Effects of hippocampal cholinergic deafferentation on learning strategy selection in a visible platform version of the water maze

Bizon, Jennifer L.; Han, Jung‐Soo; Hudon, Carol; Gallagher, Michela

doi:10.1002/hipo.10113

Cited by 34 publications

(30 citation statements)

References 58 publications

(76 reference statements)

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“…In contrast, all of the 23-mo-old mice swam to the visible platform without visiting the original platform location. Not surprisingly, as in adult rats, most mice in the current study adapted to the new visible platform location by the second strategy probe trial (Devan and White 1999;Bizon et al 2003).…”

Section: Discussionmentioning

confidence: 58%

Emergence of a Cue Strategy Preference on the Water Maze Task in Aged C57B6 × SJL F1 Hybrid Mice

Nicolle¹,

Prescott²,

Bizon³

2003

Learn. Mem.

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The effects of age on cue learning, spatial reference memory, and strategy preference were assessed in B6 × SJL F1 mice by using the Morris water maze. This mouse strain is of particular interest because it is the background strain for a common transgenic model of Alzheimer's disease, the Tg2576 mouse, which develops plaques and other neurobiological markers of pathology beginning at 8 mo and increasing in severity with advanced age. In the current study, 12-and 23-mo-old C57B6 × SJL F1 mice were serially trained in cue and place versions of the Morris water maze task. At the completion of training, mice received a strategy probe test in which place (hidden) and cue (visible) strategies were in competition. Cue and spatial learning ability was maintained between 12 and 23 mo of age; however, on the strategy preference probe test, the 23-mo-old mice exhibited a significant bias toward the selection of a cue strategy. There was no relationship between strategy preference in the probe test and spatial learning ability, but the 23-mo-old mice did exhibit a strong trend toward shorter latencies during visible platform training, possibly reflecting the enhanced function of striatal-based neural systems in aging. These data demonstrate that 23-mo-old C57B6 × SJL F1 mice are capable of effective place learning, but if a place strategy is pitted against the use of a cue strategy, the use of a cue strategy predominates in the aged mice. The strategy preference observed here may reflect an emergence of differential processing in underlying brain circuitry with age in the B6 × SJL F1 mouse strain.Substantial literature regarding the disparate behavioral phenotypes of background mouse strains used for targeted gene mutations highlights the need for careful behavioral characterization in the host strain prior to interpreting the effects of mutations (Crawley et al. 1997;Wahlsten et al. 2003). In addition, when the expression of the gene mutation is age-dependent, understanding the effects of age on the behavior of interest in that particular strain is crucial; the neurobiology of aging can vary across strains, as different strains have different life spans and susceptibility to diseases of aging (Wahlsten et al. 2003). The present study was designed to assess the effects of normal aging on cue learning, spatial learning, and strategy preference in the mouse hybrid strain C57B6 ‫ן‬ SJL F1. This strain has been used as the background strain for a common transgenic model of Alzheimer's disease, the Tg2576 mouse (see Hsiao et al. 1996;Westerman et al. 2002). Because the mutant mouse begins to show pathology at 8 mo of age that becomes more pronounced over time (Kawarabayashi et al. 2001;Westerman et al. 2002), the current study focused on spatial behaviors in the background strain at middle (12 mo) and advanced (23 mo) ages.In addition to traditional water maze measures (i.e., cue learning and spatial reference learning), strategy preference was assessed in the current study by evaluating strategy choice (cue or spatial) after se...

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Section: Discussionmentioning

confidence: 58%

Emergence of a Cue Strategy Preference on the Water Maze Task in Aged C57B6 × SJL F1 Hybrid Mice

Nicolle¹,

Prescott²,

Bizon³

2003

Learn. Mem.

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Section: -Igg Saporin Lesionsmentioning

confidence: 95%

“…However, this study was carried out 48 hours post surgery at a time when the cholinergic lesion is not complete. More recent studies have found an increased preference for a spatial strategy in rats with MS/VDB lesions (Bizon et al, 2003;Jonasson et al, 2004).The effects of IgG SAP lesions on non-spatial memory tasks have not been as extensively studied, but a few studies have reported no effect on freezing behaviour during fear conditioning to tone or to context following a selective MS/VDB lesion or a complete CBF lesion (Frick et al, 2004). Attentional processes are also affected following a NB lesion as tested on the 5-choice serial reaction task (Lehmann et al, 2003;Harati et al, 2008).…”

