The septo-hippocampal system and cognitive mapping

Rawlins, J. N. P.; Olton, David S.

doi:10.1016/0166-4328(82)90039-0

Cited by 223 publications

(111 citation statements)

References 20 publications

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“…Lesions of the fimbria-fornix, or electrolytic or neurotoxic lesions of the medial septum, impair hippocampal-dependent learning and memory (Mahut 1972;Olton et al 1978;Mitchell et al 1982;Rawlins and Olton 1982;Hepler et al 1985;Kelsey and Landry 1988;Markowska et al 1989;Kelsey and Vargas 1993). These studies have been interpreted as supporting the hypothesis that hippocampal ACh is necessary for normal memory function.…”

Section: Lesions Of the Medial Septum Or Its Projectionssupporting

confidence: 54%

Septohippocampal Acetylcholine: Involved in but not Necessary for Learning and Memory?

Parent¹,

Baxter²

2004

Learn. Mem.

175

132

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The neurotransmitter acetylcholine (ACh) has been accorded an important role in supporting learning and memory processes in the hippocampus. Cholinergic activity in the hippocampus is correlated with memory, and restoration of ACh in the hippocampus after disruption of the septohippocampal pathway is sufficient to rescue memory. However, selective ablation of cholinergic septohippocampal projections is largely without effect on hippocampal-dependent learning and memory processes. We consider the evidence underlying each of these statements, and the contradictions they pose for understanding the functional role of hippocampal ACh in memory. We suggest that although hippocampal ACh is involved in memory in the intact brain, it is not necessary for many aspects of hippocampal memory function.The goal of this review is to consider the role of septohippocampal acetylcholine (ACh) in learning and memory processes. The evidence in this regard falls broadly into two different classes. On the one hand, considerable data implicate septohippocampal ACh in memory function. This system is engaged during memory processing, indexed by ACh release or by modification of cholinergic markers, and manipulations that affect memory produce parallel changes in hippocampal cholinergic activity. Furthermore, agents that increase hippocampal cholinergic function are sufficient to reverse memory impairments caused by disruption of the septohippocampal system. However, data from studies of selective lesions of septohippocampal cholinergic neurons with the immunotoxin 192 IgG-saporin call into question the essential role of this system in learning and memory, because these studies generally failed to find severe impairments in memory function. Our goal in this article is to review the data underlying each of these lines of evidence, and to attempt to reconcile these apparently disparate observations.The discrepancy between these lines of evidence might imply that septohippocampal ACh is involved in memory processing, but is not necessary for it to occur. This viewpoint would allow for correlated changes in ACh release and memory, and for the ability of cholinergic agents to reverse memory impairments caused by disruption of septohippocampal function. However, it also would permit memory to proceed relatively normally in the absence of septohippocampal cholinergic input. By describing this viewpoint and its implications for the functional role of hippocampal ACh in memory, we seek to promote the idea that data from lesions are compatible with data from other experimental approaches. Furthermore, we suggest that a convergent approach that incorporates observations from different experimental methods will reveal functional characteristics of hippocampal ACh that would not be apparent from studies using a single strategy.Before discussing the role of this system in cognition, a brief review of its anatomical and neurochemical organization is warranted. The septum is connected to the hippocampus via the fimbria-fornix, which carries projections ...

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Section: Lesions Of the Medial Septum Or Its Projectionssupporting

confidence: 54%

Septohippocampal Acetylcholine: Involved in but not Necessary for Learning and Memory?

Parent¹,

Baxter²

2004

Learn. Mem.

175

132

View full text Add to dashboard Cite

show abstract

“…Consistent with this hypothesis, hippocampal lesions in rodents impair allocentric but not egocentric spatial memory 4,5,19 across a wide variety of tasks including the Morris watermaze, 4,5 the radial maze 3,20 , T-maze rewarded alternation 6 , and many others (see BOX 1). Indeed, the hippocampus plays an important role in allocentric spatial information processing in a great many species, including humans 2,8,9 .…”

Section: What Is Spatial Memory?mentioning

confidence: 60%

“…Spatial navigation and spatial memory are primarily associated with the hippocampus, both in rodents and humans 1,2 . Much of the evidence for this has come from lesion studies using spatial memory tasks, particularly in rodents [3][4][5][6] (see BOX 1), the observation of place cells in rodents 7 , and more recently from fMRI studies in humans 8,9 . However, these approaches are limited in that they typically provide little information about the psychological, synaptic and molecular mechanisms that underlie spatial information processing and thus, they represent only a limited tool for understanding spatial learning and memory.…”

