Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects

Abstract

Previous research in the dorsal CA1 and dorsal CA3 subregions of the hippocampus has been shown to play an important role in mediating temporal order memory for spatial location information. What is not known is whether the dorsal CA3 and dorsal CA1 subregions of the hippocampus are also involved in temporal order for visual object information. Rats with dorsal CA1, dorsal CA3 or control lesions were tested in a temporal order task for visual objects using an exploratory paradigm. The results indicated that the controls and the dorsal CA3 lesioned rats preferred the first rather then the last object they had explored previously, indicating good memory for temporal order of object presentation. In contrast, rats with dorsal CA1 lesions displayed a profound deficit in remembering the order of the visual object presentations in that they preferred the last object rather than the first. All three groups of rats preferred a novel object compared to a previously explored object suggesting normal detection of visual object novelty. The results suggest that only the dorsal CA1, but not dorsal CA3, region is critical for processing temporal information for visual objects without affecting the detection of new visual objects.

Introduction

The hippocampus has been shown to play an important role in processing of temporal information (Kesner, 1998, Levy, 1996, Lisman, 1999, Rolls and Kesner, 2006). More specifically the hippocampus supports processing of temporal order, recency discrimination or temporal pattern separation for spatial location and order information in that a lesion of the hippocampus produces temporal order memory deficits (Chiba et al., 1994, Fortin et al., 2002, Gilbert et al., 1998, Kesner et al., 2002). Similar results were obtained for temporal order memory for spatial locations in hypoxic subjects with hippocampal damage (Hopkins et al., 1995a, Hopkins et al., 1995b). It should be noted that patients with prefrontal lobe damage or rats with medial prefrontal cortex lesions also have difficulty in temporal order memory for spatial location information (for a review see Kesner, 1998). There are likely to be important interactions between the hippocampus and the prefrontal cortex. With respect to a subregional locus for processing temporal order for spatial locations, it has been reported that the dorsal CA1, but not dorsal dentate gyrus, is of critical importance in that dorsal CA1, but not dorsal dentate gyrus, lesions disrupt performance on a temporal order for spatial location information task (Gilbert, Kesner, & Lee, 2001). Based on unpublished data it appears that the dorsal CA3 also produces a deficit in processing temporal order for spatial information (Kesner and Gilbert, unpublished observation).

It would be of interest to extend the above mentioned finding to temporal order memory for visual object information. A modified paradigm was used based on previous research described by Mitchell and Laiacona (1998) and Hannesson, Howland, and Phillips (2004). They showed that rats when exposed to two or three different sets of objects select on a subsequent preference or recency discrimination test between the first or second and the third of the previously experienced objects the earlier of the two objects. As a control, normal rats when given a test between the first or the second and a novel object select the novel object. They show that rats with medial prefrontal or perirhinal cortex lesions disrupt recency discrimination or temporal order for visual objects without altering their preference for the novel object or recognition memory for the visual objects. The purpose of the present study was to use this new paradigm to examine temporal order memory for visual object information to examine whether both the dorsal CA1 and CA3 regions are critical for processing of temporal information for objects or whether the dorsal CA3 region only processes temporal information for space, but not for objects, in which case there would not be a deficit for dorsal CA3. Alternatively dorsal CA1 may mediate temporal processing for both spatial and nonspatial information and thus, there might be a deficit for visual object information.