Complementary subicular pathways to the anterior thalamic nuclei and mammillary bodies in the rat and macaque monkey brain.

Kat Christiansen,Christopher M Dillingham,Richard C Saunders,Seralynne D Vann,Nicholas F Wright,John P Aggleton,Helen Barbas

doi:10.1111/ejn.13208

Kat Christiansen, Christopher M Dillingham + Show 5 more

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https://doi.org/10.1111/ejn.13208

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Abstract

The origins of the hippocampal (subicular) projections to the anterior thalamic nuclei and mammillary bodies were compared in rats and macaque monkeys using retrograde tracers. These projections form core components of the Papez circuit, which is vital for normal memory. The study revealed a complex pattern of subicular efferents, consistent with the presence of different, parallel information streams, whose segregation appears more marked in the rat brain. In both species, the cells projecting to the mammillary bodies and anterior thalamic nuclei showed laminar separation but also differed along other hippocampal axes. In the rat, these diencephalic inputs showed complementary topographies in the proximal–distal (columnar) plane, consistent with differential involvement in object‐based (proximal subiculum) and context‐based (distal subiculum) information. The medial mammillary inputs, which arose along the anterior–posterior extent of the rat subiculum, favoured the central subiculum (septal hippocampus) and the more proximal subiculum (temporal hippocampus). In contrast, anterior thalamic inputs were largely confined to the dorsal (i.e. septal and intermediate) subiculum, where projections to the anteromedial nucleus favoured the proximal subiculum while those to the anteroventral nucleus predominantly arose in the distal subiculum. In the macaque, the corresponding diencephalic inputs were again distinguished by anterior–posterior topographies, as subicular inputs to the medial mammillary bodies predominantly arose from the posterior hippocampus while subicular inputs to the anteromedial thalamic nucleus predominantly arose from the anterior hippocampus. Unlike the rat, there was no clear evidence of proximal–distal separation as all of these medial diencephalic projections preferentially arose from the more distal subiculum.

Highlights

Analyses of different functions within the hippocampus often involve comparisons among its principal subareas, i.e. dentate gyrus, CA fields and subiculum (Lee et al, 2005; O’Mara, 2005; Hunsaker et al, 2008; Chinnakkaruppan et al, 2014; Hitti & Siegelbaum, 2014; Schlighting et al, 2014) or comparisons along its anterior– posterior (AP) axis (Moser et al, 1995; Colombo et al, 1998; Bannerman et al, 1999; Fanselow & Dong, 2010; Poppenck & Moscovitch, 2011; Aggleton, 2012; Poppenck et al, 2013; Strange et al, 2014; Chase et al, 2015). [Note that in the rodent, the temporal hippocampus is homologous with the primate anterior hippocampus, while the septal hippocampus is homologous with the primate posterior hippocampus (Strange et al, 2014)]
Cells projecting to the medial mammillary nucleus, the anteroventral thalamic nucleus (AV) and the anteromedial thalamic nucleus (AM) all displayed different topographies in the proximal–distal plane (Figs 1, 3 and 4)
The majority of projections to the mammillary body (MB) came from the posterior subiculum, while the inputs to the AM predominantly arose from the anterior subiculum

Summary

Introduction

Analyses of different functions within the hippocampus often involve comparisons among its principal subareas, i.e. dentate gyrus, CA fields and subiculum (Lee et al, 2005; O’Mara, 2005; Hunsaker et al, 2008; Chinnakkaruppan et al, 2014; Hitti & Siegelbaum, 2014; Schlighting et al, 2014) or comparisons along its anterior– posterior (AP) axis (Moser et al, 1995; Colombo et al, 1998; Bannerman et al, 1999; Fanselow & Dong, 2010; Poppenck & Moscovitch, 2011; Aggleton, 2012; Poppenck et al, 2013; Strange et al, 2014; Chase et al, 2015). [Note that in the rodent, the temporal (ventral) hippocampus is homologous with the primate anterior hippocampus, while the septal (dorsal) hippocampus is homologous with the primate posterior hippocampus (Strange et al, 2014)]. The present study mapped the topographic organisation of the hippocampal neurons projecting to the anterior thalamic nuclei and mammillary bodies (MBs) in the rat (Experiment 1) and monkey (Experiment 2). These projections arise from the subiculum (Meibach & Siegel, 1977; Rosene & Van Hoesen, 1977; Sikes et al, 1977; Swanson & Cowan, 1977; Aggleton et al, 1986, 2005), in which the ‘proximal’ subiculum is closest to the CA1 border while the ‘distal’ subiculum is furthest from CA1, i.e. adjacent to the presubiculum. While previous tracer studies have described these connections in both rats (e.g. Meibach & Siegel, 1977; Naber & Witter, 1998; Ishizuka, 2001; Wright et al, 2013) and monkeys (Krayniak et al., 1979; Aggleton et al, 1986, 2005; Xiao & Barbas, 2002b; Saunders et al, 2005), there has been little attempt to quantify or compare the sources of these projections across species

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