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The Journal of Neuroscience, April 14, 2004, 24(15):3870-3878; doi:10.1523/JNEUROSCI.5205-03.2004

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Behavioral/Systems/Cognitive
Cognitive Aging and the Hippocampus: How Old Rats Represent New Environments

Iain A. Wilson,¹ Sami Ikonen,¹ Irina Gureviciene,¹ Robert W. McMahan,² Michela Gallagher,² Howard Eichenbaum,³ and Heikki Tanila^1,4

¹Department of Neuroscience and Neurology, University of Kuopio, Kuopio 70211, Finland, ²Department of Psychology, Johns Hopkins University, Baltimore, Maryland 21218, ³Department of Psychology, Boston University, Boston, Massachusetts 02215, and ⁴Department of Neurology, Kuopio University Hospital, Kuopio 70211 Finland

Spatial learning impairment in aged rats is associated with changes in hippocampal connectivity and plasticity. Several studies have explored the age-related deficit in spatial information processing by recording the location-specific activity of hippocampal neurons (place cells). However, these studies have generated disparate characterizations of place cells in aged rats as unstable (Barnes et al., 1997), resistant to change (Tanila et al., 1997b; Oler and Markus, 2000; Wilson et al., 2003), or delayed in using external cues (Rosenzweig et al., 2003). To reconcile these findings, we recorded place cells from aged and young rats as they repeatedly explored both a highly familiar environment and an initially novel environment, and we repeatedly tested whether the place fields formed in the novel environment were anchored by external cues. Initially, spatial representations in aged rats were abnormally maintained between the familiar and novel environments. Then, new representations were formed but were also delayed in becoming anchored to the external landmarks. Finally, even when the new spatial representations became bound to the landmarks, they were multi-stable across repetitive exposures to the formerly novel environment. These observations help to reconcile previously divergent characterizations of spatial representation in aged rats and suggest a model of cognitive aging and hippocampal function.

Key words: place cells; spatial memory; aging; hippocampus; novel environment; age-associated cognitive impairment

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Received Nov 1, 2003; revised March 2, 2004; accepted March 2, 2004.

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