Encoding, consolidation, and retrieval of contextual memory: Differential involvement of dorsal CA3 and CA1 hippocampal subregions

Daumas, Stéphanie; Halley, Hélène; Francés, Bernard; Lassalle, Jean‐Michel

doi:10.1101/lm.81905

Cited by 225 publications

(169 citation statements)

References 52 publications

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“…Thus, the observed deficits are assumed to be attributed to apomorphine acting on those receptors specifically. Furthermore, these data parallel impairments demonstrated in previous studies involving DA (Murphy et al, 1996;Zahrt et al, 1997) and CA1 dysfunction (Sybirska et al, 2000;Lee and Kesner, 2002;Kesner et al, 2004;Lee and Kesner, 2004a;Remondes and Schuman, 2004;Daumas et al, 2005).…”

Section: Discussionsupporting

confidence: 77%

“…Contemporary analysis of hippocampal function has suggested that memory encoding and retrieval require unique computational processes that are independently supported by specific subregions and pathways projecting into this region (O'Reilly and McClelland, 1994;Treves and Rolls, 1994;Moser and Moser, 1998;Kesner et al, 2004;Daumas et al, 2005;Hasselmo, 2005;Rolls and Kesner, 2006). There is strong evidence suggesting the CA1 subregion plays a significant role in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes (O'Reilly and McClelland, 1994;Treves and Rolls, 1994;Maren et al, 1997;Bertaina-Anglade et al, 2000;Kesner et al, 2004;Lee and Kesner, 2004a;Remondes and Schuman, 2004;Daumas et al, 2005;Hasselmo, 2005;Sharifzadeh et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

“…There is strong evidence suggesting the CA1 subregion plays a significant role in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes (O'Reilly and McClelland, 1994;Treves and Rolls, 1994;Maren et al, 1997;Bertaina-Anglade et al, 2000;Kesner et al, 2004;Lee and Kesner, 2004a;Remondes and Schuman, 2004;Daumas et al, 2005;Hasselmo, 2005;Sharifzadeh et al, 2006). Encoding of information acquired in a Hebb-Williams maze or in contextual fear conditioning, using a within-days analysis, is impaired by targeted lesions to the CA3 and dentate gyrus (DG) subregions, but not from targeted lesions to the CA1 subregion.…”

Section: Introductionmentioning

confidence: 99%

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The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

2007

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Subregional analyses of the hippocampus have suggested a selective role for the CA1 subregion in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes. It remains unclear how the direct cortical projection to CA1 via the perforant path (pp) contributes to these CA1-dependent processes. It has been suggested that dopamine selectively modulates the pp projection to CA1 while having little to no effect on the Schaffer collateral (SC) projection to CA1. This series of behavioral and electro-physiological experiments takes advantage of this pharmacological dissociation to demonstrate that the direct pp inputs to CA1 are critical in CA1-dependent intermediate-term retention and retrieval function. Here we demonstrate that local infusion of the nonselective dopamine agonist, apomorphine (10, 15 μg), into the CA1 subregion of awake animals produces impairments in between-day retention and retrieval, sparing within-day encoding of a modified Hebb-Williams maze and contextual conditioning of fear. In contrast, apomorphine produces no deficits when infused into the CA3 subregion. To complement the behavioral analyses, electrophysiological data was collected. In anesthetized animals, local infusion of the same doses of apomorphine significantly modifies evoked responses in the distal dendrites of CA1 following angular bundle stimulation, but produces no significant effects in the more proximal dendritic layer following stimulation of the SC. These results support a modulatory role for dopamine in the EC-CA1, but not CA3-CA1 circuitry, and suggest the possibility of a more fundamental role for EC-CA1 synaptic transmission in terms of intermediate-term, but not short-term spatial memory.

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Section: Discussionsupporting

confidence: 77%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

2007

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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.

129

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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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“…Reactivation during these periods is initiated by sharp wave-ripple complexes (SPW-R) in the CA3 region of the hippocampus (Buzsaki 1989;Chrobak and Buzsaki 1996;Sullivan et al 2011). Blocking SPW-R events or disrupting the fibers by which they are transmitted to the neocortex impairs the consolidation of recently acquired memories (Daumas et al 2005;Girardeau et al 2009;Jadhav et al 2012).…”

Section: Assumptions Of Smcmentioning

confidence: 99%

New methods for understanding systems consolidation

Tayler

Wiltgen

2013

Learn. Mem.

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According to the standard model of systems consolidation (SMC), neocortical circuits are reactivated during the retrieval of declarative memories. This process initially requires the hippocampus. However, with the passage of time, neocortical circuits become strengthened and can eventually retrieve memory without input from the hippocampus. Although consistent with lesion data, these assumptions have been difficult to confirm experimentally. In the current review, we discuss recent methodological advances in behavioral neuroscience that are making it possible to test the basic assumptions of SMC for the first time. For example, new transgenic mice can be used to monitor the activity of individual neurons across the entire brain while optogenetic approaches provide precise control over the activity of these cells using light stimulation. These tools can be used to examine the reactivation of neocortical neurons during recent and remote memory retrieval and determine if this process requires the hippocampus.

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Encoding, consolidation, and retrieval of contextual memory: Differential involvement of dorsal CA3 and CA1 hippocampal subregions

Cited by 225 publications

References 52 publications

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

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

New methods for understanding systems consolidation

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