Spatial information is preferentially processed by the distal part of CA3: implication for memory retrieval

Flasbeck, Vera; Atucha, Erika; Nakamura, N.; Yoshida, Masatoshi; Sauvage, Magdalena

doi:10.1016/j.bbr.2018.02.046

Cited by 17 publications

(8 citation statements)

References 62 publications

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“…In summary, these findings complement our recent studies that revealed that spatial information (location) and non-spatial information (odors) can be processed in a segregated manner within the hippocampus [ 24 , 25 ] by showing that temporal and spatial information bound to objects engage, at least part of, the same subnetworks. In addition, we identified the distal part of CA1 as a potential “hub” for time cells and showed that the new concept of segregated processing of spatial and non-spatial information within the hippocampus is, to a large extent, reconcilable with the traditional view of an integration of this information at the level of the hippocampus.…”

Section: Discussionsupporting

confidence: 86%

“…The second question of the present study was to assess whether the processing of spatial information bound to objects was topographically organized along the proximodistal axis of the hippocampus as it was shown for locations [ 25 ], i.e., whether it would also preferentially recruit the “spatial” hippocampal subnetwork. Our results show that, in addition to increasing with the temporal discrimination ratio, Arc expression in distal CA1 also increased as a function of the spatial discrimination index, indicating a relative tuning of distal CA1 to spatial information ( Fig 4 ).…”

Section: Discussionmentioning

confidence: 99%

“…(B–D) Schemas of models of information processing in the medial temporal lobe. According to the “segregated” view of information processing in the hippocampus [ 24 , 25 ], only the “spatial” subnetwork (proximal CA1 and distal CA3) would be recruited if the salient dimension of the memory was spatial (panel B), while only the “non-spatial” subnetwork (distal CA1 and proximal CA3) would be engaged if the salient dimension was non-spatial (panel C).Within the frame of the “two-streams model” [ 1 , 2 ], the spatial and non-spatial dimensions of an episode are integrated at the level of the hippocampus. In other words, both the “spatial” (i.e., distal CA3–proximal CA1) and the “non-spatial” (i.e., proximal CA3–distal CA1) hippocampal subnetworks would be recruited in this case (panel D).…”

Section: Introductionmentioning

confidence: 99%

“…Altogether, these findings led us to recently suggest the existence of distinct “spatial” and “non-spatial” hippocampal subnetworks segregated along the proximodistal axis of the hippocampus that would preferentially be engaged either when only the spatial dimension or only the non-spatial dimension of a memory is salient, i.e., when the integration of both dimensions is not “necessary” ( Fig 1B and 1C ) [ 24 , 25 ]. These networks were termed “spatial” and “non-spatial” subnetworks with regards to their relative ability (i.e., not absolute) to process non-spatial and spatial information, i.e., the “non-spatial” subnetwork processes non-spatial information over spatial information, whereas the “spatial” network favors the processing of spatial information over non-spatial information.…”

Section: Introductionmentioning

confidence: 99%

“…In addition, activity differences along the proximodistal axis of CA1 were reported to be attenuated with aging and proximodistal theta activity coherence to be reduced in the dorsal hippocampus of a rodent animal model of epilepsy [ 26 – 27 ]. Furthermore, some of these reports and others also showed a preferential involvement of proximal CA3 for the retrieval of non-spatial memory and that of distal CA3 for the processing of spatial locations [ 24 – 25 ]. Finally, a proximodistal segregation of CA3 was also reported in terms of pattern completion and pattern separation [ 28 – 29 ].…”

Section: Introductionmentioning

confidence: 99%

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The memory for time and space differentially engages the proximal and distal parts of the hippocampal subfields CA1 and CA3

et al. 2018

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A well-accepted model of episodic memory involves the processing of spatial and non-spatial information by segregated pathways and their association within the hippocampus. However, these pathways project to distinct proximodistal levels of the hippocampus. Moreover, spatial and non-spatial subnetworks segregated along this axis have been recently described using memory tasks with either a spatial or a non-spatial salient dimension. Here, we tested whether the concept of segregated subnetworks and the traditional model are reconcilable by studying whether activity within CA1 and CA3 remains segregated when both dimensions are salient, as is the case for episodes. Simultaneously, we investigated whether temporal or spatial information bound to objects recruits similar subnetworks as items or locations per se, respectively. To do so, we studied the correlations between brain activity and spatial and/or temporal discrimination ratios in proximal and distal CA1 and CA3 by detecting Arc RNA in mice. We report a robust proximodistal segregation in CA1 for temporal information processing and in both CA1 and CA3 for spatial information processing. Our results suggest that the traditional model of episodic memory and the concept of segregated networks are reconcilable, to a large extent and put forward distal CA1 as a possible “home” location for time cells.

