Elsevier

Brain Research

Volume 1094, Issue 1, 13 June 2006, Pages 138-148
Brain Research

Research Report
The supragenual nucleus: A putative relay station for ascending vestibular signs to head direction cells

https://doi.org/10.1016/j.brainres.2006.03.101Get rights and content

Abstract

Head direction (HD) cells located in several regions of the brain, including the postsubiculum, retrosplenial cortex, lateral dorsal thalamic nucleus, anterior dorsal thalamic nucleus, and lateral mammillary nucleus, provide a signal of the rat's momentary directional heading. Experimental evidence suggests that vestibular inputs are critical for the maintenance these cells' directional sensitivity. However, it is still unclear how vestibular information is conveyed to the HD cell-related circuitry. In a recent study, the supragenual nucleus (SG) was suggested as a putative relay of vestibular inputs to this circuitry. In the present study, using anterograde and retrograde tract-tracing methods, we first investigated whether the SG is in a position to convey vestibular inputs. Next, we examined the projections of the SG with the Phaseolus vulgaris leucoagglutinin method. Our results indicate that the SG receives direct inputs from the medial vestibular nucleus and projects to elements of the HD cell-related circuitry, providing a massive input to the contralateral dorsal tegmental nucleus and a moderately dense projection to the shell region of the lateral mammillary nucleus. Overall, the present findings serve to clarify how vestibular inputs reach the HD cell-related circuit and point out the SG as an important interface to this end.

Introduction

Head direction (HD) cells discharge as a function of the animal's head direction in the horizontal plane and are independent of the rat's location in the environment as well as ongoing behavior. Evidence suggests that these cells participate in navigation and spatial cognition (Muller et al., 1996). The circuitry responsible for the generation and maintenance of the HD signal has been extensively studied, and HD cells have been identified in the postsubiculum (Taube et al., 1990), retrosplenial cortex (Chen et al., 1994, Cho and Sharp, 2001), lateral dorsal thalamic nucleus (Mizumori and Williams, 1993), anterior dorsal thalamic nucleus (Taube, 1995), and lateral mammillary nucleus (Blair et al., 1998, Stackman and Taube, 1998).

Vestibular information plays an essential role in the generation of HD signal. Recent lesion studies (Stackman and Taube, 1997, Stackman et al., 2002) indicated that inactivation of labyrinthine inputs abolished the direction-related activity of HD cells. Unfortunately, knowledge of the putative paths conveying vestibular information to the circuitry responsible for the generation and maintenance of the HD signal is still very fragmentary.

In this circuitry, the lateral mammillary nucleus plays a critical role to generate HD cell activity in upstream thalamic targets, such as the anterior dorsal thalamic nucleus (Blair et al., 1998). Vestibular information to the lateral mammillary nucleus is thought to be conveyed by the dorsal tegmental nucleus (Bassett and Taube, 2001, Sharp et al., 2001), which is classically known to provide a dense projection to this mammillary region (Guillery, 1957, Groenewegen and Van Dijk, 1984, Liu et al., 1984, Hayakawa and Zyo, 1990). Importantly, the dorsal tegmental nucleus contains head angular velocity cells likely to be involved in the generation of the HD signal (Bassett and Taube, 2001, Sharp et al., 2001).

In a recent study, by using viral transneuronal tracing method, the supragenual nucleus (SG) emerged as a putative relay of vestibular inputs to the lateral mammillary nucleus (Brown et al., 2005). The SG forms part of the periventricular gray surrounding the floor of the fourth ventricle and lies directly dorsal to the genu of the facial nerve. It is composed of round or ovoid medium-sized neurons, intensely stained with Nissl staining methods. In the present study, using anterograde and retrograde tract-tracing methods, we investigated the contribution of the SG in conveying vestibular inputs to the HD cell-related circuitry. Of particular relevance, the results from our study indicate the SG as an important relay station for vestibular information to the circuitry responsible for the generation and maintenance of the HD signal.

Section snippets

Fluorogold injections into the SG

In the present study, we first examined the pattern of retrograde labeling in the vestibular nuclei after Fluorogold injection in the SG. As illustrated in Fig. 1, in three experiments, the tracer deposit was centered in the SG with a faint tracer spreading over the adjacent caudal end of the nucleus incertus (indicated in Fig. 1 as a light gray area). In one case, a light tracer spreading also included the rostral tip of the nucleus prepositus (Fig. 1A). All these experiments yielded a similar

Discussion

The present findings support the idea that the SG works as an important relay station for vestibular inputs to the circuitry responsible for the generation and maintenance of the HD signal. First, using anterograde and retrograde tract-tracing methods, we were able to show that the medial vestibular nucleus provides a direct projection to the SG.

The results of the present retrograde axonal tract-tracing experiments indicate that vestibular inputs to the SG arise from the medial vestibular

Animals and housing

Adult male Wistar rats (n = 15), weighing about 250 g and obtained from the local breeding facilities, were used in the present study. The animals were kept under controlled temperature (23°C) and illumination (12-h cycle) in the animal quarters, and had free access to water and standard laboratory diet (Nutrilab CR1, Nuvital Nutrientes, Ribeirão Preto, SP, Brazil). Experiments were carried out in accordance with the National Institute of Health Guide for the Care and Use of Laboratory Animals

Acknowledgments

This research was supported by grants from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, no. 01/14039-9) and Conselho Nacional de Desenvolvimento Científico e Tecnologico (CNPq, no. 300360/2003-7) awarded to N.S.C.

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