Age and Experience-Dependent Representational Reorganization During Spatial Learning

Abstract

Age and experience-dependent representational reorganization during spatial learning NEUROBIOL AGING 18(6) 651-659, 1997.-Previously, we found that aged rats showed a significant enhancement of hippocampal CA1 place cell spatial specificity, as well as a reduction of hilar place cell spatial specificity, during asymptote performance of a spatial memory task. Because such an age effect was not observed when animals performed a nonspatial task, the present study tested the hypothesis that the different patterns of spatial selectivity observed in memory and nonmemory tests reflected a redistribution of spatial representations that occurred in response to changing task demands. In the present experiment, after animals became familiar with the test environment and motor demands of performance on a radial maze, CA1 and hilar place cells were recorded as they learned a spatial memory task. CA1 place cells recorded from unimpaired old, but not impaired old or young, animals became more spatially selective as animals learned the task. Hilar spatial selectivity for both age groups was not significantly related to choice accuracy. These data support the hypothesis that at least a subpopulation of aged rats may benefit from reorganization of spatial representations in such a way that the normal age-related spatial learning deficit is attenuated. © 1997 Elsevier Science Inc. Place cellsHippocampus Spatial learning Representational neuroplasticity Aging THE relatively poor performance of aged rats on spatial memory tasks has been shown not to be due to general sensory or motor decline (e.g., 3,6,12,29,33). Rather, arguments have been made for a select difficulty in acquiring new information, especially spatial information. Recent studies have shown that aged rats and monkeys do not show significant loss of cells in any of the hippocampal subregions examined (i.e., the granule cell layer, hilus, CA3, CA1, or subiculum; refs. 28,30,31). Therefore, it is likely that a hippocampal contribution to the spatial learning decline with senescence reflects more subtle changes in hippocampal cell function. Indeed, there is evidence that the synaptic structure of hippocampal neurons undergoes age-associated changes that are correlated with the memory impairment (e.g., ref. 9). The functional significance of such synaptic changes is presently unknown. However, it is not unreasonable to postulate that such intracellular alterations might change the manner in which information is coded by aged hippocampal neurons. A large proportion of hippocampal neurons (place cells) are known to selectively discharge as animals traverse circumscribed portions of environmental space, referred to as place fields (24,25). Hill and Best (11) showed that place fields emerge relatively quickly when placed in a new environment. This initial result was recently extended by Wilson and McNaughton (32) and Austin and colleagues (1), who showed that place coding by particular hippocampal neurons can undergo initially rapid, then more subtle long-term changes with co...

Age-Associated Alterations of Hippocampal Place Cells Are Subregion Specific

“…Past analyses of hippocampal information processing in aged animals have focused either exclusively on cells of the CA1 subregion Shen et al, 1997;McEchron et al, 2001; or have combined the data obtained from the CA1 and CA3 subregions for analytical purposes Oler and Markus, 2000;Wilson et al, 2003Wilson et al, , 2004Wilson et al, , 2005. In studies of aging that did analyze subregions separately (Mizumori et al, 1996;Mizumori and Kalyani, 1997), the experimental conditions for recordings were not suitable for detecting the distinctive features of CA1 and CA3 encoding in response to changes in the environment. In making this hippocampal subregion comparison, we found that the CA1 cells of aged rats had firing properties similar to those of the young adults: both groups had overall firing rates at similar values and made some adjustments in firing rates in response to a change in the environment.…”

Individual differences in neurocognitive aging of the medial temporal lobe

“…Similarly, despite a diminished entorhinal input, CA1 and CA3 "place fields" of aged rats with behavioral impairments are not degraded with respect to field size, coherence, and other parameters that characterize spatial information content (Rosenzweig et al 2003;Wilson et al 2003). Instead, alterations in encoding are revealed in the experience-dependent plasticity of those cells, effects that are manifest in distinct settings across different hippocampal subregions Mizumori and Kalyani 1997;Shen et al 1997;Wilson et al 2005).…”

Hippocampal and neocortical interactions during context discrimination: Electrophysiological evidence from the rat

“…Indeed it has been shown that such measures of place fields vary with experience (e.g. Mizumori and Kalyani, 1997;Puryear et al, 2006). Also, the degree of temporal coherence amongst a group of neurons could depend on their recent activation patterns (e.g.…”