The activity of 378 single neurons was recorded from areas of the parahippocampal region (PHR), including the perirhinal and lateral entorhinal cortex, as well as the subiculum, in rats performing an odor-guided delayed nonmatching-to-sample task. Nearly every neuron fired in association with some trial event, and every identifiable trial event or behavior was encoded by neuronal activity in the PHR. The greatest proportion of cells was active during odor sampling, and for many cells, activity during this period was odor selective. In addition, odor memory coding was reflected in two general ways. First, a substantial proportion of cells showed odorselective activity throughout or at the end of the memory delay period. Second, odor-responsive cells showed odor-selective enhancement or suppression of activity during stimulus repetition in the recognition phase of the task. These data, combined with evidence that the PHR is critical for maintaining odor memories in animals performing the same task, indicate that this cortical region mediates the encoding of specific memory cues, maintains stimulus representations, and supports specific match-nonmatch judgments critical to recognition memory. By contrast, hippocampal neurons do not demonstrate evoked or maintained stimulusspecific codings, and hippocampal damage results in little if any decrement in performance on this task. Thus it becomes increasingly clear that the parahippocampal cortex can support recognition memory independent of the distinct memory functions of the hippocampus itself. Key words: entorhinal cortex; perirhinal cortex; subiculum; hippocampus; recognition memory; delayed nonmatching; single unitsThe parahippocampal region (PHR) has become a focus for anatomical, behavioral, and electrophysiological studies of the medial temporal lobe memory system (Eichenbaum et al., 1994;Brown, 1996;Murray, 1996;Suzuki, 1996). This cortical area surrounds the hippocampus and amygdala and is composed of several distinct subdivisions, including the perirhinal, entorhinal, and parahippocampal (in monkeys) or postrhinal (in rats) cortices (Witter et al., 1989;Burwell et al., 1995). The PHR receives inputs from widespread secondary or "association" cortical regions and provides the major conduit for hippocampal outputs to the same cortical association areas. This anatomical evidence indicates that the PHR occupies a pivotal position for mediating memory functions of the hippocampal region.Neuropsychological findings indicate that the PHR indeed plays a critical role in recognition memory, independent of its role as an intermediary for cortical-hippocampal interactions (Eichenbaum et al., 1994;Murray, 1996). This evidence comes mainly from experiments examining the effects of damage to the hippocampal region on performance in a simple recognition memory test known as delayed nonmatching to sample (DNMS) (Eichenbaum et al., 1994). In the standard version of this task, originally devised by Gaffan (1974), animals are presented with a novel "sample" cue and then after a...
The observation of hippocampal place cells forms a major line of evidence supporting the view that the hippocampus is dedicated to spatial processing. However, most studies demonstrating the spatial properties of hippocampal unit activity have employed tasks that emphasize spatial cues but minimize nonspatial cues. In the present experiment we recorded the activity of hippocampal complex-spike cells from rats performing a nonspatial radial maze task. Performance in this task was guided by local visual-tactile cues on the maze arms, while distal spatial cues were minimized and made irrelevant. The influence of three variables on unit activity was examined:type of cue on an arm, spatial location of an arm, and the relative position of the animal on an arm. Of the units recorded, almost one-fifth were classified as “cue cells” in that their activity was associated with cue type but not spatial location. Conversely, a similar proportion of the units were classified as “place cells” in that their activity was associated with location, but not cue type. In an additional similar proportion of units, firing was influenced only by relative position and not by local cues or spatial locations. For the majority of units, however, firing was related to combinations of these three variables, indicating that most hippocampal neurons encoded conjunctions or relations between spatial and local cue information. This pattern of results indicates that when local rather than distal spatial cues are emphasized, hippocampal neural activity is strongly influenced by salient nonspatial cues and shows no overwhelming predominance of place coding. These findings are at odds with the hypothesis that the hippocampus is selectively involved in spatial processing and, conversely, support the broader view that the hippocampus encodes both spatial and nonspatial relations among important experimental variables.
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