Distinct directional couplings between slow and fast gamma power to the phase of theta oscillations in the rat hippocampus

Haiteng Jiang,Marcel A J Van Gerven,Ali Bahramisharif,Ole Jensen

doi:10.1111/ejn.14644

Abstract

It is well-established that theta (~4-10Hz) and gamma (~25-100Hz) oscillations interact in the rat hippocampus. This cross-frequency coupling might facilitate neuronal coordination both within and between brain areas. However, it remains unclear whether the phase of theta oscillations controls the power of slow and fast gamma activity or vice versa. We here applied spectral Granger causality, phase slope index and a newly developed cross-frequency directionality (CFD) measure to investigate directional interactions between local field potentials recorded within and across hippocampal subregions of CA1 and CA3 of freely exploring rats. Given the well-known CA3 to CA1 anatomical connection, we hypothesized that interregional directional interactions were constrained by anatomical connection, and within-frequency and cross-frequency directional interactions were always from CA3 to CA1. As expected, we found that CA3 drove CA1 in the theta band, and theta phase-to-gamma power coupling was prominent both within and between CA3 and CA1 regions. The CFD measure further demonstrated thatdistinct directional couplings with respect to theta phase was different between slow and fast gamma activity. Importantly, CA3 slow gamma power phase-adjusted CA1 theta oscillations, suggesting that slow gamma activity in CA3 entrains theta oscillations in CA1. In contrast, CA3 theta phase controls CA1 fast gamma activity, indicating that communication atCA1 fast gamma is coordinated byCA3 theta phase. Overall, these findings demonstrate dynamic directional interactions between theta and slow/fast gamma oscillations in the hippocampal network, suggesting that anatomical connections constrain the directional interactions.

Highlights

Neuronal oscillations are believed to play a fundamental role in shaping the functional architecture of the hippocampus (Csicsvari et al, 2003)
A cluster permutation approach was applied to statically access the difference in Granger causality (GC) values while controlling for multiple comparisons over frequency bins. This was done by keeping the original CA3 while circularly shifting a random number of time points in CA3 are bigger than 1 (CA1) 1000 times and recalculating the GC difference t-maps to obtain a reference distribution. This analysis confirmed that the GC influence from CA3 to CA1 was significantly stronger than the influence from CA1 to CA3 in the theta band (Figure 2c)
We confirmed the presence of prominent coupling between theta phase and gamma power within and between CA3 and CA1 regions (Bragin et al, 1995; Colgin et al, 2009; Belluscio et al, 2012)

Summary

Introduction

Neuronal oscillations are believed to play a fundamental role in shaping the functional architecture of the hippocampus (Csicsvari et al, 2003). Bursts of gamma oscillations (∼25 – 100 Hz) are phase-locked to theta oscillations (∼4 – 10 Hz) in the hippocampal circuit; a process called cross-frequency coupling (CFC) (Bragin et al, 1995) This theta-gamma coupling occurs prominently in exploring rats (Bragin et al, 1995; Csicsvari et al, 2003; Colgin et al, 2009; Belluscio et al, 2012; Buzsaki & Wang, 2012; Jackson et al, 2014) and is proposed to play a key role in memory and spatial information processing (Hasselmo et al, 2002b; Buzsaki & Moser, 2013; Lisman & Jensen, 2013; Lopes-Dos-Santos et al, 2018). Slow and fast gamma oscillations are suggested to correspond to distinct functional states in the entorhinal-hippocampal network (Colgin, 2015a)

Methods

Results

Conclusion