Hippocampal theta bursting and waveform shape reflect CA1 spiking patterns

Abstract

Brain rhythms are nearly always analyzed in the spectral domain in terms of their power, phase, and frequency. While this conventional approach has uncovered spike-field coupling, as well as correlations to normal behaviors and pathological states, emerging work has highlighted the physiological and behavioral importance of multiple novel oscillation features. Oscillatory bursts, for example, uniquely index a variety of cognitive states, and the nonsinusoidal shape of oscillations relate to physiological changes, including Parkinson's disease. Open questions remain regarding how bursts and nonsinusoidal features relate to circuit-level processes, and how they interrelate. By analyzing unit and local field recordings in the rodent hippocampus, we uncover a number of significant relationships between oscillatory bursts, nonsinusoidal waveforms, and local inhibitory and excitatory spiking patterns. Bursts of theta oscillations are surprisingly related to a decrease in pyramidal neuron synchrony, and have no detectable effect on firing sequences, despite significant increases in neuronal firing rates during periods of theta bursting. Theta burst duration is predicted by the asymmetries of its first cycle, and cycle asymmetries relate to firing rate, synchrony, and sequences of pyramidal neurons and interneurons. These results provide compelling physiological evidence that time-domain features, of both nonsinusoidal hippocampal theta waveform and the theta bursting state, reflects local circuit properties. These results point to the possibility of inferring circuit states from local field potential features in the hippocampus and perhaps other brain regions with other rhythms.

Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks

“…We also included running speed as it has been shown to co-vary with the power and frequency of hippocampal gamma oscillations ( Ahmed and Mehta, 2012 ; Zheng et al, 2015 ). We considered two factors to measure theta asymmetry: the ratio between the duration of rise and decay phases in each cycle and the ratio between the duration of the peak and the trough ( Cole and Voytek, 2018 ; see Materials and methods). The analysis confirmed the influence of theta power and speed on gamma power ( Zheng et al, 2015 ; Figure 3—figure supplement 2 ), and a negligible contribution of theta asymmetry.…”

Mammillothalamic disconnection alters hippocampo-cortical oscillatory activity and microstructure: Implications for diencephalic amnesia

“…Phase entrainment of RSC interneurons is independent of hippocampal input (Talk et al, 2004). Recent modelling of the dynamics of spike-phase coupling in the context of theta cycle asymmetry (Cole and Voytek, 2018) present an interesting case that the duration of phase within a cycle is related to the firing frequency of phase-locked neurons such that longer duration descending phases in RSC may provide for a longer window in which firing activity may reach peak frequency, thus resulting in increased frequency activity. In the context of our findings, such a mechanism may serve to link the lesion-related changes in descending phase duration in RSC ( Fig.…”

Instantaneous amplitude and shape of postrhinal theta oscillations differentially encode running speed

“…Neural oscillations, however, change rapidly with time (Burns et al, 2011;Lopesdos-Santos et al, 2018), with no two consecutive cycles being alike. Each single oscillatory cycle has instantaneous properties that can be quantified in the time domain, including amplitude, duration, nested oscillatory components, and waveform shape (Cole and Voytek, 2018;Gupta et al, 2012;Lopes-dos-Santos et al, 2018;Nelli et al, 2017;Zhang et al, 2019). These instantaneous cycle-by-cycle features can provide information that is complementary to that gained from spectral techniques (Amemiya and Redish, 2018;Cole and Voytek, 2018;Gupta et al, 2012;Lopes-dos-Santos et al, 2018;Nelli et al, 2017;Schaworonkow and Nikulin, 2019) and are the focus of the current study.…”