Parallel processing across neural systems: Implications for a multiple memory system hypothesis

Mizumori, Sheri J. Y.; Yeshenko, Oksana; Gill, Kathryn; Davis, Dale

doi:10.1016/j.nlm.2004.07.007

Cited by 108 publications

(99 citation statements)

References 84 publications

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“…in terms of signal reliability, signal specificity, and temporally correlated firing) and quantitatively (e.g. increasing or decreasing magnitude of correlated discharge) depending upon task demands (Mizumori, Yeshenko, Gill, & Davis, 2004). There was no relationship between the type of response and spike width, suggesting that particular kinds of responses were not selective to particular kinds of neuron.…”

Section: Hpc Neural Responsesmentioning

confidence: 88%

Memory influences on hippocampal and striatal neural codes: Effects of a shift between task rules

Eschenko

Mizumori

2007

Neurobiology of Learning and Memory

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Interactions with neocortical memory systems may facilitate flexible information processing by hippocampus. We sought direct evidence for such memory influences by recording hippocampal neural responses to a change in cognitive strategy. Well trained rats switched (within a single recording session) between the use of place and response strategies to solve a plus maze task. Maze and extramaze environments were constant throughout testing. Place fields demonstrated (in-field) firing rate and location based reorganization (Leutgeb, Leutgeb, Barnes, Moser, McNaughton, & Moser, 2005) after a task switch, suggesting that hippocampus encoded each phase of testing as a different context, or episode. The task switch also resulted in qualitative and quantitative changes to discharge that were correlated with an animal's velocity or acceleration of movement. Thus, the effects of a strategy switch extended beyond the spatial domain, and the movement correlates were not passive reflections of the current behavioral state. To determine whether hippocampal neural responses were unique, striatal place and movement-correlated neurons were simultaneously recorded with hippocampal neurons. Striatal place and movement cells exhibited a response profile that was similar, but not identical, to that observed for hippocampus after a strategy switch. Thus, retrieval of a different memory led both neural systems to represent a different context. However, hippocampus may play a special (though not exclusive) role in flexible spatial processing since correlated firing amongst cell pairs was highest when rats successfully switched between two spatial tasks. Correlated firing by striatal cell pairs increased following any strategy switch, supporting the view that striatum codes changes in reinforcement contingencies.

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Section: Hpc Neural Responsesmentioning

confidence: 88%

Memory influences on hippocampal and striatal neural codes: Effects of a shift between task rules

Eschenko

Mizumori

2007

Neurobiology of Learning and Memory

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“…In the present study, subjects were placed in the same corner of the holeboard for every trial and thus, response/procedural learning might also yield successful results. Brain systems consisting of different structures are involved in processes for similar types of learning and memory ("parallel processing") (Lee and Kesner, 2003;McIntyre et al, 2003;Mizumori et al, 2004). Which neural system has more relative influence on behavioral expression may vary depending upon a number of factors such as age, experience, or incentive.…”

Section: Discussionmentioning

confidence: 99%

Animal model of posterior cingulate cortex hypometabolism implicated in amnestic MCI and AD

Riha

Rojas

Colorado³

et al. 2008

Neurobiology of Learning and Memory

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The posterior cingulate cortex (PCC) is the brain region displaying the earliest sign of energy hypometabolism in patients with amnestic mild cognitive impairment (MCI) who develop Alzheimer's disease (AD). In particular, the activity of the mitochondrial respiratory enzyme cytochrome oxidase (C.O.) is selectively inhibited within the PCC in AD. The present study is the first experimental analysis designed to model in animals the localized cortical C.O. inhibition found as the earliest metabolic sign of early-stage AD in human neuroimaging studies. Rats were used to model local inhibition of C.O. by direct injection of the C.O. inhibitor sodium azide into the PCC. Learning and memory were examined in a spatial holeboard task and brains were analyzed using quantitative histochemical, morphological and biochemical techniques. Behavioral results showed that sodium azide-treated rats were impaired in their memory of the baited pattern in probe trials as compared to their training scores before treatment, without non-specific behavioral differences. Brain analyses showed that C.O. inhibition was specific to the PCC, and sodium azide increased lipid peroxidation, gliosis and neuron loss, and lead to a network functional disconnection between the PCC and interconnected hippocampal regions. It was concluded that impaired memory by local C.O. inhibition in the PCC may serve to model in animals a metabolic lesion similar to that found in patients with amnestic MCI and early-stage AD. This model may be useful as an in vivo testing platform to investigate neuroprotective strategies to prevent or reduce the amnestic effects produced by posterior cingulate energy hypometabolism.

