How Many Gammas? Redefining Hippocampal Theta-Gamma Dynamic During Spatial Learning

Abstract

The hippocampal formation is one of the brain systems in which the functional roles of coordinated oscillations in information representation and communication are better studied. Within this circuit, neuronal oscillations are conceived as a mechanism to precisely coordinate upstream and downstream neuronal ensembles, underlying dynamic exchange of information. Within a global reference framework provided by theta (θ) oscillations, different gamma-frequency (γ) carriers would temporally segregate information originating from different sources, thereby allowing networks to disambiguate convergent inputs. Two γ sub-bands were thus defined according to their frequency (slow γ, 30–80 Hz; medium γ, 60–120 Hz) and differential power distribution across CA1 dendritic layers. According to this prevalent model, layer-specific γ oscillations in CA1 would reliably identify the temporal dynamics of afferent inputs and may therefore aid in identifying specific memory processes (encoding for medium γ vs. retrieval for slow γ). However, this influential view, derived from time-averages of either specific γ sub-bands or different projection methods, might not capture the complexity of CA1 θ-γ interactions. Recent studies investigating γ oscillations at the θ cycle timescale have revealed a more dynamic and diverse landscape of θ-γ motifs, with many θ cycles containing multiple γ bouts of various frequencies. To properly capture the hippocampal oscillatory complexity, we have argued in this review that we should consider the entirety of the data and its multidimensional complexity. This will call for a revision of the actual model and will require the use of new tools allowing the description of individual γ bouts in their full complexity.