Hippocampal activation during the recall of remote spatial memories in radial maze tasks

Schlesiger, Magdalene I.; Cressey, John C.; Boublil, Brittney L.; Koenig, Julie; Melvin, Neal R.; Leutgeb, Jill K.; Leutgeb, Stefan

doi:10.1016/j.nlm.2013.05.007

Cited by 24 publications

(20 citation statements)

References 44 publications

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“…First, damage to the DG was partial: the upper blade of the DG was not affected, while lesions to the lower blade of the DG were incomplete (Figure 2A). Second, DG seems to be involved primarily during early stages of spatial memory formation (Lee and Kesner, 2004; Jerman et al, 2006; Poirier et al, 2008; Schlesiger et al, 2013), while our lesioned animals performed tasks well learned prior to surgery. Third, our MEC lesions also interfered with DG input to some extent, as these lesions often included layer II EC neurons that project directly to the granule cells (Witter and Amaral, 2004).…”

Section: Discussionmentioning

confidence: 77%

Relative contributions of CA3 and medial entorhinal cortex to memory in rats

O’Reilly

Alarcón

Ferbinteanu

2014

Front. Behav. Neurosci.

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The hippocampal CA1 field processes spatial information, but the relative importance of intra- vs. extra-hippocampal sources of input into CA1 for spatial behavior is unclear. To characterize the relative roles of these two sources of input, originating in the hippocampal field CA3 and in the medial entorhinal cortex (MEC), we studied effects of discrete neurotoxic lesions of CA3 or MEC on concurrent spatial and nonspatial navigation tasks, and on synaptic transmission in afferents to CA1. Lesions in CA3 or MEC regions that abolished CA3-CA1, or reduced MEC-CA1 synaptic transmission, respectively, impaired spatial navigation and unexpectedly interfered with cue response, suggesting that in certain conditions of training regimen, hippocampal activity may influence behavior otherwise supported by nonhippocampal neural networks. MEC lesions had milder and temporary behavioral effects, but also markedly amplified transmission in the CA3-CA1 pathway. Extensive behavioral training had a similar, but more modest effect on CA3-CA1 transmission. Thus, cortical input to the hippocampus modulates CA1 activity both directly and indirectly, through heterosynaptic interaction, to control information flow in the hippocampal loop. Following damage to hippocampal cortical input, the functional coupling of separate intra- and extra-hippocampal inputs to CA1 involved in normal learning may initiate processes that support recovery of behavioral function. Such a process may explain how CA3 lesions, which do not significantly modify the basic features of CA1 neural activity, nonetheless impair spatial recall, whereas lesions of EC input to CA1, which reduce the spatial selectivity of CA1 firing in foraging rats, have only mild effects on spatial navigation.

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Section: Discussionmentioning

confidence: 77%

Relative contributions of CA3 and medial entorhinal cortex to memory in rats

O’Reilly

Alarcón

Ferbinteanu

2014

Front. Behav. Neurosci.

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“…Past research has suggested there is a progressive reduction in hippocampal activation as a memory ages (Bontempi et al, 1999;Frankland and Bontempi, 2005;Maviel et al, 2004). The present thesis, along with other recent studies (Bonaccorsi et al, 2013;Lopez et al, 2012;Schlesiger et al, 2013;Wartman and Holahan, 2013), does not provide support for a reduction in hippocampal activation. In fact, results from this thesis showed greater hippocampal activation at remote, compared to recent, time points.…”

Section: Relevant Findings and Future Directionscontrasting

confidence: 97%

“…Stereological analyses revealed remotely tested groups had significantly higher numbers of c-Fos positive cells than recently tested groups. This finding contradicts some earlier reports that revealed lower hippocampal activation at remote time points (Frankland et al, 2004;Maviel et al, 2004) but is similar to other reported data (Bonaccorsi et al, 2013;Lopez et al, 2012;Schlesiger et al, 2013;Wartman and Holahan, 2013). As the WM task is a hippocampal-dependent task, it comes as no surprise the hippocampus was activated during the probe test (Broadbent et al, 2006;Clark et al, 2005a,b;D'Hooge and De Deyn, 2001;Holahan and Routtenberg, 2011;Morris et al, 1986Morris et al, , 1982Ramos, 2009;Remondes and Schuman, 2004;Sutherland et al, 2001Sutherland et al, , 1983Teixeira et al, 2006;Wiltgen et al, 2010).…”

Section: Discussionsupporting

confidence: 78%

“…Bonaccorsi et al (2013), Wartman and Holahan (2013), and Lopez et al (2012), used the water maze task as a behavioural measure and found increased activation of the hippocampus at remote compared to recent time points, consistent with the present set of results. Schlesiger et al (2013) used a modified radial arm maze task that incorporated different start locations and retention testing in a single trial in an effort to incorporate aspects of a standard water maze procedure. Frankland et al (2004) used contextual fear conditioning, while Maviel et al (2004) used a five-arm maze as their behavioural measure.…”

Section: Discussionmentioning

confidence: 99%

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A Synaptic and Systems Level Investigation of Memory Processes Using a Novel Multiple Memory Behavioural Procedure