Section: Introductionmentioning

confidence: 99%

Hippocampal synaptic plasticity, spatial memory and anxiety

et al. 2014

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. (2014) 'Hippocampal synaptic plasticity, spatial memory and anxiety.', Nature reviews neuroscience., 15 (3). pp. 181-192. Further information on publisher's website:https://doi.org/10.1038/nrn3677Publisher's copyright statement:Additional information: Use policyThe full-text may be used and/or reproduced, and given to third parties in any format or medium, without prior permission or charge, for personal research or study, educational, or not-for-prot purposes provided that:• a full bibliographic reference is made to the original source • a link is made to the metadata record in DRO • the full-text is not changed in any way The full-text must not be sold in any format or medium without the formal permission of the copyright holders.Please consult the full DRO policy for further details. AbstractRecent studies with transgenic mice lacking NMDARs in the hippocampus challenge head-on the longstanding hypothesis that hippocampal LTP-like mechanisms underlie the encoding and storage of associative, long-term spatial memories. However, it may not be the synaptic plasticity/memory hypothesis that is wrong. Instead, it may be the role of the hippocampus that needs re-examination. We present an account of hippocampal function which explains its role in both memory and anxiety.3

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“…This is in contrast to the GluRA Ϫ/Ϫ mice in which the rewarded-alternation deficit is both profound and lasting, with knock-out mice displaying chance levels of performance even after repeated test sessions (Reisel et al, 2002). In this respect, GluRA Ϫ/Ϫ mice resemble rodents with lesions to the septohippocampal system (Rawlins and Olton, 1982;Gray and McNaughton, 1983), although it should also be noted that impaired synaptic plasticity at any one of several sets of synapses within the septohippocampal system could underlie a spatial WM impairment. Tissue-specific GluRA knock-outs, in which the gene deletion can be limited to just the hippocampus or possibly even to specific subfields within the hippocampus, should resolve this issue.…”

Section: Discussionmentioning

confidence: 76%

A Within-Subjects, Within-Task Demonstration of Intact Spatial Reference Memory and Impaired Spatial Working Memory in Glutamate Receptor-A-Deficient Mice

et al. 2003

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Gene-targeted mice lacking the AMPA receptor subunit glutamate receptor-A (GluRA) (GluR1) and wild-type controls were compared on a radial-maze task in which the same three of six arms were always baited, but in which the rewards of milk were not replaced within a trial. This procedure allowed not only a within-subjects but also a within-trials assessment of both spatial working memory (WM) and reference memory (RM) in GluRA Ϫ/Ϫ mice, using identical spatial cues. In experiment 1, the GluRA Ϫ/Ϫ mice made more WM and RM errors during task acquisition. However, separate groups of GluRA Ϫ/Ϫ and wild-type mice (experiment 2) acquired a purely RM version of the task at a similar rate, using a paradigm with which it was not possible to make WM errors (doors prevented mice from re-entering an arm that they had already visited on that trial). In contrast, mice with hippocampal lesions were dramatically impaired. These results are consistent with the possibility that the WM impairment in the GluRA Ϫ/Ϫ mice during experiment 1 produced interference that disrupted RM acquisition. A WM component was therefore introduced after RM acquisition in experiment 2 (i.e., the mice were no longer prevented from re-entering a previously visited arm). The GluRA Ϫ/Ϫ mice now made considerably more WM errors than did wild-type mice, but simultaneously, RM was only mildly and transiently impaired. These experiments provide additional evidence of a selective spatial WM deficit coexisting with intact spatial RM acquisition in GluRA Ϫ/Ϫ mice, suggesting that different neuronal mechanisms within the hippocampus may support these different kinds of information processing.

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The septo-hippocampal system and cognitive mapping

Cited by 223 publications

References 20 publications

Septohippocampal Acetylcholine: Involved in but not Necessary for Learning and Memory?

Septohippocampal Acetylcholine: Involved in but not Necessary for Learning and Memory?

Hippocampal synaptic plasticity, spatial memory and anxiety

A Within-Subjects, Within-Task Demonstration of Intact Spatial Reference Memory and Impaired Spatial Working Memory in Glutamate Receptor-A-Deficient Mice

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