Theta Phase Modulates Multiple Layer-Specific Oscillations in the CA1 Region

Abstract

It was recently proposed that fast gamma oscillations (60-150 Hz) convey spatial information from the medial entorhinal cortex (EC) to the CA1 region of the hippocampus. However, here we describe 2 functionally distinct oscillations within this frequency range, both coupled to the theta rhythm during active exploration and rapid eye movement sleep: an oscillation with peak activity at ∼80 Hz and a faster oscillation centered at ∼140 Hz. The 2 oscillations are differentially modulated by the phase of theta depending on the CA1 layer; theta-80 Hz coupling is strongest at stratum lacunosum-moleculare, while theta-140 Hz coupling is strongest at stratum oriens-alveus. This laminar profile suggests that the ∼80 Hz oscillation originates from EC inputs to deeper CA1 layers, while the ∼140 Hz oscillation reflects CA1 activity in superficial layers. We further show that the ∼140 Hz oscillation differs from sharp wave-associated ripple oscillations in several key characteristics. Our results demonstrate the existence of novel theta-associated high-frequency oscillations and suggest a redefinition of fast gamma oscillations.

Theta-associated high-frequency oscillations (110–160Hz) in the hippocampus and neocortex

“…Recent work carried out in an independent laboratory corroborated the existence of HFOs in CA1 (Fig. 2b) (Scheffer-Teixeira et al, 2012), and similar theta-associated HFOs were also found in CA3 in vivo (Tort, Komorowski, Kopell, Eichenbaum, unpublished observations). In addition, Jackson et al (2011) have recently shown that the isolated rat hippocampus produces theta-associated HFOs (Fig.…”

“…Previously described, behavior-dependent bands of cortical network activity include delta (1-4 Hz), theta (4-12 Hz), alpha (8-12 Hz), highvoltage spindle (7-12 Hz), beta (12-30 Hz), gamma (30-100 Hz), and sharp wave-associated ripple (100-250 Hz) oscillations (Buzsá ki and Draguhn, 2004;Buzsá ki, 2006;Wang, 2010). In addition to these well-characterized rhythms, a novel type of cortical oscillatory activity in the 110-160 Hz range has been recently described (Scheffer-Teixeira et al, 2012;Tort et al, 2008). For reasons we explain below, in this work we denote this rhythm as high-frequency oscillations (HFOs), but we note that this same pattern of oscillatory activity has also been referred to as ''fast gamma'' (Jackson et al, 2011;Scheffzü k et al, 2011).…”

“…For reasons we explain below, in this work we denote this rhythm as high-frequency oscillations (HFOs), but we note that this same pattern of oscillatory activity has also been referred to as ''fast gamma'' (Jackson et al, 2011;Scheffzü k et al, 2011). The HFOs have been detected in LFP recordings from the hippocampus (Jackson et al, 2011;Scheffer-Teixeira et al, 2012;Tort et al, 2008) and neocortex (Scheffzü k et al, 2011; see also Sirota et al, 2008). In contrast to hippocampal ripples, they characteristically occur superimposed on theta activity and are modulated by the phase of this slower rhythm.…”

Vagus Nerve Stimulation Applied with a Rapid Cycle Has More Profound Influence on Hippocampal Electrophysiology Than a Standard Cycle

“…This suggests that the amount of theta activity in the hippocampus determines to what degree gamma frequencies are modulated by this theta rhythm. The fact that the coupling strength is reduced during VNS is thus most likely an indirect consequence of the VNS-induced decrease in theta power [29,30].…”

“…VNS was associated with a general reduction in broadband 2-100 Hz hippocampal power, which was most prominent in the theta frequency band (4-12 Hz) and gamma frequency ranges (>30 Hz), while little change was observed in an intermediate [15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30] Hz band (Fig. 3a, b).…”