Research report
Vomeronasal inputs to the rodent ventral striatum

https://doi.org/10.1016/j.brainresbull.2007.10.028Get rights and content

Abstract

Vertebrates sense chemical signals through the olfactory and vomeronasal systems. In squamate reptiles, which possess the largest vomeronasal system of all vertebrates, the accessory olfactory bulb projects to the nucleus sphericus, which in turn projects to a portion of the ventral striatum known as olfactostriatum. Characteristically, the olfactostriatum is innervated by neuropeptide Y, tyrosine hydroxylase and serotonin immunoreactive fibers. In this study, the possibility that a structure similar to the reptilian olfactostriatum might be present in the mammalian brain has been investigated. Injections of dextran-amines have been aimed at the posteromedial cortical amygdaloid nucleus (the putative mammalian homologue of the reptilian nucleus sphericus) of rats and mice. The resulting anterograde labeling includes the olfactory tubercle, the islands of Calleja and sparse terminal fields in the shell of the nucleus accumbens and ventral pallidum. This projection has been confirmed by injections of retrograde tracers into the ventral striato-pallidum that render retrograde labeling in the posteromedial cortical amygdaloid nucleus. The analysis of the distribution of neuropeptide Y, tyrosine hydroxylase, serotonin and substance P in the ventral striato-pallidum of rats, and the anterograde tracing of the vomeronasal amygdaloid input in the same material confirm that, similar to reptiles, the ventral striatum of mammals includes a specialized vomeronasal structure (olfactory tubercle and islands of Calleja) displaying dense neuropeptide Y-, tyrosine hydroxylase- and serotonin-immunoreactive innervations. The possibility that parts of the accumbens shell and/or ventral pallidum could be included in the mammalian olfactostriatum cannot be discarded.

Introduction

Vertebrates sense chemical signals through the olfactory system. Tetrapods, in addition, possess the vomeronasal system, which detects mainly, but not exclusively, pheromones [4]. The vomeronasal system is particularly well-developed in some reptiles [27], where the accessory olfactory bulb predominantly projects to the nucleus sphericus [11], [17], a part of the vomeronasal amygdala that occupies up to one third of the telencephalic volume. The nucleus sphericus, in turn, projects massively to the basal ganglia, specifically, to the olfactostriatum [10], classically defined in reptiles as a striatal structure [2], [3], [6], [8]. The reptilian olfactostriatum can be defined, therefore, as a specialized vomeronasal structure within the ventral striatum that chemoarchitectonically is densely immunoreactive for neuropeptide Y and serotonin and shows moderate-to-weak immunoreactivity for tyrosine hydroxylase [19], [20], [21].

In the present study, the possibility that a structure similar to the olfactostriatum might be present in the mammalian ventral striatum has been investigated using a combination of anterograde (including injections in the posteromedial cortical amygdaloid nucleus, the putative mammalian homologue of the reptilian nucleus sphericus) and retrograde (injections in the basal ganglia) tract-tracing and immunohistochemical methods (including neuropeptide Y, tyrosine hydroxylase, serotonin and substance P). Substance P has been used to identify ventral pallidal territories and differentiate from ventral striatal areas [5]. Our data indicate the presence of a specialized structure in the mammalian basal ganglia similar to the reptilian olfactostriatum, which includes parts of the olfactory tubercle and some islands of Calleja.

Section snippets

2.1 Animals

Fifteen adult male and female Sprague–Dawley rats from the University Hospital of Albacete and 10 female C57BL/J6 mice (Harlan, Barcelona) were used in the present study. Experimental procedures were carried out according to the guidelines of the European Community on Welfare of Research Animals (directive 86/609/EEC) and were approved by the Ethical Committees of Animal Research of the Universities of Castilla-La Mancha and València.

2.2 Injection procedures

Eleven rats were intraperitoneally injected with a combined

3.1 Tract-tracing experiments in rats

Six rats received iontophoretic injections of either biotinylated or fluorescein-labeled dextran-amine in the posteromedial cortical amygdaloid nucleus. Case 9305 is described as example. Injection of fluorescein-labeled dextran-amine is located at caudal levels of the posteromedial cortical amygdaloid nucleus with minor involvement of the amygdalo-hippocampal area (Fig. 1A). Anterograde (arrows Fig. 1B) and retrograde labeling could be observed in the contralateral posteromedial cortical

Discussion

The aim of the present study was to investigate the presence of tertiary vomeronasal structure in the mammalian basal ganglia similar to that described in reptiles, i.e., the olfactostriatum [10], [19], [20], [21]. The term “olfactostriatum” was classically introduced to name a part of the striatal complex mainly related to olfactory and visceral inputs [8]. The term was later redefined based on cytoarchitectonical grounds [2], [3], [6]. Recently, this area has been shown to receive vomeronasal

Acknowledgments

Authors thank members of LNH and LCFN for fruitful discussions and Dr. García Olmo for her help with animals. Supported by The Autonomous Government of Castilla-La Mancha-FEDER (Grants PAC-05-007-01, GCS-2006_E/03 and PI-2006/15 to AMM; GC04007 to RI; PAC-05-007-02 to EL), The Spanish Ministry of Education and Science-FEDER (BFU2004-04272/BFI to FMG), The Autonomous Valencian Government (ACOMP06/258 to FMG) and The University of Valencia (Programa Cinc Segles predoctoral grant to AN).

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