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Comparison of thalamic populations in mammals and birds: expression of ErbB4 mRNA
Brain Research Bulletin, Vol. 57, Nos. 3/4, pp. 455– 461, 2002 Copyright © 2002 Elsevier Science Inc. Printed in the USA. All rights reserved 0361-9230/02/$–see front matter
PII S0361-9230(01)00678-5
Comparison of thalamic populations in mammals and birds: Expression of ErbB4 mRNA Laura L. Bruce,1* Harley I. Kornblum2 and Kim B. Seroogy3 1
Department of Biomedical Sciences, Creighton University, Omaha, NE, USA; 2Departments of Pharmacology and Pediatrics, UCLA School of Medicine, Los Angeles, CA, USA; and 3Department of Anatomy and Neurobiology, University of Kentucky, Lexington, KY, USA
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. © 2002 Elsevier Science Inc.
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 [16,32–34,36]. 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.
KEY WORDS: Thalamus, Telencephalon, Evolution, Dorsal ventricular ridge, Neostriatum, Amygdala.
MATERIALS AND METHODS 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 m 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 were isolated and prepared as described for the rat brains. All experiments were conducted in accordance with the National Institutes of Health Guide regarding the care and use of animals for experimental procedures.
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 – 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].
In Situ Hybridization Methods The slide-mounted sections were processed for the detection of ErbB4 mRNA by using in situ hybridization with 35S-labeled
* Address for correspondence: Dr. Laura L. Bruce, Department of Biomedical Sciences, Creighton University, 2500 California Plaza, Omaha, NE 68178-0405, USA. Fax: (402) 280-5556; E-mail: [email protected]
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FIG. 1. Photomicrographs of ErbB4 mRNA-expressing cells in rostral (left) and caudal (right) levels of the rat thalamus. Bar ⫽ 1 mm.
cRNA probes, as described previously [19,35]. Hybridization was conducted at 60°C for 18 –24 h with the 35S-labeled cRNA at a concentration of 1 ⫻ 106 cpm/50 l/slide. After posthybridization ribonuclease treatment and washes, the sections were exposed to -Max Hyperfilm (Amersham, Arlington Heights, IL, USA) for 5 to 6 days to generate film autoradiograms. After development of the film, the sections were coated with NTB2 nuclear track emulsion (Kodak, Rochester, NY, USA; 1:1 in H20), air-dried, and exposed in sealed, light-tight slide boxes at 4°C for 3 to 4 weeks. After standard emulsion development, the sections were counterstained with cresyl violet (Sigma Chemical Co., St. Louis, MO, USA) and coverslipped with DPX mountant (Fluka, Milwaukee, WI, USA). Control procedures included prehybridization treatment of tissue with ribonuclease A (45°C for 30 min) and processing tissue with sense transcript controls; both resulted in no specific hybridization signal. 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 (Figs. 1 and 2). The morphology of the labeled cells within the posterior thalamic region suggested that they were neuronal and not glial. They were medium to large in size, and their nuclei and cytoplasm stained lightly with cresyl violet. This contrasted with small cells that had densely stained nuclei and did not express ErbB4 mRNA.
ErbB4 mRNA Expression in the Adult Rat Thalamus Epithalamus. Both the medial and lateral habenulae contained numerous labeled cells. The medial habenula was densely labeled, and the lateral habenula contained moderately labeled cells (Figs. 1 and 3). Midline thalamic nuclei. ErbB4 mRNA expression was limited to the caudal midline nuclei: the posterior part of the paraventricular thalamic nucleus (PVP), the intermediodorsal thalamic nucleus (IMD), and the medial edge of the central medial thalamic nucleus (CM). Labeled cells were not observed in midline nuclei located rostral or ventral to this group. Intralaminar nuclei. Hybridizing cells were observed predominantly in the posterior intralaminar nuclei. These included the caudomedial portions of the posterior nucleus (Po), the parafascicular nucleus (Pf), and the subparafascicular nucleus (SPF). In addition, a number of posterior intralaminar groups surrounding the medial geniculate nucleus were labeled, including the suprageniculate nucleus (SG), the posterior limitans nucleus (PLi), the medial part of the medial geniculate nucleus (MGm), the marginal zone of the medial geniculate nucleus (MZ), the peripeduncular nucleus (PPN), the posterior intralaminar nucleus (PIN), and the subparafascicular nucleus pars lateralis (SPFL). Clusters of labeled and unlabeled cells were present within these nuclei, which suggests that not all neurons expressed ErbB4 mRNA. Principal/association nuclei. Neurons expressing ErbB4 mRNA were observed in the medial portion of the lateral posterior nucleus. These hybridizing cells are located dorsal to the ErbB4expressing neurons in the posterior nucleus. Occasional labeled neurons were also present in the dorsal and ventral divisions of the medial geniculate nucleus.
