The challenges of understanding mammalian cognition and memory-based behaviours: an interactive learning and memory systems approach

McDonald, Robert J.; Hong, Nancy S.; Devan, Bryan D.

doi:10.1016/j.neubiorev.2004.09.014

Cited by 68 publications

(46 citation statements)

References 159 publications

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“…However, when they were tested after more extensive training, their performance indicated that they were using the response strategy. These results suggest that the hippocampal output tends to dominate the cortico-striatal output early in training, but the hippocampal system goes offline with extensive training and relinquishes control to the cortico-striatal system.In conclusion, our results are consistent with the general idea of complementary learning systems in the brain (White and McDonald 2002;Atallah et al 2004;McDonald et al 2004), which assumes that the cortico-striatal system and the medial temporal hippocampal system operate in parallel. The information contained in the two systems can either synergize or be incompatible.…”

supporting

confidence: 91%

“…In conclusion, our results are consistent with the general idea of complementary learning systems in the brain (White and McDonald 2002;Atallah et al 2004;McDonald et al 2004), which assumes that the cortico-striatal system and the medial temporal hippocampal system operate in parallel. The information contained in the two systems can either synergize or be incompatible.…”

supporting

confidence: 91%

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The role of the dorsal striatum and dorsal hippocampus in probabilistic and deterministic odor discrimination tasks

Atallah¹,

Rudy²,

O’Reilly³

2008

Learn. Mem.

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Three experiments explored the contribution of the cortico-striatal system and the hippocampus system to the acquisition of solutions to simultaneous instrumental odor discriminations. Inactivation of the dorsal striatum after rats had reached criterion on a three problem probabilistic set of discriminations-A (80%) vs. B (20%), C (67%) vs. D (33%), E(67%) vs. F(33%)-impaired test performance and disrupted performance when the rats were tested with novel cue combinations (C vs. F and E vs. D), where control animals chose C and F. In contrast, inactivating the dorsal hippocampus enhanced performance on this task and on a deterministic discrimination A (100%) vs. B (0%). These results are consistent with the complementary learning systems view, which assumes that the cortico-striatal and hippocampal system capture information in parallel. How this information combines to influence task performance depends on the compatibility of the content captured by each system. These results suggest that the trial-specific information captured by the hippocampal system can be incompatible with the across-trial integration of trial outcomes captured by the cortico-striatal system.There are both experimental and theoretical reasons to believe that the memory system supported by cortico-striatal areas and the system supported by the hippocampal formation have very different properties (Hirsh 1974;Oberg and Divac 1975;Mishkin and Petrie 1984;White and McDonald 2002). The cortico-striatal system is believed to support instrumental behaviors that are modified by the outcomes or rewards that they produce. This system integrates the outcomes of multiple response-reward experiences. In contrast, the hippocampal formation is part of the episodic memory system that is designed to capture representations of individual experiences and keep them separate (see Teyler and DiScenna 1986;Tulving and Markowitsch 1998;O'Reilly and Rudy 2001;Teyler and Rudy 2007). Thus, these two systems have complementary functions (Atallah et al. 2004).Given that these systems are normally both online, their complementary functions (Mishkin and Petrie 1984;Sherry and Schacter 1987;McClelland et al. 1995;White and McDonald 2002) might sometimes be incompatible with the demands of a particular learning task. For example, McDonald and White (1993) have shown that lesions of the hippocampal formation can improve performance on a task that is dependent on the cortico-striatal system.We report three experiments that further explore the interaction between the cortico-striatal system and hippocampal system. To do this, we used a probabilistic multiple odor discrimination task. The subjects were required to simultaneously solve three odor discrimination problems: A (80%) vs. B (20%), C (67%) vs. D (33%), and E (67%) vs. F (33%), where the probability that the choice response would be rewarded is in parenthesis. Note that any given choice can result in a rewarded or nonrewarded outcome. Thus, the outcome of any one trial does not perfectly specify the outcome a response ...

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supporting

confidence: 91%

supporting

confidence: 91%

The role of the dorsal striatum and dorsal hippocampus in probabilistic and deterministic odor discrimination tasks

Atallah¹,

Rudy²,

O’Reilly³

2008

Learn. Mem.

