Behavioural Brain Research 174 (2006) 265–271
Research report
Constraints on hippocampal processing imposed by the connectivity
between CA1, subiculum and subicular targets
John Gigg
*
Faculty of Life Sciences, Jackson Mill, University of Manchester, Manchester M60 1QD, UK
Received 24 May 2006; accepted 12 June 2006
Available online 21 July 2006
Abstract
A long-held fundamental function of the rat hippocampus is to provide a spatial map of the environment. The principal hippocampal output
region for spatial information is area CA1 and the major target of CA1 is the subiculum. Thus, one possible role of the subiculum is to receive,
process and transmit information regarding location to areas outside the hippocampus.
Anatomical experiments in the rat have shown that the projections from CA1 to subiculum exist in a series of ‘nested loops’. Thus, each part
of CA1 does not connect with each part of the subiculum. In turn, the majority of subicular principal neurons at the end of these loops have only
one axonal projection target. The identity of these target areas depends on the location of the projecting cell within the subiculum, that is, neurons
in different loops (and different septo-temporal levels of the subiculum) project to different sites. Principal neurons in subiculum and CA1 are not
highly interconnected, suggesting that spatial information within any one of the nested loops is not shared amongst the others. This anatomical
arrangement suggests that spatial information from any one part of CA1 is sent only to the sub-population of subicular principal cells within the
same loop. In turn, this sub-population of subicular cells projects information to only a subset of the total range of subicular target areas. Thus,
these subicular targets receive spatial information from only a subset of those in CA1. One conclusion from this is that for subicular targets to
receive spatial information from the whole environment, area CA1 must have multiple spatial maps, one for each major projection (nested loop)
to the subiculum.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Hippocampus; CA1; Subiculum; Spatial map
1. Introduction
The ‘spatial map’ hypothesis of the hippocampal formation
is one of the most popular explanations for hippocampal func-
tion [42]. Place cells and their associated place fields constitute
the neural basis for these cognitive maps. Place cells were first
recorded more than 30 years ago and continue to form the basis
of a large research effort into how the hippocampus can guide
spatial behaviour [32,40,41,43,45]. Place cells have now been
recorded in all hippocampal fields (dentate gyrus (DG), CA3 and
CA1) as well as the entorhinal cortex (EC) and the subiculum
(SUB). However, whilst the presence of place cells in these areas
is ubiquitous, little effort has been given to analysing how the
environment is represented within hippocampal areas. This is
*
Tel.: +44 161 306 3876; fax: +44 161 306 3887.
E-mail address: j.gigg@manchester.ac.uk.
largely because there is no obvious topography for the represen-
tation of space in the hippocampus (e.g., [46]; but see [21,27]).
Thus, adjacent place cells do not necessarily fire in topographical
register. Nevertheless, the fact that there is no obvious topogra-
phy from electrophysiological recordings does not mean there
is no anatomical constraint on the mapping of space within the
hippocampus. Recent anatomical findings reviewed here have
shown that hippocampal areas, particularly those that provide
hippocampal output, are connected in a complex fashion. For
example, not every part of CA1 is connected to every part of the
subiculum. A major role of the hippocampus is to provide a map
of the environment. However, for every hippocampal target to
receive a complete map, a full map must be present in each
of these hippocampal loops. Such a spatial re-representation
may help to explain the remarkably high chances of finding
hippocampal place cells for any given environment at the end of
randomly placed hippocampal electrodes. Portions of the current
manuscript have been published elsewhere in abstract form [16].
0166-4328/$ – see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbr.2006.06.014