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FIG. 2. Photomicrographs of ErbB4 mRNA-expressing cells in rostral (left) and caudal (right) levels of the chick thalamus. Bar ⫽ 1 mm.
Ventral thalamus. ErbB4 hybridizing neurons were present throughout the ventral thalamus, including the reticular thalamic nucleus, the zona incerta, and the ventral lateral geniculate nucleus. Expression was particularly dense in the reticular thalamic nucleus. ErbB4 mRNA Expression in the Thalamus of the Chick Epithalamus. Cells in both the lateral and medial habenulae expressed ErbB4 mRNA (Figs. 2 and 3). Dorsal thalamus. ErbB4 hybridization was observed in cells throughout the subhabenular nucleus (SHb), and in mediodorsal portions of the dorsomedialis posterior (DMP). The dorsointermedius posterior nucleus (DIP) contained large numbers of ErbB4-hybridizing neurons. Hybridizing cells were also present in areas surrounding the rotundus (Rt) and ovoidalis (Ov) nuclei, including the subrotundal (SRt) and suprarotundal lamina (SRL). Hybridizing neurons were also scattered throughout subdivisions of the rotundal nuclei, including the nucleus triangularis (T) and the posteromedial division of rotundus (Rpm). Labeled neurons were also scattered within the boundaries of the ovoidalis and rotundus nuclei, particularly along the caudoventral margins. The majority of cells within the ovoidalis and rotundus nuclei remained unlabeled. Cells expressing ErbB4 mRNA were present in the nucleus of the septomesencephalic tract (SPC), and were most numerous in the caudal regions of the nucleus. Ventral thalamus. Cells throughout the ventral thalamus expressed ErbB4 mRNA, including the dorsal and ventral divisions of the superior reticular thalamic nucleus (RSd and RSv), the ventrolateral thalamic nucleus (VLT), and the ventral lateral geniculate nucleus (GLv). Hybridizing cells in the dorsal and ventral
divisions of the superior reticular thalamic nucleus were especially numerous and densely labeled. 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 chicks, and this will be the focus of the Discussion. Gene expression patterns can and do vary between species, as occurs in the rhombomeres in the brainstem [14]. While keeping this in mind, we will first consider the possibility that the ErbB4 expression pattern has been retained in the tetrapod thalamus and seek homologies that require the fewest number of evolutionary changes. The location of the ErbB4-expressing neurons in rat and chick will be compared with (1) the locations of visual, auditory, and somatomotor projections from brainstem regions; (2) thalamic areas that express calcitonin gene-related peptide (CGRP); and (3) areas that project diffusely to the striatum, neostriatum (basolateral amygdala), and cortex. Finally, possible homologues of the avian rotundus and ovoidalis nuclei (which do not express ErbB4 mRNA) will be suggested. Overlap of ErbB4 Expression and Sensory Brainstem Targets Dorsal thalamic areas that express ErbB4 mRNA receive multiple auditory, visual, and somatomotor projections in both rats and
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FIG. 3. Drawings of transverse sections in rat (top) and chick (bottom) from rostral (left) and caudal (right) levels show the ErbB4 hybridization pattern (filled circles) in the epithalamus, dorsal thalamus, and ventral thalamus. Vertical hatches represent areas that project diffusely to the telencephalon, and horizontal hatches represent areas that project to specific areas of the neostriatum/lateral amygdala. Crosshatches represent areas that have both characteristics.
