Brain Aging: Impaired Coding of Novel Environmental Cues

Tanila, Heikki; Sipilä, Perttu; Shapiro, Matthew L.; Eichenbaum, Howard

doi:10.1523/jneurosci.17-13-05167.1997

Cited by 120 publications

(82 citation statements)

References 30 publications

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“…With similar inconsistency, spatial representations in aged rats rotate with rotated landmarks on some occasions but not others [81]. Furthermore, rigidity can be evident in the encoding properties of CA1 cells [78][79][80][81], but this is not as invariable in CA1 as it seems to be in CA3 [82]. As we now describe further, in our model these inconsistencies in CA1 might represent shifts between dependence on CA3 inputs and direct EC inputs to the CA1 subregion.…”

Section: Ca1mentioning

confidence: 68%

“…Of particular importance here, numerous studies have shown that CA3 and CA1 place cells of aged rats fail to encode new spatial or task information rapidly [78][79][80][81][82]. After young rats have explored one environment until it becomes highly familiar, introduction into a novel environment typically results in the creation of a new spatial representation, reflected in spatial firing patterns of hippocampal neurons that are drastically different from those associated with the familiar environment [83,84].…”

Section: Information Processing By Hippocampal Place Cells Of Aged Anmentioning

confidence: 99%

“…Reduced inputs might not transmit sufficient details to resolve changes in external contextual information that would normally be used to induce a switch from pattern completion to pattern separation. Based on this, the rigidity of encoding observed downstream in CA3 place cells [78][79][80][81][82] might be due, at least in part, to failure in the DG to reduce the similarity of input patterns sufficiently (e.g. pattern separation).…”

Section: Dentate Gyrusmentioning

confidence: 99%

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Neurocognitive aging: prior memories hinder new hippocampal encoding

Wilson

Gallagher

Eichenbaum

et al. 2006

Trends in Neurosciences

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327

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Normal aging is often accompanied by impairments in forming new memories, and studies of aging rodents have revealed structural and functional changes to the hippocampus that might point to the mechanisms behind such memory loss. In this article, we synthesize recent neurobiological and neurophysiological findings into a model of the information-processing circuit of the aging hippocampus. The key point of the model is that small concurrent changes during aging strengthen the auto-associative network of the CA3 subregion at the cost of processing new information coming in from the entorhinal cortex. As a result of such reorganization in aged memory-impaired individuals, information that is already stored would become the dominant pattern of the hippocampus to the detriment of the ability to encode new information.

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Section: Ca1mentioning

confidence: 68%

Section: Information Processing By Hippocampal Place Cells Of Aged Anmentioning

confidence: 99%

Section: Dentate Gyrusmentioning

confidence: 99%

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Neurocognitive aging: prior memories hinder new hippocampal encoding

Wilson

Gallagher

Eichenbaum

et al. 2006

Trends in Neurosciences

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304

327

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“…The present finding of increased spatial selectivity standard conditions toward the end of the experiment in both young and aged rats suggests that this aspect of spatial processing is intact in aging. However, as demonstrated in our accompanying paper (Tanila et al, 1997), this focussing of place fields may take more time in aged memory-impaired rats than in memory-intact ones. Moreover, the present observation that place cells of memory-impaired aged rats began firing significantly earlier in the testing episode suggests that less processing of the relationships among the environmental cues may be done before the place cell fires in memory-impaired aged animals.…”