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“…One group of mice was pre-exposed to the same context as training and testing (PTC) and the other group was pre-exposed to a different context (PDC). Our results show that the PTC condition biased mice to place strategy use in males, but this bias was dependent on the presence of ovarian hormones in females.The participation of different brain areas in place and response learning strategies has been studied extensively (White and McDonald 2002;Gold 2004;Mizumori et al 2004). Place strategy is an allocentric navigation strategy that depends on extramaze cues.…”

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“…The participation of different brain areas in place and response learning strategies has been studied extensively (White and McDonald 2002;Gold 2004;Mizumori et al 2004). Place strategy is an allocentric navigation strategy that depends on extramaze cues.…”

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confidence: 99%

Pre-exposure to context affects learning strategy selection in mice

Tunur

Dohanich²,

Schrader³

2010

Learn. Mem.

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The multiple memory systems hypothesis proposes that different types of learning strategies are mediated by distinct neural systems in the brain. Male and female mice were tested on a water plus-maze task that could be solved by either a place or response strategy. One group of mice was pre-exposed to the same context as training and testing (PTC) and the other group was pre-exposed to a different context (PDC). Our results show that the PTC condition biased mice to place strategy use in males, but this bias was dependent on the presence of ovarian hormones in females.The participation of different brain areas in place and response learning strategies has been studied extensively (White and McDonald 2002;Gold 2004;Mizumori et al. 2004). Place strategy is an allocentric navigation strategy that depends on extramaze cues. Response strategy is an egocentric navigation strategy based on proprioceptive cues. Inactivation of the hippocampus biased animals to response strategy use, and inactivation of the striatum biased animals to place strategy use (Packard and McGaugh 1996;Lee et al. 2008). Furthermore, glutamate infusion into the hippocampus strengthened place strategy use and, conversely, glutamate infusion into the striatum enhanced response strategy use (Packard 1999). These studies suggest that the hippocampus system mediates place strategy, while the striatum system mediates response strategy.Various factors can modulate learning strategy use, including training intensity (Packard and McGaugh 1996;Martel et al. 2007). A recent study investigated the influence of training on strategy use on a probe trial conducted 1 h after training (Martel et al. 2007). Male mice displayed enhanced place strategy use when trained on 12 or 22 trials compared with four trials, suggesting an effect of training intensity on strategy choice (Martel et al. 2007). This study further investigated the effect of pre-exposure to the training and testing context (PTC). Pre-exposure enhanced place strategy use in male mice after only four trials relative to animals pre-exposed to a different context (PDC). These results suggest that a sufficient exposure to the training and testing context promotes place strategy use in mice.The type of strategy used by rats is affected by both biological sex and gonadal steroids. Male rats typically employ a place strategy, especially during the early phase of training, on both land and water T-mazes (Packard and McGaugh 1992, 1996;Packard and Teather 1997). However, strategy use by female rats depends on hormonal conditions (Dohanich 2002;Dohanich et al. 2009). Place strategy is preferred by intact female rats on the day of proestrus when estradiol levels are elevated, and by ovariectomized rats treated with estradiol (Korol and Kolo 2002;Korol 2004;Korol et al. 2004). In contrast, response strategy is more often displayed by intact females on diestrus, and by ovariectomized females that did not receive estradiol replacement (Korol and Kolo 2002;Korol et al. 2004). To date, the effects of biological sex ...

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Parallel processing across neural systems: Implications for a multiple memory system hypothesis

Cited by 108 publications

References 84 publications

Memory influences on hippocampal and striatal neural codes: Effects of a shift between task rules

Memory influences on hippocampal and striatal neural codes: Effects of a shift between task rules

Animal model of posterior cingulate cortex hypometabolism implicated in amnestic MCI and AD

Pre-exposure to context affects learning strategy selection in mice

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