chicks. In rats, projections from the superficial superior colliculus, the deep superior colliculus, the cerebellum, the inferior colliculus, and the spinal cord project to the ErbB4-expressing areas of the dorsal thalamus [9,17,25,28]. In birds, comparable brainstem regions project to the ErbB4-labeled regions in the dorsal thalamus [13,15,20,40 – 42]. Thus, the similarity of ascending sensory projections to ErbB4-expressing targets in the dorsal thalamus of mammals and birds are consistent with the suggestion that ErbB4 is expressed in homologous thalamic regions. Overlap of ErbB4 and CGRP Expression ErbB4-expressing cells overlap the location of CGRP-containing neurons in both birds and mammals. In birds, CGRP expression is found in areas ventral and medial to ovoidalis. Additional thalamic regions, including parts of the nucleus dorsointermedius posterior and the nucleus dorsolateralis posterior, are labeled in chick and quail, which suggests that species differences may occur [3,23]. With the exception of CGRP-containing cells in the nucleus dorsolateralis posterior of chick and quail, these populations are colocalized within a subset of the ErbB4-expressing neurons. In rats, CGRP expression has been reported in the posterior thalamic region ventral and medial to the medial geniculate nucleus, including the peripeduncular nucleus, posterior intralaminar nucleus, subparafascicular nucleus pars lateralis, and subparafascicular nucleus [44], nuclei that also express ErbB4. Furthermore, in both rats and birds, these neurons project to diffuse targets in the striatum, amygdalar nuclei (including neostriatum of birds), and cortical regions [3,23,44].
Overlap of ErbB4 Expression and Areas That Project Diffusely to Telencephalon The ErbB4-expressing thalamic areas in rat and chick have similar efferent projection targets. They project to diffuse areas in the cortex, the amygdala/neostriatum, and the striatum [2,3,11,21, 23,24,27–29,39,44]. Possible Homologues of ErbB4-Expressing Neurons in the Dorsal Thalamus Dorsomedial-midline thalamic group. Previous studies have suggested homologues for some of the nuclei that contain ErbB4-expressing cells based on connectional and histochemical data [40]. Specifically, the mediodorsal portion of the dorsomedialis posterior, the subhabenular nucleus, and the dorsointermedius posterior nucleus of birds may be homologous with the medial part of the centromedial thalamic nucleus, the intermediodorsal thalamic nucleus, the posterior part of the paraventricular thalamic nucleus, and the posterior part of the parafascicular nucleus of rats [40]. Our results are largely consistent with these suggestions. Pararotundal-posterior intralaminar thalamic groups. Based on the similar afferent and efferent connections, histochemistry, and expression of ErbB4 mRNA detailed in the paragraphs above, we suggest that ErbB4-expressing neurons in the pararotundal thalamic groups of birds (including the nucleus subrotundus, suprarotundal lamina, the nucleus triangularis, and the nucleus rotundus pars posteromedialis) may be comparable to the posterior
ErbB4 EXPRESSION IN THALAMUS intralaminar thalamic nuclei of mammals (including the suprageniculate nucleus, the medial geniculate nucleus, pars medialis, the posterior intralaminar nucleus, the peripeduncular nucleus, and the subparafascicular nucleus). Futhermore, the similar pattern of afferent and efferent projections that originate from ErbB4-expressing regions of the mammalian and bird dorsal thalamus suggests that they may be derived from a single anlage that migrates into multiple thalamic regions that are derived from a different proliferative zone. A tangential cell migration from the medial and lateral ganglionic eminences into cortex has been described [1], but it is not known to occur in the thalamus so far. Nucleus tractus septomesencephalici compared with the lateral posterior and posterior nuclei. A remaining group of ErbB4-expressing cells in the dorsal thalamus of chicks and rats, in the tractus septomesencephalici and the medial portions of the lateral posterior nucleus and posterior nucleus, respectively, may be comparable cell groups. In addition to the ErbB4 expression, both groups appear to receive superficial tectal projections [17,28,38], and project to cortical and amygdalar/ neostriatal areas [21,27], but they are not known to project to the striatum. They also have similar topographical locations lateral to the habenula and near the surface of the dorsal thalamus. Together, these similarities suggest that portions of these nuclei may be comparable. Possible Mammalian Homologues of the Avian Rotundus and Ovoidalis Nuclei The lack of ErbB4 expression in most cells in the rotundus and ovoidalis nuclei suggests several possible evolutionary courses. 