Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus

Abstract

Summary Neuronal oscillations allow for temporal segmentation of neuronal spikes. Interdependent oscillators can integrate multiple layers of information. We examined phase-phase coupling of theta and gamma oscillators in the CA1 region of rat hippocampus during maze exploration and REM sleep. Hippocampal theta waves were asymmetric, and estimation of the spatial position of the animal was improved by identifying the waveform-based phase of spiking, compared to traditional methods used for phase estimation. Using the waveform-based theta phase, 3 distinct gamma bands were identified: slow gammaS (30-50 Hz), mid-frequency gammaM (50-90 Hz) and fast gammaF (90-150 Hz or epsilon band). The amplitude of each sub-band was modulated by the theta phase. In addition, we found reliable phase-phase coupling between theta and both gammaS and gammaM but not gammaF oscillators. We suggest that cross-frequency phase coupling can support multiple time-scale control of neuronal spikes within and across structures.

Theta–gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts

“…The observation that ACC/ PFC circuits theta-synchronized the activation at a low-gammafrequency band is, to our knowledge, unprecedented in LFP recordings in the primate brain. However, a similar theta to low-gamma P-A correlation has been found in rodents to emerge in medial frontal, entorhinal, and hippocampal circuits (8,26,27,31). In the cortex of nonhuman primates, synchronization of a low (35-55 Hz) gamma-frequency band has recently been described to characterize local LFP and spike-LFP coherence within the macaque frontal eye field (FEF) during sustained selective attention (32) (for a lower 30-to 40-Hz beta/ gamma in LPFC, see ref.…”

“…4). In previous studies, 5-to 10-Hz activity fluctuations were shown to organize distinct band-limited gamma-frequency bands categorized as low (∼35-55 Hz), medium (∼50-90 Hz), and high (epsilon; ∼90-140 Hz) bands, each likely originating in separable underlying circuit motifs (8,11,26). The observation that ACC/ PFC circuits theta-synchronized the activation at a low-gammafrequency band is, to our knowledge, unprecedented in LFP recordings in the primate brain.…”

“…One candidate means to achieve such interareal integration is by synchronizing local processes in distant brain areas to a common process. A rich set of predominantly rodent studies have documented such interareal neuronal interactions in the form of a phase-amplitude (P-A) correlations between lowfrequency periodic excitability fluctuation and high-frequency gamma-band activity (7)(8)(9). It is, however, unknown whether there are reliable cross-frequency P-A interactions between those primate ACC/PFC nodes that underlie flexible attention shifts and, if so, whether P-A correlations are reliably linked to the actual successful deployment of attention (10,11).…”

Mechanisms of physiological and epileptic HFO generation

“…The frequency of these oscillations proved to be modulated by experimental manipulations of the size and duration of the IPSPs as predicted by computer simulations (Whittington et al, 1995). Inhibitory neurons also play a key role in pacing faster physiological activity, in the ripple band 80-250 Hz, as shown by unit recordings in vivo (Ylinen et al, 1995): as mentioned above the distinction between γ and ripples is less clear that it once seemed (Belluscio et al, 2012;Crone et al, 2006;Edwards et al, 2005;Sullivan et al, 2011). However, prolonged highfrequency oscillations based exclusively on synaptic mechanisms are unlikely because neurotransmitter depletion will lead to a strong synaptic depression and thus to termination of these oscillations (Zucker and Regehr, 2002).…”

“…However, we will review some aspects of γ oscillations, partly because they shed some light on HFO mechanisms, and partly because there can be overlap between γ and "ripples", a transient hippocampal HFO in the 100 Hz to 200-250 Hz band. Functionally γ and ripples can coexist under physiological conditions and share mechanisms (Sullivan et al, 2011), or can be linked under the term fast γ (90-150 Hz, with slow γ at 30-50 Hz and mid γ 50-90 Hz) (Belluscio et al, 2012), while other authors call oscillations from ~60 to 200-250 Hz "high γ" (Crone et al, 2006;Edwards et al, 2005).…”