Elsevier

Brain Research Bulletin

Volume 57, Issues 3–4, February–March 2002, Pages 455-461
Brain Research Bulletin

Comparison of thalamic populations in mammals and birds: expression of ErbB4 mRNA

https://doi.org/10.1016/S0361-9230(01)00678-5Get rights and content

Abstract

The expression of ErbB4 mRNA was examined in dorsal thalamic regions of chicks and rats. In rats, ErbB4 expression was observed in the habenular nuclei, the paraventricular nucleus, intermediodorsal nucleus, the central medial thalamic nucleus, the posterior nucleus, the parafascicular nucleus, the subparafascicular nucleus, the suprageniculate nucleus, the posterior limitans nucleus, the medial part of the medial geniculate nucleus, the peripeduncular nucleus, the posterior intralaminar nucleus, the lateral subparafascicular nucleus, the lateral posterior nucleus, and all ventral thalamic nuclei. In chicks, expression was observed in the subhabenular nucleus, the dorsomedialis posterior nucleus, the dorsointermedius posterior nucleus, the nucleus of the septomesencephalic tract, and areas surrounding the rotundus and ovoidalis nuclei, including the subrotundal and suprarotundal areas, and all ventral thalamic nuclei. Most cells within ovoidalis and rotundus were not labeled. The similar pattern of afferent and efferent projections originating from ErbB4-expressing regions of the mammalian and bird dorsal thalamus suggests that ErbB4 hybridizing cells may be derived from a single anlage that migrates into multiple thalamic regions. Most neurons in the rotundus and ovoidalis nuclei of chick may be homologous to unlabeled clusters of neurons intermingled with ErbB4-expressing cells of the mammalian posterior/intralaminar region.

Introduction

Our ideas of brain evolution are continually being tested and adapted as we learn more about connections, development, histochemical markers, and genetic expression. The identification of homologous pallial areas in the tetrapod telencephalon has been particularly difficult. The search for comparable brain regions has produced several major lines of thought, including the suggestion that the basolateral amygdalar complex of mammals and the dorsal ventricular ridge (neostriatum) of reptiles and birds are homologous 4, 5, 6. This concept has been intensely debated 8, 22, 30, 31, 36, 37. However, studies using developmental and genetic expression techniques have led to a growing consensus of opinion that a large portion of the reptilian/avian dorsal ventricular ridge is homologous to the mammalian amygdala, and perhaps also to the mammalian claustrum 31, 36, 37.

The telencephalic regions of mammals, reptiles, and birds are intimately connected with specific dorsal thalamic groups. A valid hypothesis of telencephalic evolution must be consistent with identified thalamic homologues, including their connections, development, histochemistry, and genetic expression. Thus, if the basolateral amygdalar complex of mammals is comparable to most of the dorsal ventricular ridge of birds and reptiles, then the thalamic nuclei that project to these regions should also be comparable. Based on connectional and histochemical analyses, nuclei in the posterior/intralaminar complex of mammals and the rotundus-ovoidalis-pararotundal nuclei of reptiles and birds have been suggested as likely homologues 6, 10.

Analyses of homologous gene expression domains suggest that the patterns of expression of early developmental genes are largely conserved 16, 32, 33, 34, 36. The aim of the present investigation was to compare the mRNA expression profile of the ErbB4 receptor gene in chicks and rats to identify potentially homologous thalamic regions. ErbB4 is a functional tyrosine kinase receptor for the neuregulin gene family of growth/differentiation factors 7, 43. The expression pattern of the ErbB4 receptor was selected because it appears to be stable throughout development and it is expressed in the posterior region of the rat thalamus, a region that is critical for understanding forebrain evolution.

Section snippets

Preparation of tissue

Adult rats were sacrificed by an injection with Beuthanasia [30–40 mg/kg, intraperitoneally (i.p.)]. The brains were removed, embedded in Tissue-Tek OCT compound (Electron Microscopy Sciences, Fort Washington, PA, USA), rapidly frozen, and sectioned using a cryostat at 16 μm onto Superfrost Plus slides (Fisher Chemical Co., Orangeburg, NY, USA). Chick embryos were obtained from fertilized eggs. The eggs were incubated from embryonic day 0 to 16 at 38°C. On embryonic day 16, the chick embryos

Results

This study addresses the ErbB4 expression pattern in the epithalamus, the dorsal thalamus, and the ventral thalamus. ErbB4 mRNA is expressed in many areas of the brain and displays specific patterns of labeling, which will not be addressed in this paper. Cells that were associated with overlying clusters of silver grains at least 10 times greater than background were considered to express ErbB4 mRNA FIG. 1, FIG. 2. The morphology of the labeled cells within the posterior thalamic region

Discussion

The present results in rat and chick demonstrate that neurons throughout the epithalamus (habenula) and the ventral thalamus express ErbB4 mRNA. Thus, our data are consistent with previous studies suggesting that these are homologous areas. The labeling pattern among the dorsal thalamic nuclei, however, is restricted to selected populations of neurons. This segregation suggests that expression of ErbB4 mRNA may be used to identify possible homologues in the dorsal thalamus of mammals and

Abbreviations

    APT

    anterior pretectal nucleus

    CL

    central lateral thalamic nucleus

    DIP

    nucleus dorsointermedius posterior thalami

    DLL

    nucleus dorsolateralis anterior, pars lateralis

    DLM

    nucleus dorsolateralis anterior, pars medialis

    DLP

    nucleus dorsolateralis posterior

    DMA

    nucleus dorsomedialis anterior

    DMP

    nucleus dorsomedialis posterior

    fr

    fasciculus retroflexus

    Glv

    nucleus geniculatus lateralis, pars ventralis

    IMD

    intermediodorsal thalamic nucleus

    LGd

    lateral geniculate nucleus, pars dorsalis

    LGv

    lateral geniculate nucleus, pars

Acknowledgements

We thank Drs. Loreta Medina and Luis Puelles for organizing and hosting this meeting. We also thank Dr. Phil Brauer for providing the fertilized chick eggs and Kerstin Lundgren and Caroline A. Miller for excellent technical assistance. This study was supported in part by National Institute of Health grant NS39128.

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