Elsevier

Neuroscience

Volume 154, Issue 1, 12 June 2008, Pages 99-113
Neuroscience

Cochlear nucleus
Revealing the molecular layer of the primate dorsal cochlear nucleus

https://doi.org/10.1016/j.neuroscience.2007.12.016Get rights and content

Abstract

In nonprimate mammals, the dorsal cochlear nucleus (DCN) is thought to play a role in the orientation of the head toward sounds of interest by integrating acoustic and somatosensory information. Humans and higher primates might not use this system because of reported phylogenetic changes in DCN cytoarchitecture [Moskowitz N (1969) Comparative aspects of some features of the central auditory system of primates. Ann N Y Acad Sci 167:357–369; Moore JK, Osen KK (1979) The cochlear nuclei in man. Am J Anat 154:393–418; Moore JK (1980) The primate cochlear nuclei: loss of lamination as a phylogenetic process. J Comp Neurol 193:609–629]. In this study, we re-evaluated this question from a comparative perspective and examined the rhesus monkey (cercopithecoid primate) using more sensitive probes and higher resolution imaging methods. We used electron microscopy to identify parallel fibers and their synapses, and molecular markers to determine that primates exhibit the main components of excitatory neurotransmission as other mammals. We observed that characteristics of the monkey molecular layer resembled what has been reported for nonprimates: (1) immunohistochemistry revealed many unmyelinated, thin axons and en passant glutamatergic synapses on dendritic spines; (2) immunohistochemistry for phosphodiesterase (PDE10A) showed the nuclei of granule cells distributed in the external molecular layer and the deep layers in the DCN; (3) antibodies for the inositol trisphosphate receptor (IP3r) and calbindin immunostained cartwheel cells; (4) postembedding immunogold labeling revealed synaptic expression of AMPA and delta glutamate receptor subunits on spines in parallel fiber endings; and (5) parallel fibers use vesicular glutamate transporter 1 (VGLUT1) to package glutamate into the synaptic vesicles and to mediate glutamate transport. These observations are consistent with the argument that the rhesus monkey DCN has neuronal features similar to those of other nonprimate mammals.

Section snippets

Tissue procedure

Tissue from rhesus monkeys was obtained after transcardial perfusion at the Johns Hopkins Medical School, Baltimore, MD, USA, or the Emory Primate Center, Atlanta, GA, USA. At both institutions, animal protocols were approved by the institutional animal care and use committees and followed NIH guidelines. All experiments conformed to named local and international guidelines on the ethical use of animals. This research minimized the number of animals used and their suffering.

Three rhesus monkeys

Granule cells and PFs in the primate DCN

Nissl staining was used to determine whether the primate DCN had a laminar organization. Coronal sections revealed a layered organization in the rhesus DCN (Fig. 1A). There was a superficial or molecular layer (layer I) with scattered small nuclei and a deeper region (layers II and III) with abundant nuclei of different shapes and sizes (8–20 µm). Large elongated cell bodies of fusiform cells (20 µm in size) were clearly observed distributed in layer II and formed a discrete but distinguishable

Discussion

By using electron microscopy and immunohistochemistry at the light and electron microscopic level we observed that the organization of the primate DCN is similar to that of the nonprimate mammal. The finding of many unmyelinated thin axons and the characteristic en passant glutamatergic synapses on dendritic spines within the molecular layer strongly support these arguments. Furthermore, we showed that the primate DCN share the main molecular components of excitatory neurotransmission with

Acknowledgments

We acknowledge NIH/NIDCD RO1 DC006881 to M.E.R., RO1 DC004395 to D.K.R. and NSF DBI-0420580 for funds to purchase the Tecnai G2 Spirit Biotwin electron microscope. We thank D. Robert Wenthold for kindly providing the antibodies for GluR1, Glu2/3, GluR4 and delta [1/2]. Antibodies directed against PDF10A were generously provided by Pfizer, Inc.

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