mentioning

confidence: 97%

Revisiting the cholinergic hypothesis in the development of Alzheimer's disease

Craig

Hong

McDonald

2011

Neuroscience & Biobehavioral Reviews

399

263

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Alzheimer's disease (AD) is the most common form of dementia affecting the elderly population today; however, there is currently no accurate description of the etiology of this devastating disorder. No single factor theory has been demonstrated as being causative; however, an alternative theory suggests that the interaction of multiple risk factors is responsible for AD. In this thesis I present data suggesting a neuroprotective role for acetylcholine during aging. Using a rat model of cholinergic depletion of the medial septum, I explored the effects of four common risk factors for AD (stress, seizures, stroke and circadian dysfunction) targeted at the hippocampus and examined the effects on measures of hippocampal dependent (water maze) and hippocampal independent (fear conditioning) memory. Here, I propose a role for acetylcholinemediated compensatory mechanisms in the functional recovery observed following sub threshold insults similar to those commonly observed in the elderly. m First and foremost I would like to thank my supervisor, Dr. Robert McDonald. Thank you for your support and encouragement, and for allowing me the independence to pursue my own projects and to learn from my experiences. I would also like to thank Nhung Hong for doing the majority of the cholinergic depletion and stroke surgeries used in this thesis and for teaching me the techniques. I would like to give a huge thank you to Joelle Kopp who was an invaluable asset who assisted in histology and spent many hours on the microscope counting cholinergic neurons. I would also like to thank Dr. Christine Werk for patiently reading and re-reading early drafts of my papers and this thesis and Dr.Hugo Lehmann for all his help in running statistics and interpreting my data. In addition, many thanks go out to Courtney Lamb, Robert Court and Arthur Verhoef for helping me with histology and behavioural testing, to Keri Colwell for running the corticosterone assays, the Metz lab for kindly allowing me the use of their microscope and to Karen Dow-Cazel and the rest of the animal care staff for taking care of my rats and helping me set up the circadian experiements. The cholinergic hypothesis of Alzheimer's disease 6 Acknowledgements IVThe basal forebrain cholinergic system 8The role of the basal forebrain cholinergic system in learning and memory 10The current state of the cholinergic hypothesis of Alzhimer's disease 15Risk factors for Alzheimer's disease 16Multiple combinations of co-factors theory of Alzheimer's disease 22The role of the hippocampus in learning and memory 24Objective of the present thesis 25Chapter 2: A series of pilot studies to determine the threshold for behaviourally sub threshold stroke, seizures and stress 28Abstract 29Experiment la: The effect of a chronic variable stress schedule on performance of the water maze task 32 Materials and Methods 33Results 36Experiment lb: The effects of a variable restraint stress procedure on levels of blood borne CORT 39 Materials and Methods 39Results 40Discussion 41Experiment 2: T...

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“…Colombo and Gallagher (1998) reported that increases in acetylcholynetransferase activity in the dorsolateral striatum are negatively correlated with the accuracy in hippocampaldependent working memory tasks. Furthermore, alterations in the cholinergic septohippocampal system leading to enhanced or impaired cholinergic function in the hippocampus seem, respectively, to enhance or reduce learning and memory in this structure (Ragozzino and Gold 1995, Janis et al 1998, Gold 2003 (but see Cahill and Baxter 2001, Bizon et al 2003). Simultaneous measurement of acetylcholine in the hippocampus and the striatum showed a correlation between the changes of ACh release and the expression of place response or S-R behaviour Gold 2003b, McIntyre et al 2003).…”

Section: Studying Interactions Between Systemsmentioning

confidence: 98%

“…Additionally, the interactions between the different systems have been studied by testing the facilitating effect of lesioning a system that is not related to the task to be solved (Packard et al 1989, Schroeder et al 2002, Chang and Gold 2003a. Another interesting line of research studies the correlation of neurochemical factors with the expression of different kinds of response (Ragozzino and Gold 1995, Colombo and Gallagher 1998, Janis et al 1998, Bizon et al 2003, Chang and Gold 2003b, McIntyre et al 2003, Marriott and Korol 2003. Devan and White (1999) applied an experimental procedure in which cue and place responses were developed simultaneously in the water maze (figure 1).…”

Section: Experimental Approaches Dissociating Parallel Navigation Sysmentioning

confidence: 99%

Competition between cue response and place response: a model of rat navigation behaviour

et al. 2005

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Different neural systems are involved in animal navigation depending on the type of task. Experimental studies support the idea that the hippocampus is necessary to learn a spatial representation required to navigate toward hidden goals (place response), whereas the dorsolateral striatum is involved in the learning of stimulus-response associations when navigating toward visible (or cued) goals. These systems compete for action selection according to the characteristics of the task, previous experience (e.g. training procedure) or endogenous factors. This paper reviews both experimental data on the theory of multiple memory systems involved in navigation, and a recent computational model of action selection based on the competition of place and cue responses learnt during training. The model implements separately the two types of response, i.e. place response and stimulus response. Furthermore, competition takes place to select which behaviour will actually be performed. The model was tested in a simulated environment using a protocol analogous to those used in experiments with animals.

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Effects of hippocampal cholinergic deafferentation on learning strategy selection in a visible platform version of the water maze

Cited by 34 publications

References 58 publications

Emergence of a Cue Strategy Preference on the Water Maze Task in Aged C57B6 × SJL F1 Hybrid Mice

Emergence of a Cue Strategy Preference on the Water Maze Task in Aged C57B6 × SJL F1 Hybrid Mice

Revisiting the cholinergic hypothesis in the development of Alzheimer's disease

Competition between cue response and place response: a model of rat navigation behaviour

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