Section: Discussionmentioning

confidence: 87%

Brain Aging: Changes in the Nature of Information Coding by the Hippocampus

et al. 1997

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Advanced age in rats is associated with a decline in spatial memory capacities dependent on hippocampal processing. As yet, however, little is known about the nature of age-related alterations in the information encoded by the hippocampus. Young rats and aged rats identified as intact or impaired in spatial learning capacity were trained on a radial arm maze task, and then multiple parameters of the environmental cues were manipulated to characterize the changes in firing patterns of hippocampal neurons corresponding to the presence of particular cues or the spatial relationships among them. The scope of information encoded by the hippocampus was reduced in memory-impaired aged subjects, even though the number of neurons responsive to salient environmental cues was not different from that in young rats. Furthermore, after repeated manipulations of the cues, memory-intact aged rats, like young rats, altered their spatial representations, whereas memory-impaired aged rats showed reduced plasticity of their representation throughout testing. Thus changes in hippocampal memory representation associated with aging and memory loss can be characterized as a rigid encoding of only part of the available information. Key words: spatial learning; spatial memory; place field; electrophysiology; encoding; representation; rat; ageDiminished memory capacity is a well known concomitant of aging in humans (Craik, 1990;Rapp and Heindel, 1994) and animals (Barnes, , 1988DeToledo-Morrell et al., 1988;Gage et al., 1988;Rapp and Amaral, 1992;Rapp and Heindel, 1994;Gallagher et al., 1995). Across all species studies have found that the memory deficit associated with aging is characterized by large variability in cognitive capacities so that some aged subjects perform as well young subjects, whereas others show severe impairment (Markowska et al., 1989;Bachevalier et al., 1991;Rapp and Amaral, 1992;Gallagher et al., 1993). Many experiments have identified anatomical, molecular, and physiological markers of memory impairment in the hippocampal region of aged animals and humans (Barnes, 1979(Barnes, , 1988DeToledo-Morrell et al., 1988;Gage et al., 1988;Rapp and Amaral, 1992; Gallagher et al., 1994;Rapp and Heindel, 1994;Grady et al., 1995;Rapp and Gallagher, 1996), but few studies to date have characterized age-associated changes in the nature of information encoded by neurons in the brain.In rats aging results in an impairment in spatial learning and memory. Spatial learning in rats is strongly dependent on hippocampal function (Morris et al., 1982), and the firing patterns of hippocampal pyramidal cells correlate with the spatial location of an animal in the testing environment during exploratory behavior (O' Keefe and Nadel, 1978). The firing pattern of such hippocampal "place cells" is controlled by spatial and other relationships among multiple environmental cues and ongoing behavior and may reflect higher-order memory processing (O'Keefe and Nadel, 1978;Muller and Kubie, 1987;Eichenbaum, 1996).The activity of place cells in rats ex...

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“…In addition, hippocampal cells show place field changes with changes in environments or the available constellation of cues [17,90,93,129,148,181,219,223,250]. Animals with learning deficits (whether by aging, NMDA-blockade, or cortical lesions) also show an instability of place fields across sessions, though not within the session itself [8,11,87,127,189,190,220,221].…”

Section: Non-spatial Place Cellsmentioning

confidence: 99%

The hippocampal debate: are we asking the right questions?

Redish

2001

Behavioural Brain Research

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For years, the debate has been: 'Is the hippocampus the cognitive map?' or 'Is the hippocampus the core of memory?' These two hypotheses derived their original power from two key experiments-the cognitive map theory from the remarkable spatial correlates seen in recordings of hippocampal pyramidal cells and the memory theory from the profound amnesias seen in the patient H.M. Both of these key experiments have been reinterpreted over the years: hippocampal cells are correlated with much more than place and H.M. is missing much more than just his hippocampus. However, both theories are still debated today. The hippocampus clearly plays a role in both navigation and memory processing. The question that must be addressed is rather: 'What is the role played by the hippocampus in the navigation and memory systems?' By looking at the navigation system as a whole, one can identify the major role played by the hippocampus as correcting for accumulation errors that occur within idiothetic navigation systems. This is most clearly experimentally evident as reorientation when an animal is lost. Carrying this over to a more general process, this becomes a role of recalling a context, bridging a contextual gap, or, in other words, it becomes a form of recognition memory. I will review recent experimental data which seems to support this theory over the more general spatial or memory theories traditionally applied to hippocampus.

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Brain Aging: Impaired Coding of Novel Environmental Cues

Cited by 120 publications

References 30 publications

Neurocognitive aging: prior memories hinder new hippocampal encoding

Neurocognitive aging: prior memories hinder new hippocampal encoding

Brain Aging: Changes in the Nature of Information Coding by the Hippocampus

The hippocampal debate: are we asking the right questions?

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