Abstract

Nucleus reuniens receives dense projections from both the hippocampus and the frontal cortices. Reflecting these connections, this nucleus is thought to enable executive functions, including those involving spatial learning. The mammillary bodies, which also support spatial learning, again receive dense hippocampal inputs, as well as lighter projections from medial frontal areas. The present study, therefore, compared the sources of these inputs to nucleus reuniens and the mammillary bodies. Retrograde tracer injections in rats showed how these two diencephalic sites receive projections from separate cell populations, often from adjacent layers in the same cortical areas. In the subiculum, which projects strongly to both sites, the mammillary body inputs originate from a homogenous pyramidal cell population in more superficial levels, while the cells that target nucleus reuniens most often originate from cells positioned at a deeper level. In these deeper levels, a more morphologically diverse set of subiculum cells contributes to the thalamic projection, especially at septal levels. While both diencephalic sites also receive medial frontal inputs, those to nucleus reuniens are especially dense. The densest inputs to the mammillary bodies appear to arise from the dorsal peduncular cortex, where the cells are mostly separate from deeper neurons that project to nucleus reuniens. Again, in those other cortical regions that innervate both nucleus reuniens and the mammillary bodies, there was no evidence of collateral projections. The findings support the notion that these diencephalic nuclei represent components of distinct, but complementary, systems that support different aspects of cognition.

Highlights

  • Two diencephalic nuclei, the mammillary bodies (MB) and nucleus reuniens (RE) share anatomical and functional properties

  • In the subiculum there was typically a distinction based on laminar level, such that while the inputs to nucleus reuniens arose from similar anterior‐posterior levels as those to the mammillary bodies, they predominantly originated in deeper cells

  • While many of the subiculum projections to nucleus reuniens arose from polymorphic cells, the dense projections to the mammillary bodies consistently arose from pyramidal cells

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Summary

Introduction

The mammillary bodies (MB) and nucleus reuniens (RE) share anatomical and functional properties. Electrophysiological recordings reveal that both the mammillary bodies and nucleus reuniens contain units with spatial properties, including head direction cells (Jankowski et al, 2014; Stackman & Taube, 1998) Consistent with these anatomical and electrophysiological findings, lesions in both sites can disrupt tests of spatial working memory such as location nonmatching (Beracochea & Jaffard, 1987; Cholvin et al, 2013; Hembrook & Mair, 2011; Hembrook, Onos, & Mair, 2012; Layfield, Patel, Hallock, & Griffin, 2015; Vann & Aggleton, 2003; Vann & Nelson, 2015). While lesions of nucleus reuniens spare initial acquisition of this same task, they affect performance during probe tests (Dolleman‐van der Weel, Morris, & Witter, 2009) and disrupt long‐term retention of the escape location (Loureiro et al, 2012) These patterns of anatomical and behavioural findings raise questions over the extent to which these two nuclei receive inputs from the same or different sources within the hippocampus and frontal cortices. The term ‘frontal cortices’ incorporates infralimbic, prelimbic, anterior cingulate, precentral, orbital and agranular insular cortices (Kolb, 1984; Krettek & Price, 1977), the terminology for sites within this region adheres to Paxinos and Watson (2004)

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