Abstract
Spatial learning and memory processes depend on anatomical and functional interactions between the hippocampus and the entorhinal cortex. A key neurophysiological component of these processes is hippocampal theta rhythm, which can be driven from subcortical areas including the pontine nucleus incertus (NI). The NI contains the largest population of neurons that produce and presumably release the neuropeptide, relaxin-3, which acts via the Gi/o-protein-coupled receptor, relaxin-family peptide 3 receptor (RXFP3). NI activation induces general arousal including hippocampal theta, and inactivation induces impairment of spatial memory acquisition or retrieval. The primary aim of this study was to map the NI/relaxin-3 innervation of the parahippocampal cortex (PHC), including the medial and lateral entorhinal cortex, endopiriform cortex, perirhinal, postrhinal, and ectorhinal cortex, the amygdalohippocampal transition area and posteromedial cortical amygdala. Retrograde tracer injections were placed in different parts of the medial and lateral entorhinal cortex, which produced prominent retrograde labeling in the ipsilateral NI and some labeling in the contralateral NI. Anterograde tracer injections into the NI and immunostaining for relaxin-3 produced fiber labeling in deep layers of all parahippocampal areas and some dispersed fibers in superficial layers. Double-labeling studies revealed that both hippocampal projecting and calcium-binding protein-positive (presumed GABAergic) neurons received a relaxin-3 NI innervation. Some of these fibers also displayed synaptophysin (Syn) immunoreactivity, consistent with the presence of the peptide at synapses; and relaxin-3-positive fibers containing Syn bouton-like staining were frequently observed in contact with hippocampal-projecting or calcium-binding protein-positive neuronal somata and more distal elements. Finally, in situ hybridization studies revealed that entorhinal neurons in the superficial layers, and to a lesser extent in deep layers, contain RXFP3 mRNA. Together, our data support functional actions of the NI/relaxin-3-parahippocampal innervation on processes related to memory, spatial navigation and contextual analysis.
Highlights
Generation and retrieval of explicit memories depends on complex interactions between the neocortex and the hippocampus, which are mediated by the entorhinal cortex (EC) of the parahippocampal region
In our descriptions of the occurrence and distribution of a RLN3/nucleus incertus (NI) innervation of the parahippocampal gyrus, we have adopted the general boundaries specified in popular atlases of the rat brain (Paxinos and Watson, 2014; Swanson, 2018), which describe the parahippocampal gyrus as occupying the ventral region between the rhinal fissure laterally and a medial indentation medially
We have considered the parahippocampal gyrus as composed of the perirhinal and postrhinal cortices around the rhinal fissure, the two main divisions of the EC, namely, the medial entorhinal (MEnt) and lateral entorhinal (LEnt), and the amygdalohippocampal transition area (AHiTr)
Summary
Generation and retrieval of explicit memories depends on complex interactions between the neocortex and the hippocampus, which are mediated by the entorhinal cortex (EC) of the parahippocampal region. The EC conveys multimodal sensory information from the neocortex to the hippocampal formation and vice-versa (Burwell, 2000). Processing along these bidirectional projections contributes to memory storage and retrieval inside the medial temporal lobe (Lavenex and Amaral, 2000). Outputs from the CA1 and subiculum fields innervate the deep layers V and VI of the EC, which relay projections back to the superficial layers of the EC (Dolorfo and Amaral, 1998; van Haeften et al, 2003) and to other areas of the neocortex (Cappaert et al, 2014; Witter et al, 2017)
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