Spatial Long-Term Memory Is Related to Mossy Fiber Synaptogenesis

Ramírez‐Amaya, Víctor; Balderas, Israela; Sandoval, J.; Escobar, Martha L.; Bermúdez‐Rattoni, Federico

doi:10.1523/jneurosci.21-18-07340.2001

Cited by 166 publications

(133 citation statements)

References 53 publications

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“…Importantly, this occurs during the 7-d post-training period at a time when the animal is no longer exposed to the training apparatus, experimental room, or experimenters. Thus, the growth process occurs off-line and, as has been previously shown, persists for at least 30 d (Ramirez-Amaya et al 2001).…”

supporting

confidence: 62%

“…Moreover, the significant training-dependent increments in the SOSP of HIDDEN rats were restricted to the rostralmost third of the septal hippocampus ( Fig. 2A), a point emphasized by both Ramirez-Amaya et al (2001) and Holahan et al (2006).In rats sacrificed 48 h after training, the size and relative distribution of MFTFs did not differ as a function of training. Specifically, no significant effect of training on the size of the SOSP, the SL, or the SOSP/SL within the regio inferior was found (data not shown).…”

mentioning

confidence: 84%

mentioning

confidence: 91%

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Remodeling of hippocampal mossy fibers is selectively induced seven days after the acquisition of a spatial but not a cued reference memory task

et al. 2007

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Relating storage of specific information to a particular neuromorphological change is difficult because behavioral performance factors are not readily disambiguated from underlying cognitive processes. This issue is addressed here by demonstrating robust reorganization of the hippocampal mossy fiber terminal field (MFTF) when adult rats learn the location of a hidden platform but not when rats learn to locate a visible platform. Because the latter task requires essentially the same behavioral performance as the former, the observed MFTF growth is seen as the consequence of specific input-dependent hippocampal activity patterns selectively generated by processing of extramaze but not intramaze cues. Successful performance on the hidden platform task requires formation of spatial memory. Increased MFTFs in hidden platform-trained rats are observed 7 d but not 2 d after training nor in swim controls. These results suggest that structural plasticity of the mossy fiber:CA3 circuit may contribute to the maintenance of long-lasting memory but not to the initial storage of the spatial context. Does gross remodeling of anatomical circuits contribute to longterm memory storage? It has long been thought that the act of learning redefines the physical structure of neural connections (e.g., Ramon y Cajal 1905); however, there are few experimental demonstrations of such rearrangements.Recently our group has provided direct evidence of learningdependent structural plasticity by demonstrating that training rats from two different strains (Holahan et al. 2006(Holahan et al. , 2007 to locate a hidden platform in a water maze induces growth of hippocampal granule cell mossy fiber terminal fields (MFTFs) from the stratum lucidum (SL) of CA3 into the stratum oriens (SO) and stratum pyramidale (SP). No growth was observed in swim controls that spent an equivalent period of time in the water maze as trained animals but with no platform present. When mice were trained in the same task no such growth was observed (Rekart et al. 2007).The presence of hippocampal MFTF growth after spatial training in rats is convergent with data from lesion studies in rats (Morris et al. 1982;Sutherland et al. 1983;Moser et al. 1993Moser et al. , 1995 and mice (Logue et al. 1997), which suggests that spatial learning tasks, such as locating a hidden platform, are mediated by the hippocampus (O'Keefe and Nadel 1978;Eichenbaum 2000). Thus, it seems likely that growth of the mossy fibers consequent to spatial learning is driven by spatial learningdependent hippocampal activity.One outstanding issue, however, is whether the learningdependent growth is truly specific for spatial (i.e., hippocampaldependent) learning, an issue raised in the original observations of Ramirez-Amaya et al. (1999. Although no growth was observed in swim control animals that were exposed to an equal amount of time in the pool as hidden platform-trained rats, swim controls, in contrast to trained animals, had no control over the amount of time spent in the pool. Indeed, the most reinf...

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confidence: 62%

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confidence: 84%

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Remodeling of hippocampal mossy fibers is selectively induced seven days after the acquisition of a spatial but not a cued reference memory task

et al. 2007

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“…Numerous early and recent studies demonstrated that a flat retrograde amnesia was induced by lesions of dHC and the entire HC at 0.5-3.5 months in watermaze memory retention (Bolhuis et al, 1994;Mumby et al, 1999; logical changes found in CA3 stratum oriens (Ramirez-Amaya et al, 2001) and may indicate involvement of the CA3 autoassociative network in recent (Nakazawa et al, 2002(Nakazawa et al, , 2003Meilandt et al, 2004) as well as in long-term memory storage and recall. Mapping data support the idea that DG is not only involved in memory encoding but also participates in memory retrieval (Nanry et al, 1989;Lisman, 1999).…”

