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The Journal of Neuroscience, January 30, 2008, 28(5):1034-1045; doi:10.1523/JNEUROSCI.4607-07.2008

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Behavioral/Systems/Cognitive
Qualitatively Different Hippocampal Subfield Engagement Emerges with Mastery of a Spatial Memory Task by Rats

Guillaume L. Poirier, Eman Amin, and John P. Aggleton

School of Psychology, Cardiff University, Cardiff CF10 3AT, United Kingdom

Correspondence should be addressed to Guillaume L. Poirier, School of Psychology, Cardiff University, 70 Park Place, Cardiff CF10 3AT, UK. Email: PoirierG{at}cardiff.ac.uk

The parallel, entorhinal cortex projections to different hippocampal regions potentially support separate mnemonic functions. To examine this possibility, rats were trained in a radial-arm maze task so that hippocampal activity could be compared after "early" (two sessions) or "late" (five sessions) learning. Induction of the immediate-early gene Zif268 was then measured, so revealing possible activity differences across hippocampal subfields and the parahippocampal cortices. Each rat in the two experimental groups (early, late) was also yoked to a control rat that obtained the same number of rewards, visited the same number of maze arms, and spent a comparable amount of time in the maze. Although overall Zif268 levels did not distinguish the four groups, significant correlations were found between spatial memory performance and levels of dentate gyrus Zif268 expression in the early but not the late training group. Conversely, hippocampal fields CA3 and CA1 Zif268 expression correlated with performance in the late but not the early training group. This reversal in the correlation pattern was echoed by structural equation modeling, which revealed dynamic changes in effective network connectivity. With early training, the dentate gyrus appeared to help determine CA1 activity, but by late training the dentate gyrus reduced its neural influence. Furthermore, CA1 was distinguished from CA3, each subfield developing opposite relations with task mastery. Thus, functional entorhinal cortex coupling with CA1 activity became more direct with additional training, so producing a trisynaptic circuit bypass. The present study reveals qualitatively different patterns of hippocampal subfield engagement dependent on task demands and mastery.

Key words: effective connectivity; network; immediate-early gene; Zif268; hippocampal subfields; radial-arm maze

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Received July 30, 2007; revised Dec. 10, 2007; accepted Dec. 14, 2007.

Correspondence should be addressed to Guillaume L. Poirier, School of Psychology, Cardiff University, 70 Park Place, Cardiff CF10 3AT, UK. Email: PoirierG{at}cardiff.ac.uk

This article has been cited by other articles:

				S. Renaudineau, B. Poucet, S. Laroche, S. Davis, and E. Save Impaired long-term stability of CA1 place cell representation in mice lacking the transcription factor zif268/egr1 PNAS, July 14, 2009; 106(28): 11771 - 11775. [Abstract] [Full Text] [PDF]

				Y. Porte, M. C. Buhot, and N. E. Mons Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus Learn. Mem., December 2, 2008; 15(12): 885 - 894. [Abstract] [Full Text] [PDF]

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