris, 2006; Maurer and McNaughton, 2007).”

“Phase–amplitude coupling may reflect integration or gating processes across populations of neurons, and thus, may be correlates of neural information processing or encoding (Steriade, 2006; Jensen, 2005; Lisman, 2005; Buzsaki & Draguhn, 2004).”

“This is theoretically elaborated and tested with neural networks ( Lisman, 2005; Jensen and Lisman, 2005; Lisman and Idart, 1995; Jensen, 2004; Jensen, 2006) as well as in human EEG studies (Fell et al., 2003b; Schack et al., 2002; Burgess and Ali, 2002; Palva et al., 2005; Mormann et al., 2005; Demiralp et al., 2007;…”

“First, oscillations segment time into frames (periods), offering a reference for temporal encoding of information in spike latencies (phases) [76].”

“of information encoding in the brain (Lisman, 2005).”

“It has highly consistent behavioural correlates in rats (Vanderwolf, 1969) and its apparent simplicity and ease of recording have resulted in a voluminous literature (Bland, 1986; Winson, 1990; O’Keefe, 1993; Kirk, 1997; Vertes and Kocsis, 1997; Sainsbury, 1998; O’Keefe and Burgess, 1999; Buzsáki, 2002, 2005; Burgess…”

“…al., 2010; Giraud and Poeppel, 2012): spiking activity and gamma oscillations may reflect individual sensory features with high temporal precision (Lisman, 2005; Fries et al., 2007), and their nesting into different phase ranges of theta oscillations may reflect the temporal organization of this…”

“This predicts that information integration is essential for updating internal models of the current situation and reorganizing the temporal structure of cell assemblies within theta cycles (Tsodyks et al., 1996; Lisman, 2005; Hasselmo, 2005; McNaughton et al., 2006; Foster and Knierim, 2012).”

“Gamma oscillatory firing on the linear track Because we found that place-selective firing was maintained during gamma oscillations, it is possible that gamma-modulated temporal sequences are formed during theta-phase precession (Lisman, 2005; Koene and Hasselmo, 2007).”

“A second type of oscillation in the hippocampus, gamma ($25–100 Hz), is thought to interact with theta to temporally organize theta sequences (Dragoi and Buzsá ki, 2006; Gupta et al., 2012; Lisman, 2005; Lisman and Jensen, 2013).”

“We suggest that this embedding takes the form of a generic coding mechanism that is already well established in neuroscience (Lisman, 2005; Buzsaki, 2008): internally generated oscillations at a high frequency such as the gamma range are embedded inside an oscillation operating at a lower frequency…”

“Local fi eld potential (LFP) oscillations are thought to refl ect organization underlying a wide range of processes across different brain areas, including attention, perception, movement planning and initiation, and memory (Buzsáki, 2006; Fries et al., 2007; Lisman, 2005).”

“Note that the number of primes indicates the degree of corruption of a memory item. memory buffer that may provide input to the hippocampus (reviewed in Jensen & Lisman, 2005).”

“Cross-frequency phase-phase coupling has previously been hypothesized to take part in memory processes (Lisman and Idiart, 1995; Jensen and Lisman, 2005; Lisman, 2005; Schack and Weiss, 2005; Sauseng et al., 2008, 2009; Holz et al., 2010; Fell and Axmacher, 2011).”

“…cross-frequency coupling (CFC) between phase and amplitude appears to be important for the integration of local neuronal activity into large-scale cerebral networks (Ward, 2003; Lisman, 2005; Canolty et al., 2006; Jensen and Colgin, 2007; Axmacher et al., 2010; Canolty and Knight, 2010).”

“The encoding of spatiotemporal information in the phase of neural oscillations has been described in the hippocampus in which mechanisms of phase precession encode spatial locations as the animal navigates in a maze (Buzsáki, 2002; Lisman, 2005; Skaggs et al., 1995).”

“firing, the phase of the local field power is used to encode the information [23].”

