A neural coding scheme formed by the combined function of gamma and theta oscillations

Abstract

Brain oscillations are important in controlling the timing of neuronal firing. This process has been extensively analyzed in connection with gamma frequency oscillations and more recently with respect to theta frequency oscillations. Here we review evidence that theta and gamma oscillations work together to form a neural code. This coding scheme provides a way for multiple neural ensembles to represent an ordered sequence of items. In the hippocampus, this coding scheme is utilized during the phase precession, a phenomenon that can be interpreted as the recall of sequences of items (places) from long-term memory. The same coding scheme may be used in certain cortical regions to encode multi-item short-term memory. The possibility that abnormalities in theta/gamma could underlie symptoms of schizophrenia is discussed.

Figures

Fig. 1.

Recordings of Dual Theta/Gamma Oscillations in the Hippocampus and Various Brain Regions. In some cases, what is clearest in these figures is the theta modulation of gamma amplitude. This modulation is an indication of the interaction of the 2 oscillations within the same network, but it remains unclear whether there is any functional significance of these amplitude changes. (A) Intracellular recording from hippocampal neuron. (B) Field recordings from hippocampus; average triggered on peak of the gamma frequency field potential oscillation. (C) Field recordings from entorhinal cortex. Highly filtered records show the slow theta component in isolation. (D) magnetoencepholography from human midline cortex. (E) Field recording from olfactory cortex. Reproduced with permission from Lisman.

Fig. 2.

Scheme of Theta-Gamma Discrete Phase Code. Two theta cycles are shown, each of which contains 7 gamma cycles. Different items (A–G) are represented by activity in different gamma cycles. The ovals above show the network activity that represents memory A during the first gamma cycle; note that a spatial code of active cells (black) is used to encode the memory. During the next gamma cycle, different cells in the same network are active, thereby encoding memory B. This entire pattern can repeat on the next theta cycle. Note that in this schematic, the theta modulation of gamma amplitude is not shown.

Fig. 3.

Ensembles During the Phase Precession. (A) Schematic showing that firing occurs at earlier theta phase as the rat moves along a track and through the place field. (B) Different CA1 cells (in different colors) respond to different positions along the track. Dots represent spikes as a function of position (x-axis) and theta phase (y-axis); as the rat moves, each neuron systematically changes its preferred phase of spiking within the theta cycle (although at different rates). (C) Cross-correlogram (CCG) between different cell pairs made from data obtained on track. The CCG between the green and red cells peak at zero (red curve), indicating that the cells are part of the same ensemble (always both active at the same theta phase, despite the change in theta phase). In contrast, the green and light blue cells have a 45-ms phase shift (blue circle) and are thus part of different ensembles. (D) The millisecond shift in the CCG is directly proportional to the difference of place field centers. Thus, cells with the same place field fire in a correlated way with no temporal shift; cells with slightly different place fields fire in different ensembles that fire with a temporal shift within a theta cycle. Modified with permission from Dragoi and Buzsaki.

Fig. 4.

Gamma-modulated Firing of Rat Pyramidal Cell During Different States (wt, Waking Theta; wi, Waking Immobility; ss, Slow Wave Sleep; rs, REM Sleep). Dashed line is gamma waveform in field potential. The “waking” data are taken at a time that the theta phase precession was occurring, thus demonstrating that both theta and gamma oscillations influence the timing of firing. Modified from Senior, Huxter, Allen, et al.