Section: Discussionmentioning

confidence: 99%

Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

Gusev¹,

Cui²,

Alkon³

et al. 2005

J. Neurosci.

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The understanding of the mechanisms of memory retrieval and its deficits, and the detection of memory underlying neuronal plasticity, is greatly impeded by a lack of precise knowledge of the brain circuitry that underlies the functions of memory. The specific roles of anatomically distinct hippocampal subdivisions in recent and long-term memory retention and recall are essentially unknown. To address these questions, we mapped the expression of Arc/Arg 3.1 mRNA, a neuronal activity marker, in memory retention at multiple rostrocaudal levels of the dentate gyrus, CA3, CA1, subiculum, and lateral and medial entorhinal cortices after a platform search in a water-maze spatial task at 24 h and 1 month compared with swim and naive controls. We found that the entorhinohippocampal neuronal activity underlying the recall of recent and remote spatial memory has an anatomically distributed and time-dependent organization throughout both the dorsal and ventral hippocampus that is subdivision specific. We found a dissociation in the activity of the entorhinal cortex, CA3, and CA1 over a period of memory consolidation. Although CA3, the dorsal hippocampus, and the entorhinal cortex demonstrated the most persistent learning-specific signal during both recent and long-term memory recall, CA1 and the ventral hippocampus displayed the most dramatic signal decline. We determined the coordinates of activity clusters in the hippocampal subdivisions during the platform search and their dynamics over time. Our mapping data suggest that although the level of corticohippocampal interaction is similar during the retrieval of recent and remote spatial memories, the mnemonic function of the hippocampus may have changed, and the activity underlying remote spatial memory could be anatomically segregated within hippocampal subdivisions in small segments.

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“…The learning deficit exhibited by heterozygous Marcks mutant mice appears to be specific to spatial navigation and does not extend to contextual aspects of hippocampal function and is most apparent following prior training to a different spatial location (spatial reversal learning) . Previous studies suggest that mossy fiber synaptic plasticity may be important for hippocampus-dependent spatial learning processes (Ishihara et al, 1997;Lassalle et al, 2000;Ramirez-Amaya et al, 2001), and naturally occurring variations in hippocampal infrapyramidal mossy fiber distribution in inbred mice are specifically correlated with spatial reversal learning performance (Schopke et al, 1991;Bernasconi-Guastalla et al, 1994). In agreement with the pattern of synaptic and behavioral deficits observed in heterozygous Marcks mutant mice, mice lacking the synaptic vesicle binding protein Rab3a also exhibit deficits in mossy fiber LTP, but not PPF or basal synaptic transmission (Castillo et al, 1997), and deficits in spatial reversal learning, but not initial spatial acquisition or contextual fear conditioning (Hensbroek et al, 2003;D'Adamo et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

Myristoylated alanine rich C kinase substrate (MARCKS) heterozygous mutant mice exhibit deficits in hippocampal mossy fiber-CA3 long-term potentiation

et al. 2006

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The myristoylated alanine-rich C kinase substrate (MARCKS) is a primary protein kinase C (PKC) substrate in brain thought to transduce PKC signaling into alterations in the filamentous (F) actin cytoskeleton. Within the adult hippocampus, MARCKS is highly expressed in the dentate gyrus (DG)-CA3 mossy fiber pathway, but is expressed at low levels in the CA3-CA1 Schaffer collateral-CA1 pathway. We have previously demonstrated that 50% reductions in MARCKS expression in heterozygous Marcks mutant mice produce robust deficits in spatial reversal learning, but not contextual fear conditioning, suggesting that only specific aspects of hippocampal function are impaired by reduction in MARCKS expression. To further elucidate the role of MARCKS in hippocampal synaptic plasticity, in the present study we examined basal synaptic transmission, paired-pulse facilitation, post-tetanic potentiation, and long-term potentiation (LTP) in the hippocampal mossy fiber-CA3 and Schaffer collateral-CA1 pathways of heterozygous Marcks mutant and wild-type mice. We found that LTP is significantly impaired in the mossy fiber-CA3 pathway, but not in the Schaffer collateral-CA1 pathway, in heterozygous Marcks mutant mice, whereas basal synaptic transmission, paired-pulse facilitation, and posttetanic potentiation are unaffected in both pathways. These findings indicate that a 50% reduction in MARCKS expression impairs processes required for long-term, but not short-term, synaptic plasticity in the mossy fiber-CA3 pathway. The implications of these findings for the role of the mossy fiber-CA3 pathway in hippocampus-dependent learning processes are discussed.

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Spatial Long-Term Memory Is Related to Mossy Fiber Synaptogenesis

Cited by 166 publications

References 53 publications

Remodeling of hippocampal mossy fibers is selectively induced seven days after the acquisition of a spatial but not a cued reference memory task

Remodeling of hippocampal mossy fibers is selectively induced seven days after the acquisition of a spatial but not a cued reference memory task

Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

Myristoylated alanine rich C kinase substrate (MARCKS) heterozygous mutant mice exhibit deficits in hippocampal mossy fiber-CA3 long-term potentiation

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