Localization of Function Within the Dorsal Hippocampus: The Role of the CA3 Subregion in Paired-Associate Learning.

Gilbert, Paul E.; Kesner, Raymond P.

doi:10.1037/0735-7044.117.6.1385

Cited by 128 publications

(134 citation statements)

References 66 publications

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“…Due to the interconnected and serial nature of the hippocampal formation it has, until recently, been thought that damage to parts of the system would challenge the operation of the entire hippocampal circuitry, rendering it impossible to study the specific function of single hippocampal regions using lesion techniques. Our results, however, support accumulating work that demonstrates functional differences between CA3 and CA1 (Gilbert and Kesner 2003;Daumas et al 2005;Ji and Maren 2008), and suggest that these two hippocampal subregions play different roles in supporting memory for the order of events in unique episodes.…”

Section: Discussionsupporting

confidence: 44%

Distinct roles for dorsal CA3 and CA1 in memory for sequential nonspatial events

Farovik¹,

Dupont²,

Eichenbaum³

2009

Learn. Mem.

127

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Previous studies have suggested that dorsal hippocampal areas CA3 and CA1 are both involved in representing sequences of events that compose unique episodes. However, it is uncertain whether the contribution of CA3 is restricted to spatial information, and it is unclear whether CA1 encodes order per se or contributes by an active maintenance of memories of sequential events. Here, we developed a new behavioral task that examines memory for the order of sequential nonspatial events presented as trial-unique odor pairings. When the interval between odors within a studied pair was brief (3 sec), bilateral dorsal CA3 lesions severely disrupted memory for their order, whereas dorsal CA1 lesions did not affect performance. However, when the inter-item interval was extended to 10 sec, CA1 lesions, as well as CA3 lesions, severely disrupted performance. These findings suggest that the role of CA3 in sequence memory is not limited to spatial information, but rather appears to be a fundamental property of CA3 function. In contrast, CA1 becomes involved when memories for events must be held or sequenced over long intervals. Thus, CA3 and CA1 are both involved in memory for sequential nonspatial events that compose unique experiences, and these areas play different roles that are distinguished by the duration of time that must be bridged between key events.Episodic memory involves the ability to encode and retrieve the order of events in individual experiences (Tulving 1983). Recent evidence in both animals and humans indicates that the hippocampus plays a critical role in this capacity. In animals, damage to the hippocampus impairs memory for the order of associated elements that compose an episode Kesner et al. 2002), and hippocampal neuronal activity reflects processing of the order of events in both spatial (Dragoi and Buzsáki 2006;Foster and Wilson 2007) and nonspatial episodes (Manns et al. 2007). In humans, hippocampal activation has also been related to memory for the order of elements (Kumaran and Maguire 2006;Lehn et al. 2009;Ross et al. 2009).Within the hippocampal circuitry, contributions of the CA3 and CA1 fields are probably most extensively studied, but this work has not yet clarified the distinct roles of these areas in sequence memory. Computational models suggest that the recurrent connections of CA3 cells operate as an attractor network that computes associations between elements (Norman and O'Reilly 2003;Rolls 2007) and is suitable for representing sequences of events in episodic memories (Jensen and Lisman 1996;Levy 1996;Lisman 1999). Studies on the effects of selective damage within the hippocampus have shown that CA3 is critical for remembering sequences of spatial locations (Hunsaker et al. 2008a), but not sequences of nonspatial events (Hoge and Kesner 2007). It is, therefore, uncertain whether CA3 is critical for sequence memory per se, rather than other aspects of spatial processing. Other observations suggest that CA1 may be involved in memory for the order of both spatial (Hunsaker et al. 2008a)...

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Section: Discussionsupporting

confidence: 44%

Distinct roles for dorsal CA3 and CA1 in memory for sequential nonspatial events

Farovik¹,

Dupont²,

Eichenbaum³

2009

Learn. Mem.

127

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“…Since neither a CA1 nor CA3-unique neurotoxin is available, we have developed injection parameters suitable to induce subregion-specific lesions with ibotenic acid, which produce selective damage to either CA1 (Gilbert et al, 2001) or CA3 (Gilbert & Kesner, 2003;Jerman, Kesner, Lee, & Berman, 2005; pyramidal cells. Although it is difficult to define the boundary between the dorsal and ventral portions of the hippocampus, the dorsal region was defined as the anterior 50% of the hippocampus (Moser & Moser, 1998).…”

Section: Histologymentioning

confidence: 99%

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

Hoge

Kesner

2007

Neurobiology of Learning and Memory

Self Cite

125

121

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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.

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“…A particularly striking contrast comes from a comparison between two studies by Kesner and colleagues (Gilbert & Kesner, 2003;Kesner, Hunsaker, & Gilbert, 2005). In one experiment, normal rats learned associations between a particular object or odor and their locations in specific places in an open field.…”

Section: Ca1 Versus Ca3mentioning

confidence: 99%

Comparative Cognition, Hippocampal Function, and Recollection

Eichenbaum¹

2006

ccbr

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Localization of Function Within the Dorsal Hippocampus: The Role of the CA3 Subregion in Paired-Associate Learning.

Cited by 128 publications

References 66 publications

Distinct roles for dorsal CA3 and CA1 in memory for sequential nonspatial events

Distinct roles for dorsal CA3 and CA1 in memory for sequential nonspatial events

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

Comparative Cognition, Hippocampal Function, and Recollection

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