1. The ancestral anlage of the nuclei rotundus and ovoidalis expressed ErbB4 in mammals and birds, and then lost expression in the avian lineage. In this case, the ErbB4 labeling is not useful for identifying thalamic homologies. 2. The ancestral anlage of the rotundus and ovoidalis nuclei did not express ErbB4, which suggests the following alternatives: a. The rotundus and ovoidalis nuclei are a population of cells unique to reptiles and birds. b. Unlabeled cells homologous to the rotundus and ovoidalis nuclei are intermingled with ErbB4 neurons in mammals. This possibility is discussed below. c. The rotundus and ovoidalis nuclei are homologous to a population of unlabeled ErbB4 neurons located among the unlabeled thalamic nuclei of mammals. Although the rotundus and ovoidalis nuclei of birds are traditionally compared with the mammalian nucleus lateralis posterior and medial geniculate nucleus, pars dorsalis and ventralis, respectively [18], significant connectional differences make these comparisons tenuous. For example, these avian nuclei project to the striatum and to a specific area of the dorsal ventricular ridge, whereas most neurons in these mammalian nuclei do not project to the striatum and project to multiple areas of the cortex. Further studies of the connections, development, histochemistry, and genetic expression of the dorsal thalamus are needed to distinguish between these possibilities. Based on the following data, however, it appears likely that the mammalian homologues of the rotundus and ovoidalis nuclei are intermingled with ErbB4-expressing cells in the posterior/intralaminar thalamus. First, visual and auditory information from the superficial superior colliculus and inferior colliculus terminates preferentially in the suprageniculate nucleus and in the medial geniculate nucleus, pars medialis, and
459 peripeduncular nucleus, respectively [25,26]. Some of the neurons in the suprageniculate nucleus in turn project predominantly to the ventrolateral part of the lateral amygdala, the medial geniculate nucleus, pars medialis to the dorsal part, and the peripeduncular nucleus to the medial part [12,27,39]. Other neurons project to the isocortex. Thus, the lateral amygdala (and striatum) receive partially segregated visual and auditory information from the posterior thalamus, reminiscent of the highly specific projection from the nuclei rotundus and ovoidalis to the striatum and neostriatum of birds. 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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ABBREVIATIONS APT, CL, DIP, DLL, DLM, DLP, DMA, DMP, fr, Glv, IMD, LGd, LGv, LHb, LP, MD, MGd, MGm, MHb, MGv, OPT, OT, OTr, Ov, PC, Pf, PIN, PLi, Po, PPN, PVP, Rpm, RSd, RSv, Rt, SG, SHb, SNc, SPC, SPF, SPFL,
anterior pretectal nucleus central lateral thalamic nucleus nucleus dorsointermedius posterior thalami nucleus dorsolateralis anterior, pars lateralis nucleus dorsolateralis anterior, pars medialis nucleus dorsolateralis posterior nucleus dorsomedialis anterior nucleus dorsomedialis posterior fasciculus retroflexus nucleus geniculatus lateralis, pars ventralis intermediodorsal thalamic nucleus lateral geniculate nucleus, pars dorsalis lateral geniculate nucleus, pars ventralis lateral habenular nucleus nucleus lateralis posterior nucleus medialis dorsalis medial geniculate nucleus, pars dorsalis medial geniculate nucleus, pars medialis medial habenular nucleus medial geniculate nucleus, pars ventralis olivary pretectal nucleus optic tectum optic tract nucleus ovoidalis paracentral thalamic nucleus parafascicular thalamic nucleus posterior intralaminar nucleus posterior limitans nucleus posterior thalamic nucleus peripeduncular nucleus paraventricular thalamic nucleus, pars posterior nucleus rotundus pars posteromedialis nucleus reticularis superior pars dorsalis nucleus reticularis superior pars ventralis nucleus rotundus suprageniculate nucleus subhabenular nucleus substantia nigra pars compacta nucleus tractus septomesencephalici subparafascicular nucleus subparafascicular nucleus, lateral part
ErbB4 EXPRESSION IN THALAMUS SRt, SRL, T, VLT,
nucleus subrotundus suprarotundal lamina nucleus triangularis nucleus ventrolateralis thalami
461 VPM, VPL, VPPC, ZI,
ventroposterior medial thalamic nucleus ventroposterior lateral thalamic nucleus ventroposterior thalamic nucleus, pars parvocellularis zona incerta
PII S0361-9230(01)00678-5
Comparison of thalamic populations in mammals and birds: Expression of ErbB4 mRNA Laura L. Bruce,1* Harley I. Kornblum2 and Kim B. Seroogy3 1
Department of Biomedical Sciences, Creighton University, Omaha, NE, USA; 2Departments of Pharmacology and Pediatrics, UCLA School of Medicine, Los Angeles, CA, USA; and 3Department of Anatomy and Neurobiology, University of Kentucky, Lexington, KY, USA
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. © 2002 Elsevier Science Inc.