“It is believed that g rhythms provide coordinating mechanism-binding ensembles of neurons that encode information (Harris et al. 2003; Lisman 2005; Fries 2009).”

“…as time bins, since a) theta oscillations provide temporal windows for organization across hippocampal-cortical networks (Jensen and Lisman, 1996; Lisman, 2005; Lisman and Redish, 2009; Mizuseki et al., 2009; Lisman and Jensen, 2013), and b) since we wanted to investigate the effect of theta…”

“Thus, our finding extends existing models of simultaneous gamma and theta oscillations during memory processes (e.g., Demiralp et al., 2007; Axmacher et al., 2006; Jensen, 2006; Lisman, 2005 ), which propose a mechanism of nested gamma and theta oscillations.”

“…different frequencies has mainly been studied in the hippocampal region (Axmacher et al., 2010; Buzsaki and Draguhn, 2004; Jutras and Buffalo, 2010; Lisman, 2005; Mormann et al., 2005) and, such methods have barely been applied to MEG/EEG data from humans.1 Only recently, hierarchically organized…”

“It has been shown that subthreshold membrane-potential resonances influence a given brain area’s ability to sustain rhythmic activity (Buzsáki and Draguhn 2004; Geisler et al. 2005), which, in turn, underlies various aspects of perception, memory, and behavior (Buzsáki 2005; Lisman 2005).”

“Theta and gamma can and do occur together, with theta modulating gamma and gamma often precipitating theta.(14,18) Investigators are attempting to understand the interplay of gamma and theta because they appear to reflect distinct aspects of information processing.”

“, 2005) and hippocampus (Bragin et al., 1995; Lisman, 2005) and is thought to be central for a number of cognitive and sensory processes (Jensen and Colgin, 2007; Lisman, 2005; Lisman and Idiart, 1995; Schroeder and Lakatos, 2009).”

“Lisman (2005) hypothesized that given the distinct features of the inputs the hippocampus receives from the entorhinal cortex (EC), sensory information from the lateral EC (LEC) and spatial information from the grid cells of the medial EC (MEC), the Dentate Gyrus (DG) could form sense-act couplets…”

“Because theta and gamma activity play a functional role in memory formation and retrieval (Bastiaansen and Hagoort, 2003; Hasselmo, 2005; Lisman, 2005), disruption of septohippocampal projection might explain cognitive deterioration in neurodegenerative diseases.”

“Third, reward-dependent associative learning mechanisms likely involve long-term synaptic modifications depending on the exact timing of presynaptic and postsynaptic activity (Levy and Steward, 1983; Markram et al., 1997; Lisman and Spruston, 2005; Cassenaer and Laurent, 2007).”

“Lisman and colleagues (Lisman and Idiart, 1995; Jensen and Lisman, 1996, 1998; Lisman, 2005) propose that oscillations in the medial temporal lobe could facilitate working memory “bundles” of 7 ± 2 items using a similar phase encoding scheme.”

“Theta phase to gamma amplitude coupling have been extensively studied in the hippocampus of rodents andmanwhere they arewidely believed to reflect the integration of components to a single cognitive stream (Jensen and Lisman, 2005; Lisman, 2005; Lisman andBuzsaki, 2008).”

“Such oscillatory rhythms are involved in many aspects of sensory and cognitive processing 8–15 , and it has been hypothesized that neural oscillations may provide different duration time windows for the chunking or linking of information 10,16–18 .”

“The key argument that heteroassociation occurs in the dentate is that the passage of information from dentate to CA3 and back to dentate requires >20 msec, producing a delay (see references in Lisman 2005) that turns out to be very important.”

“…to produce a neural code (‘‘7 ± 2 short-term memories’’) has been proposed a decade ago (Lisman and Idiart, 1995); later it was improved, but the essence of this theta–gamma coding model was remained (Jensen and Lisman, 2005; Lisman, 2005; Lisman and Buzsáki, 2008; Lisman and Jensen, 2013).”