Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1

Gilbert, Paul E.; Kesner, Raymond P.; Lee, Inah

doi:10.1002/hipo.1077

Cited by 553 publications

(597 citation statements)

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“…Multiple theories have hypothesized that the hippocampus serves to reduce interference via a process referred to as pattern separation (Marr 1971;Shapiro and Olton 1994;McClelland et al 1995;Rolls 1996). Given its sparse pattern of activity (Barnes et al 1990;Chawla et al 2005), particular attention has been paid to the DG as a potential mediator of pattern separation (Gilbert et al 2001;Lee et al 2004;Leutgeb et al 2007;Clelland et al 2009). A failure in pattern separation may provide an alternative explanation for the deficits we observe in our ADX rats.…”

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confidence: 77%

“…Despite the short retention, the behavior of ADX rats was impaired specifically in the object/context mismatch task. Prior research has demonstrated that larger disruptions of DG function can also impair novel object preference (Lee et al 2005;Jessberger et al 2009) and spatial behavior (Sutherland et al 1983;Xavier et al 1999;Gilbert et al 2001). A possible explanation for this disparity is that discriminations based upon context may typically require a higher degree of complexity in information load, resulting in a greater sensitivity to DG granule cell layer disruption.…”

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confidence: 99%

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Object/context-specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats

Spanswick¹,

Sutherland²

2010

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Chronic adrenalectomy (ADX) causes a gradual and selective loss of granule cells in the dentate gyrus (DG) of the rat. Here, we administered replacement corticosterone to rats beginning 10 wk after ADX. We then tested them in three discrimination tasks based on object novelty, location, or object/context association. Only during testing of the object/context association did ADX rats demonstrate deficits. These findings add to a body of evidence that the hippocampus is necessary when contextual information is important. We also confirm that memory deficits after chronic adrenalectomy are not a result of loss of corticosterone per se.Research with rats (Sutherland and McDonald 1990;Kim and Faneslow 1992;Anagnostaras et al. 2001;Lehmann et al. 2009), nonhuman primates (Machado and Bachevalier 2006;Pascalis et al. 2009), and humans (Alvarez et al. 2008;Marschner et al. 2008) shows that hippocampal damage can disrupt the ability to recall or express information about context. Furthermore, several reports suggest that the hippocampus is important for creating flexible representations of context and object associations. Studies in rats (Mumby et al. 2002;O'Brien et al. 2006) and humans (Pascalis et al. 2009) show that lesions specific to the hippocampus produce deficits in object recognition only when contextual information is altered.Within the hippocampus, the dentate gyrus (DG) is important for certain aspects of memory (Xavier et al. 1999;Garthe et al. 2009). Chronic adrenalectomy (ADX) causes a gradual and selective loss of granule cells in the DG of the rat (Sloviter et al. 1989). This loss of cells is attributed to a lack of circulating corticosterone (CORT) (Sloviter et al. 1989;Woolley et al. 1991). Behavioral deficits as a result of chronic ADX have been reported in the Morris water task (Armstrong et al. 1993;Roozendaal et al. 1998;Spanswick et al. 2007) and open-field task (Islam et al. 1995). There has been debate as to whether the deficits experienced by ADX rats are a result of lost CORT or due to the depletion of the granule cell layer itself. Conrad and Roy (1995) and McCormick et al. (1997) report that acute CORT replacement is sufficient to alleviate some of the deficits in spatial tasks associated with chronic ADX. These findings have led some to conclude that the removal of CORT is responsible for the behavioral deficits experienced by ADX rats and not the loss of granule cells per se. In direct contrast to these findings, Spanswick et al. (2007) report that administration of CORT after 6 wk of ADX does not alleviate spatial deficits in a moving-platform version of the Morris water task. Also in opposition to Conrad and Roy (1995) and McCormick et al. (1997), studies utilizing colchicine as a method to remove granule cells report spatial deficits as a result of cell loss (Sutherland et al. 1983;Xavier et al. 1999;Jeltsch et al. 2001).Here, we show using three versions of a novelty-preference task (novel object, novel place, and object/context mismatch) that lesions limited to the granule cell layer...

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confidence: 77%

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Object/context-specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats

Spanswick¹,

Sutherland²

2010

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“…Within the hippocampus, computational, electrophysiological and lesion evidence has implicated the dentate gyrus (DG) in pattern separation, and subfields CA3 and CA1 in pattern separation or completion, depending on the degree of overlap between incoming and existing representations (Gilbert et al, 2001;Guzowski et al, 2004;Leutgeb et al, 2007;Rolls, 2007;Vazdarjanova and Guzowski, 2004). High-resolution functional magnetic resonance imaging (fMRI) evidence from humans is consistent with these findings.…”

Section: Introductionmentioning

confidence: 86%

Cortical pattern separation and item-specific memory encoding

Pidgeon

Morcom

2016

Neuropsychologia

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Pattern separation and pattern completion are fundamental brain processes thought to be critical for episodic memory encoding and retrieval, and for discrimination between similar memories. These processes are best understood in the hippocampus, but are proposed to occur throughout the brain, in particular in sensory regions. Cortical, as well as hippocampal, pattern separation may therefore support formation of event-unique memory traces. Using fMRI, we investigated cortical pattern separation and pattern completion and their relationship to encoding activity predicting subsequent item-specific compared to gist memory. During scanning, participants viewed images of novel objects, repeated objects, and objects which were both perceptually and conceptually similar to previously presented images, while performing a size judgement task. In a later surprise recognition test, they judged whether test items were 'same' 'similar' or 'new' relative to studied items. Activity consistent with pattern separation -responses to similar items as if novel -was observed in bilateral occipito-temporal cortex. Activity consistent with pattern completion -responses to similar items as if repeated -was observed in left prefrontal cortex and hippocampus. Curve fitting analysis further revealed that graded responses to change in image conceptual and perceptual similarity in bilateral prefrontal and right parietal regions met specific computational predictions for pattern separation for one or both of these similarity dimensions. Functional overlap between encoding activity predicting subsequent item-specific recognition and pattern separation activity was also observed in left occipital cortex and bilateral inferior frontal cortex. The findings suggest that extrahippocampal regions including sensory and prefrontal cortex contribute to pattern separation and pattern completion of visual input, consistent with the proposal that cortical pattern separation contributes to formation of item-specific memory traces, facilitating accurate recognition memory.

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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%

“…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 *Correspondence and requests for offprint copies should be addressed to R. P. K. Raymond P. Kesner, University of Utah, Department of Psychology, 380 South 1530 East, Room 502, Salt Lake City, UT 84112,rpkesner@behsci.utah.edu.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, and 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 observations).…”

Section: Introductionmentioning

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

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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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Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1

Cited by 553 publications

References 29 publications

Object/context-specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats

Object/context-specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats

Cortical pattern separation and item-specific memory encoding

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

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