ORGANIZATION OF HIPPOCAMPAL CELL ASSEMBLIES BASED ON THETA PHASE PRECESSION.
ARL NSMA, Univ Arizona, Tucson, AZ
The factors that control the spatial tuning of hippocampal neurons are incompletely understood, and there is no generally agreed upon definition of what constitutes a ‘place field’. One factor that must be considered is the phenomenon of ‘phase precession’. As a rat passes through the place field of a particular hippocampal neuron, its spikes shift to earlier phases of the theta rhythm. Except for the special cases discussed herein, the phase shift never exceeds 360º. Moreover, under conditions in which place field sizes change dynamically, precession rate is tightly coupled with the place field size, suggesting that a single cycle of theta phase precession could be used to define unitary place field boundaries. Theta phase precession implies that the ‘cell assembly’ of active hippocampal neurons changes systematically over the course of a single theta cycle. A segment of the overall sequence of place fields as a rat follows a route is thus compressed within a single theta cycle. A given cell can exhibit more than one place field in a given environment, each field showing the same pattern of 360º of phase precession. The existence of multiple fields implies that one cell can participate in multiple cell assemblies within the same environment. We show here that place fields, defined as a single cycle of phase precession, can overlap spatially, with the result that the cell fires with spikes clustered at two different phases over the theta cycles in which the fields overlap. Thus, the same neuron can participate in different cell assemblies within a single theta cycle. Overlapping fields (and cycles of phase precession) pose a significant challenge for explanations of the phase precession phenomenon based solely on intrinsic membrane dynamics of hippocampal neurons, and favor network level explanations, based on learning-related or intrinsic asymmetries in the synaptic connection matrix. Such models carry the additional implication that the region of space over which the hippocampal place cell is driven by extrinsic inputs, as opposed to intrinsic inputs, is much smaller than the classical place field.
Supported by: NS020331, AG012609