Wartman¹

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It is proposed that memories stabilize through synaptic and systems level consolidation processes, forming long-lasting memory representations. Systems consolidation models suggest that hippocampal contribution to memory storage disengages as time progresses, while ensembles of cortical neurons are proposed to form increasingly strong connections that store and represent remote memories as consolidation proceeds. Investigations into memory representations highlight discrepancies between the involvement of a cortical region in remote memory processes, the anterior cingulate cortex (ACC), and the hippocampus. The present thesis introduces a novel behavioural procedure that examines the effect of increased processing demands on the hippocampus and the consequent effect on memory consolidation, storage and retrieval.Rats were trained on a single spatial task, two different spatial tasks, or one spatial and one non-spatial task. Regional involvement of the hippocampus and the ACC during retrieval were examined using immediate early genes and proteins of interest. Structural modifications in memory storage were examined using the Golgi-Cox method and quantification of dendritic complexity was analyzed through neuron reconstruction. The contribution of the ACC to spatial memory retrieval was assessed through behavioural performance and transient ACC pharmacological inactivation.The present thesis provides evidence that increased demand on the hippocampus results in accelerated processing of spatial memories. Findings show that the involvement of the ACC in memory processing can be manipulated by increasing hippocampal-processing demand. Functional, structural and behavioral data suggest that taxing the demand on the hippocampus accelerates the involvement of the ACC. There is also evidence of continued hippocampal involvement in memory processes at recent and remote time points. Taken together, these findings indicate an increased recruitment of the ACC, but not an accelerated independence from the hippocampus, in spatial memory processes. The use of a novel behavioral procedure aimed at increasing hippocampaldemand can reveal processes more similar to those present in the human condition, where there is a constant demand on memory systems. The novelty of the findings presented in this thesis will further our understanding of remote memory. i 0.2 Co-Authors Mathew R. Holahan Jennifer Gabel ii AcknowledgmentsThere are many people to credit with helping me reach this goal. I owe thanks to my colleagues, the staff and faculty at Carleton University and my supervisor, Dr. Matthew Holahan. I want to extend a special thanks to my friends and family for their encouragement and patience with me throughout this process and the reassuring words they provided me with countless times.iii 0.4 Dedication I dedicate this thesis to my soon-to-be husband, Dr. Zack Patterson. Over the last five years, Zack has had unwavering confidence in my abilities. He has celebrated my successes and supported me through tough times. I could not have ...

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“…In these regions, Mn causes neurodegenerative disorders, with symptoms that include memory impairment, cognitive slowing, and decreased learning capacity and mental flexibility (Levy and Nassetta, 2003;Josephs et al, 2005;Meyer-Baron et al, 2009). Multiple studies in rats have shown that the integrity of hippocampal CA1 field activity is necessary for the encoding and long-term storage of spatial information (Song et al, 2009), and the dentate gyrus (DG) seems to be primarily involved during the early stages of spatial memory formation (Schlesiger et al, 2013). Similarly, the effects of CA3 neurotoxic lesions or other experimentally induced dysfunctions of CA3 have been interpreted as impairing spatial memory (Poirier et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Chronic exposure to manganese sulfate leads to adverse dose‐dependent effects on the neurobehavioral ability of rats

Chen

Zou

et al. 2015

Environmental Toxicology

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Manganese sulfate is the main combustion product of methylcyclopentadienyl manganese tricarbonyl (MMT). Currently, little is known about the neurobehavioral consequences of chronic manganese sulfate exposure. In this study, rats were treated with 0, 5.0, 10.0, and 20.0 mg/kg MnSO ·H O for 24 consecutive weeks via intraperitoneal injection. During the treatment period, spatial learning-memory ability was measured using the Morris water maze (MWM). At the end of the exposure period, spontaneous motor behavior and emotional status, hippocampal histologic changes, and Hsp70 mRNA levels were measured using the open-field test (OFT), hematoxylin-eosin staining and real-time quantitative PCR (RT-PCR), respectively. A dose-dependent decrease was noted in the spatial learning-memory ability and the spontaneous activities of rats (P < 0.05), and negative emotions differed significantly between the exposed groups and the control group (P < 0.05). Moreover, overt morphological changes in the hippocampuses of the exposed rats were detected. Cellular degeneration and death were also found. The Hsp70 mRNA levels of the hippocampal areas in the 20.0 mg/kg group (1.567 ± 0.236) were significantly increased compared with the control group (P < 0.05). These results suggest that chronic exposure to manganese sulfate can have adverse dose-dependent effects on rats' neurobehavioral ability, and the mechanism of abnormal hippocampal Hsp70 expression needs to be further explored. © 2015 Wiley Periodicals, Inc. Environ Toxicol 31: 1571-1579, 2016.

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Hippocampal activation during the recall of remote spatial memories in radial maze tasks

Cited by 24 publications

References 44 publications

Relative contributions of CA3 and medial entorhinal cortex to memory in rats

Relative contributions of CA3 and medial entorhinal cortex to memory in rats

A Synaptic and Systems Level Investigation of Memory Processes Using a Novel Multiple Memory Behavioural Procedure

Chronic exposure to manganese sulfate leads to adverse dose‐dependent effects on the neurobehavioral ability of rats

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