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Journal List > PLoS Biol > v.7(4); Apr 2009
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PubMed articles by:
Bast, T.
Wilson, I.
Witter, M.
Morris, R.
PLoS Biol. 2009 April; 7(4): e1000089.
Published online 2009 April 21. doi: 10.1371/journal.pbio.1000089.
PMCID: PMC2671558
Copyright : © 2009 Bast et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
From Rapid Place Learning to Behavioral Performance: A Key Role for the Intermediate Hippocampus
Tobias Bast,1,2* Iain A Wilson,1† Menno P Witter,3,4 and Richard G. M Morris1
1 Centre for Cognitive and Neural Systems (CCNS), School of Biomedical Sciences, University of Edinburgh, Edinburgh, United Kingdom
2 School of Psychology and Institute of Neuroscience, University of Nottingham, Nottingham, United Kingdom
3 Centre for the Biology of Memory and Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology (NTNU), Trondheim, Norway
4 Department of Anatomy and Neuroscience, VU University medical center, Amsterdam, the Netherlands
Mick D Rugg, Academic Editor
University of California, Irvine, United States of America
* To whom correspondence should be addressed. E-mail: tobias.bast/at/nottingham.ac.uk
Received October 3, 2008; Accepted March 6, 2009.
 
Abstract
Rapid place encoding by hippocampal neurons, as reflected by place-related firing, has been intensely studied, whereas the substrates that translate hippocampal place codes into behavior have received little attention. A key point relevant to this translation is that hippocampal organization is characterized by functional–anatomical gradients along the septotemporal axis: Whereas the ability of hippocampal neurons to encode accurate place information declines from the septal to temporal end, hippocampal connectivity to prefrontal and subcortical sites that might relate such place information to behavioral-control processes shows an opposite gradient. We examined in rats the impact of selective lesions to relevant parts of the hippocampus on behavioral tests requiring place learning (watermaze procedures) and on in vivo electrophysiological models of hippocampal encoding (long-term potentiation [LTP], place cells). We found that the intermediate hippocampus is necessary and largely sufficient for behavioral performance based on rapid place learning. In contrast, a residual septal pole of the hippocampus, although displaying intact electrophysiological indices of rapid information encoding (LTP, precise place-related firing, and rapid remapping), failed to sustain watermaze performance based on rapid place learning. These data highlight the important distinction between hippocampal encoding and the behavioral performance based on such encoding, and suggest that the intermediate hippocampus, where substrates of rapid accurate place encoding converge with links to behavioral control, is critical to translate rapid (one-trial) place learning into navigational performance.
 
Author Summary
The ability to remember locations in space is dependent on an area of the brain called the hippocampus. A much-studied property of neurons in the hippocampus is that they rapidly come to represent or code for specific places—i.e., the hippocampus “learns” places—as animals or humans move through an environment. Here, we identified in rats the hippocampal substrate enabling the translation of place learning into appropriate search and approach behavior (similar to the task of returning to a novel place where you parked your car). We examined the impact of selective lesions to distinct parts of the hippocampus on behavior requiring rapid place learning and on in vivo electrophysiological models of hippocampal learning such as place-related neuronal activity. We showed that translation of rapid place learning into efficient search behavior requires the “intermediate” region of the hippocampus, a region that likely combines anatomical links to visuospatial information processed by the neocortex with links to behavioral control through prefrontal cortex and subcortical sites. In contrast, the so-called “septal” region of the hippocampus, which features the relevant anatomical links to visuospatial information processing, can sustain rapid place learning (as reflected by formation of place-related neuronal firing), but not translate such learning into appropriate search and approach behavior.
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