DISCORDANCE OF SPATIAL REPRESENTATION IN ENSEMBLES OF HIPPOCAMPAL PLACE CELLS

The extent to which small ensembles of neighboring hippocampal neurons alter their spatial firing patterns concurrently in response to stimu lus manipulations was examined in young adult rats as well as in aged rats with and without memory impairment. Recordings from CAI and CA3 c ells were taken as rats performed a spatial radial-maze task that empl oyed prominent distal visual stimuli attached to dark curtains surroun ding the maze and local cues on each maze arm provided by inserts with distinctive visual, tactile, and olfactory stimuli. To test the influ ence of the different stimulus subsets, the distal and local cues were rotated 90 degrees in opposite directions (a Double Rotation). In res ponse to this manipulation, place fields could maintain a fixed positi on to room coordinates, rotate with either the local or the distal cue s, disappear, or new fields could appear. On average 79% of the cells within an ensemble responded in the same way, but only 37% of all ense mbles were fully concordant. Typically discordant ensembles had place fields that rotated with one set of cues, whereas the other fields dis appeared or new fields appeared. Ensembles in which the place fields r otated in two opposite directions were less frequent in young rats tha n would be expected by the occurrence of the individual responses, ind icating selective competition between directly conflicting representat ions and ultimate suppression of one. These findings indicate that hip pocampal neurons independently encode distinct subsets of the cues in a complex environment, although processing within the hippocampal netw ork may actively reduce the simultaneous representation of conflicting orientation information. This kind of population activity might refle ct the higher-order organization of new memories within an established knowledge framework or scheme. Concordance was higher in aged memory- impaired rats than in young rats, and the suppression of conflicting r epresentations was absent in these rats. These findings suggest that a ge-related memory impairment is at least in part associated with a dec rease in the scope of information coded and in the coordination of enc oded representations. (C) 1997 Wiley-Liss, Inc.