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“…extensive floating) or active coping strategies (escape behavior along the walls; Lipp & Wolfer 1998;Wotjak 2004). Several modifications of the water maze task have been designed to circumvent some of these caveats and therefore to supposedly serve as better measures of hippocampusdependent learning, as exemplified by one trial place learning (successfully applied in rats; McDonald et al 2004) or discriminatory place learning (successfully used in mice; Arns et al 1999). In the latter task, the water tank contains two identical floating platforms which are visible to the animals.…”

Section: Cognitive Behaviormentioning

confidence: 99%

A hitchhiker's guide to behavioral analysis in laboratory rodents

Sousa

Almeida²,

Wotjak

2006

Genes Brain and Behavior

243

171

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Genes and environment are both essential and interdependent determinants of behavioral responses. Behavioral genetics focuses on the role of genes on behavior. In this article, we aim to provide a succinct, but comprehensive, overview of the different means through which behavioral analysis may be performed in rodents. We give general recommendations for planning and performing behavioral experiments in rats and mice, followed by brief descriptions of experimental paradigms most commonly used for the analysis of reflexes, sensory function, motor function and exploratory, social, emotional and cognitive behavior. We end with a discussion of some of the shortcomings of current concepts of genetic determinism and argue that the genetic basis of behavior should be analyzed in the context of environmental factors.

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“…This recovered function has been ascribed to overcoming sensorimotor deficits produced by NMDAr blockade (Keith and Rudy 1990;Cain et al 1996Cain et al , 1997Saucier et al 1996). The possibility also exists that pretraining protocols might enhance the processing capacities of intrahippocampal networks necessary for the cognitive aspects of the task (Otnaess et al 1999;Uekita et al 2006;Uekita and Okaichi 2009) or extra-hippocampal networks that also contribute to spatial information processing White 1994, 1995;Devan and White 1999;McDonald et al 2004;Holahan et al 2005;Knierim 2006). In this way, pretraining would affect a mnemonic function rather than sensorimotor processes.…”

mentioning

confidence: 99%

Effect of juvenile pretraining on adolescent structural hippocampal attributes as a substrate for enhanced spatial performance

Keeley¹,

Wartman²,

Häusler³

et al. 2010

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Research has demonstrated that Long -Evans rats (LER) display superior mnemonic function over Wistar rats (WR). These differences are correlated with endogenous and input-dependent properties of the hippocampus. The present work sought to determine if juvenile pretraining might enhance hippocampal structural markers and if this would be associated with spatial processing improvements. Male and female WR and LER were either handled or trained on a water maze task from postnatal day 16 (p16) to p26 (pretraining). All animals were then trained on the task from p40 to p44 followed by immunohistochemical assessment of synaptophysin (to mark presynaptic terminals), MAP-2 (to mark dendrites), and the phosphorylated (activated) form of the extracellular signal-regulated kinase-1 (pERK1) in the hippocampus. From p19 to p20, LER (both male and female) showed a dramatic improvement in locating the hidden platform compared to their WR counterparts. On the first day of training at p40, all pretrained groups showed shorter latencies to locate the platform compared to groups without pretraining. Over the next 4 d, only pretrained male LER showed enhanced memory. Immunohistochemical analysis revealed fewer pERK1-labeled neurons in the CA3 hippocampal region in all pretrained groups and fewer pERK1-labeled neurons in the CA1 region of pretrained male LER. Pretrained male LER also showed more MAP-2 staining in CA1 and dentate gyrus regions. Synaptophysin staining revealed a pattern of axonal redistribution in the CA3 region in the pretrained groups. Results suggest a pattern of structural hippocampal alterations that may help to identify network malleability following pretraining protocols.

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The challenges of understanding mammalian cognition and memory-based behaviours: an interactive learning and memory systems approach

Cited by 68 publications

References 159 publications

The role of the dorsal striatum and dorsal hippocampus in probabilistic and deterministic odor discrimination tasks

The role of the dorsal striatum and dorsal hippocampus in probabilistic and deterministic odor discrimination tasks

A hitchhiker's guide to behavioral analysis in laboratory rodents

Effect of juvenile pretraining on adolescent structural hippocampal attributes as a substrate for enhanced spatial performance

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