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 [16,32–34,36]. 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.
KEY WORDS: Thalamus, Telencephalon, Evolution, Dorsal ventricular ridge, Neostriatum, Amygdala.
MATERIALS AND METHODS 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 m 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 were isolated and prepared as described for the rat brains. All experiments were conducted in accordance with the National Institutes of Health Guide regarding the care and use of animals for experimental procedures.
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 – 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].
In Situ Hybridization Methods The slide-mounted sections were processed for the detection of ErbB4 mRNA by using in situ hybridization with 35S-labeled
* Address for correspondence: Dr. Laura L. Bruce, Department of Biomedical Sciences, Creighton University, 2500 California Plaza, Omaha, NE 68178-0405, USA. Fax: (402) 280-5556; E-mail: [email protected]
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FIG. 1. Photomicrographs of ErbB4 mRNA-expressing cells in rostral (left) and caudal (right) levels of the rat thalamus. Bar ⫽ 1 mm.
cRNA probes, as described previously [19,35]. Hybridization was conducted at 60°C for 18 –24 h with the 35S-labeled cRNA at a concentration of 1 ⫻ 106 cpm/50 l/slide. After posthybridization ribonuclease treatment and washes, the sections were exposed to -Max Hyperfilm (Amersham, Arlington Heights, IL, USA) for 5 to 6 days to generate film autoradiograms. After development of the film, the sections were coated with NTB2 nuclear track emulsion (Kodak, Rochester, NY, USA; 1:1 in H20), air-dried, and exposed in sealed, light-tight slide boxes at 4°C for 3 to 4 weeks. After standard emulsion development, the sections were counterstained with cresyl violet (Sigma Chemical Co., St. Louis, MO, USA) and coverslipped with DPX mountant (Fluka, Milwaukee, WI, USA). Control procedures included prehybridization treatment of tissue with ribonuclease A (45°C for 30 min) and processing tissue with sense transcript controls; both resulted in no specific hybridization signal. 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 (Figs. 1 and 2). The morphology of the labeled cells within the posterior thalamic region suggested that they were neuronal and not glial. They were medium to large in size, and their nuclei and cytoplasm stained lightly with cresyl violet. This contrasted with small cells that had densely stained nuclei and did not express ErbB4 mRNA.
ErbB4 mRNA Expression in the Adult Rat Thalamus Epithalamus. Both the medial and lateral habenulae contained numerous labeled cells. The medial habenula was densely labeled, and the lateral habenula contained moderately labeled cells (Figs. 1 and 3). Midline thalamic nuclei. ErbB4 mRNA expression was limited to the caudal midline nuclei: the posterior part of the paraventricular thalamic nucleus (PVP), the intermediodorsal thalamic nucleus (IMD), and the medial edge of the central medial thalamic nucleus (CM). Labeled cells were not observed in midline nuclei located rostral or ventral to this group. Intralaminar nuclei. Hybridizing cells were observed predominantly in the posterior intralaminar nuclei. These included the caudomedial portions of the posterior nucleus (Po), the parafascicular nucleus (Pf), and the subparafascicular nucleus (SPF). In addition, a number of posterior intralaminar groups surrounding the medial geniculate nucleus were labeled, including the suprageniculate nucleus (SG), the posterior limitans nucleus (PLi), the medial part of the medial geniculate nucleus (MGm), the marginal zone of the medial geniculate nucleus (MZ), the peripeduncular nucleus (PPN), the posterior intralaminar nucleus (PIN), and the subparafascicular nucleus pars lateralis (SPFL). Clusters of labeled and unlabeled cells were present within these nuclei, which suggests that not all neurons expressed ErbB4 mRNA. Principal/association nuclei. Neurons expressing ErbB4 mRNA were observed in the medial portion of the lateral posterior nucleus. These hybridizing cells are located dorsal to the ErbB4expressing neurons in the posterior nucleus. Occasional labeled neurons were also present in the dorsal and ventral divisions of the medial geniculate nucleus.