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Section: Discussionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The memory for time and space differentially engages the proximal and distal parts of the hippocampal subfields CA1 and CA3

et al. 2018

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Disruption of circadian timing increases synaptic inhibition and reduces cholinergic responsiveness in the dentate gyrus

et al. 2021

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We investigated synaptic mechanisms in the hippocampus that could explain how loss of circadian timing leads to impairments in spatial and recognition memory. Experiments were performed in hippocampal slices from Siberian hamsters (Phodopus sungorus) because, unlike mice and rats, their circadian rhythms are easily eliminated without modifications to their genome and without surgical manipulations, thereby leaving neuronal circuits intact. Recordings of excitatory postsynaptic field potentials and population spikes in area CA1 and dentate gyrus granule cells revealed no effect of circadian arrhythmia on basic functions of synaptic circuitry, including long-term potentiation. However, dentate granule cells from circadian-arrhythmic animals maintained a more depolarized resting membrane potential than cells from circadian-intact animals; a significantly greater proportion of these cells depolarized in response to the cholinergic agonist carbachol (10 μM), and did so by increasing their membrane potential threefold greater than cells from the control (entrained) group. Dentate granule cells from arrhythmic animals also exhibited higher levels of tonic inhibition, as measured by the frequency of spontaneous inhibitory postsynaptic potentials. Carbachol also decreased stimulus-evoked synaptic excitation in dentate granule cells from both intact and arrhythmic animals as expected, but reduced stimulus-evoked synaptic inhibition only in cells from control hamsters. These findings show that loss of circadian timing is accompanied by greater tonic inhibition, and increased synaptic inhibition in response to muscarinic receptor activation in dentate granule cells. Increased inhibition would likely attenuate excitation in dentate-CA3 microcircuits, which in turn might explain the spatial memory deficits previously observed in circadian-arrhythmic hamsters.

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The role of hippocampus in memory reactivation: an implication for a therapeutic target against opioid use disorder

Dai

Chen

et al. 2022

Curr Addict Rep

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Purpose of the review The abuse of opioids induces many terrible problems in human health and social stability. For opioid-dependent individuals, withdrawal memory can be reactivated by context, which is then associated with extremely unpleasant physical and emotional feelings during opioid withdrawal. The reactivation of withdrawal memory is considered one of the most important reasons for opioid relapse, and it also allows for memory modulation based on the reconsolidation phenomenon. However, studies exploring withdrawal memory modulation during the reconsolidation window are lacking. By summarizing the previous findings about the reactivation of negative emotional memories, we are going to suggest potential neural regions and systems for modulating opioid withdrawal memory. Recent findings Here, we first present the role of memory reactivation in its modification, discuss how the hippocampus participates in memory reactivation, and discuss the importance of noradrenergic signaling in the hippocampus for memory reactivation. Then, we review the engagement of other limbic regions receiving noradrenergic signaling in memory reactivation. We suggest that noradrenergic signaling targeting hippocampus neurons might play a potential role in strengthening the disruptive effect of withdrawal memory extinction by facilitating the degree of memory reactivation. Summary This review will contribute to a better understanding of the mechanisms underlying reactivation-dependent memory malleability and will provide new therapeutic avenues for treating opioid use disorders.

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Spatial information is preferentially processed by the distal part of CA3: implication for memory retrieval

Cited by 17 publications

References 62 publications

The memory for time and space differentially engages the proximal and distal parts of the hippocampal subfields CA1 and CA3

The memory for time and space differentially engages the proximal and distal parts of the hippocampal subfields CA1 and CA3

Disruption of circadian timing increases synaptic inhibition and reduces cholinergic responsiveness in the dentate gyrus

The role of hippocampus in memory reactivation: an implication for a therapeutic target against opioid use disorder

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