Scientific Understanding of Consciousness
Grid Cells and Theta Oscillations
Science 29 April 2011: Vol. 332 no. 6029 pp. 592-595
Julie Koenig, Ashley N. Linder, Jill K. Leutgeb, and Stefan Leutgeb
Neurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, USA.
Grid cells in parahippocampal cortices fire at vertices of a periodic triangular grid that spans the entire recording environment. Such precise neural computations in space have been proposed to emerge from equally precise temporal oscillations within cells or within the local neural circuitry. We found that grid-like firing patterns in the entorhinal cortex vanished when theta oscillations were reduced after intraseptal lidocaine infusions in rats. Other spatially modulated cells in the same cortical region and place cells in the hippocampus retained their spatial firing patterns to a larger extent during these periods without well-organized oscillatory neuronal activity. Precisely timed neural activity within single cells or local networks is thus required for periodic spatial firing but not for single place fields.
Brain oscillations are thought to be essential for neural computations and for organizing cognitive processes. Yet it has been difficult to distinguish computations in neural circuits that require oscillatory neural activity from those that occur irrespective of the precise temporal organization that oscillatory rhythms can provide.
Theta oscillations (4 to 11 Hz) can be recorded in the local field potential of the hippocampus and the parahippocampal cortices, including the entorhinal cortex. These brain regions are important for memory and navigation and contain a number of different cell types with precise spatial firing patterns, such as place cells, head-direction cells, and grid cells. Grid cells are found in the medial entorhinal cortex (MEC), parasubiculum, and presubiculum and have multiple firing peaks that form a highly regular hexagonal firing pattern in two-dimensional space.
The coexistence of cells with well-defined spatial firing patterns and of theta oscillations that are particularly prominent during voluntary movement suggests that oscillatory brain activity might be essential for spatial computations. In particular, it has been proposed that precisely tuned theta oscillations, as an animal moves through its environment, might be necessary for generating the periodic spatial firing of grid cells. Such spatial regularity might arise from interference between oscillators with small frequency differences, given that those oscillators are controlled by both movement velocity and movement direction. Although the oscillators could be implemented in various ways in single neurons or local circuits, at least one of them would likely be phase-locked to theta oscillations. We tested the hypothesis that reducing theta oscillations by inactivating inputs from the subcortical pacemakers in the medial septal area would disrupt the spatial computations of grid cells.
To explore the effects of reduced theta oscillations on spatial firing patterns, we trained 14 rats to randomly forage in a 1.2-m–by–1.2-m box and recorded the local field potential (LFP) and cells in the superficial layers of the MEC (n = 90 cells) and in the hippocampus (n = 64) during four consecutive 10-min recording sessions.
By silencing the septal area, we diminished theta oscillations in the entorhino-hippocampal circuitry and showed that the periodic firing of grid cells does not persist. Subcortical inputs to hippocampus and parahippocampal cortices are thus essential not only for theta oscillations but also for sustaining the spatial periodicity of grid cells. These findings are consistent with the theory that grid cells emerge from the interference between multiple precisely tuned theta oscillations within individual cells. Alternatively, the silencing of septal inputs to the MEC might result in the desynchronization of grid cells, so that the local network of cortical cells can no longer generate oscillatory interference. Our data also identified a subpopulation of grid cells that do not regain their spatial regularity when theta oscillations recover. This suggests that a fraction of grid cells might not be directly participating in the generation of grid patterns, but rather becomes associated with other grid cells by plasticity-dependent mechanisms.
Our results show that the neuronal network mechanisms that sustain the periodic spatial firing of grid cells are different from those required for other firing correlates in the entorhino-hippocampal circuitry, including head-direction cells and place cells. The effect on grid cells is likely not mediated through effects of septal silencing on the firing of hippocampal place cells, because it has been shown that grid cell firing initially remains intact after the hippocampus has been silenced. Subcortical inputs are therefore necessary for the neural computations in the MEC that generate grid-like, periodic, spatial firing patterns, whereas the firing locations of place cells largely persist after inputs from grid cells and from subcortical areas to the hippocampus have substantially changed.
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