In this study, hippocampal place cells were recorded in a behavioral paradi
gm previously not employed in place-cell research. Rats were exposed to the
same fixed environment for as long as 8-24 h without interruption, while t
he firing of CA1 and CA3 place cells was monitored continuously. The first
finding was that all place cells that were detected at the beginning of the
recording sessions ceased to produce location-specific firing in their ori
ginal firing fields within 2-12 h. This was observed despite the fact that
the animals kept visiting the original firing fields, the hippocampal EEG w
as virtually unchanged, and the discriminated action potentials of the cell
s could be clearly recorded. The second finding was that some complex-spike
cells that produced no spatially selective firing pattern at the beginning
of the recording sessions developed location-specific discharges within 3-
12 h. Thus, place cells can flexibly terminate and develop their spatial fi
ring, even in a fixed environment and during similar behaviors, if that env
ironment is explored continuously for a prolonged period. To explain this p
henomenon, a new place-cell theory is outlined. Accordingly, the high-frequ
ency discharges of these neurons may serve to create, under multiple extrah
ippocampal control and within limited periods, stable engrams for specific
spatial sites in the association cortex where the cognitive map probably re
sides. After the creation of a stable engram, or in the absence of favorabl
e extrahippocampal inputs, place cells may suspend their location-specific
firing in the original field, and initiate the processing of another spatia
l site. (C) 1999 Elsevier Science Inc.