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FIG. 2. Photomicrographs of ErbB4 mRNA-expressing cells in rostral (left) and caudal (right) levels of the chick thalamus. Bar ⫽ 1 mm.
Ventral thalamus. ErbB4 hybridizing neurons were present throughout the ventral thalamus, including the reticular thalamic nucleus, the zona incerta, and the ventral lateral geniculate nucleus. Expression was particularly dense in the reticular thalamic nucleus. ErbB4 mRNA Expression in the Thalamus of the Chick Epithalamus. Cells in both the lateral and medial habenulae expressed ErbB4 mRNA (Figs. 2 and 3). Dorsal thalamus. ErbB4 hybridization was observed in cells throughout the subhabenular nucleus (SHb), and in mediodorsal portions of the dorsomedialis posterior (DMP). The dorsointermedius posterior nucleus (DIP) contained large numbers of ErbB4-hybridizing neurons. Hybridizing cells were also present in areas surrounding the rotundus (Rt) and ovoidalis (Ov) nuclei, including the subrotundal (SRt) and suprarotundal lamina (SRL). Hybridizing neurons were also scattered throughout subdivisions of the rotundal nuclei, including the nucleus triangularis (T) and the posteromedial division of rotundus (Rpm). Labeled neurons were also scattered within the boundaries of the ovoidalis and rotundus nuclei, particularly along the caudoventral margins. The majority of cells within the ovoidalis and rotundus nuclei remained unlabeled. Cells expressing ErbB4 mRNA were present in the nucleus of the septomesencephalic tract (SPC), and were most numerous in the caudal regions of the nucleus. Ventral thalamus. Cells throughout the ventral thalamus expressed ErbB4 mRNA, including the dorsal and ventral divisions of the superior reticular thalamic nucleus (RSd and RSv), the ventrolateral thalamic nucleus (VLT), and the ventral lateral geniculate nucleus (GLv). Hybridizing cells in the dorsal and ventral
divisions of the superior reticular thalamic nucleus were especially numerous and densely labeled. 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 chicks, and this will be the focus of the Discussion. Gene expression patterns can and do vary between species, as occurs in the rhombomeres in the brainstem [14]. While keeping this in mind, we will first consider the possibility that the ErbB4 expression pattern has been retained in the tetrapod thalamus and seek homologies that require the fewest number of evolutionary changes. The location of the ErbB4-expressing neurons in rat and chick will be compared with (1) the locations of visual, auditory, and somatomotor projections from brainstem regions; (2) thalamic areas that express calcitonin gene-related peptide (CGRP); and (3) areas that project diffusely to the striatum, neostriatum (basolateral amygdala), and cortex. Finally, possible homologues of the avian rotundus and ovoidalis nuclei (which do not express ErbB4 mRNA) will be suggested. Overlap of ErbB4 Expression and Sensory Brainstem Targets Dorsal thalamic areas that express ErbB4 mRNA receive multiple auditory, visual, and somatomotor projections in both rats and
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FIG. 3. Drawings of transverse sections in rat (top) and chick (bottom) from rostral (left) and caudal (right) levels show the ErbB4 hybridization pattern (filled circles) in the epithalamus, dorsal thalamus, and ventral thalamus. Vertical hatches represent areas that project diffusely to the telencephalon, and horizontal hatches represent areas that project to specific areas of the neostriatum/lateral amygdala. Crosshatches represent areas that have both characteristics.
chicks. In rats, projections from the superficial superior colliculus, the deep superior colliculus, the cerebellum, the inferior colliculus, and the spinal cord project to the ErbB4-expressing areas of the dorsal thalamus [9,17,25,28]. In birds, comparable brainstem regions project to the ErbB4-labeled regions in the dorsal thalamus [13,15,20,40 – 42]. Thus, the similarity of ascending sensory projections to ErbB4-expressing targets in the dorsal thalamus of mammals and birds are consistent with the suggestion that ErbB4 is expressed in homologous thalamic regions. Overlap of ErbB4 and CGRP Expression ErbB4-expressing cells overlap the location of CGRP-containing neurons in both birds and mammals. In birds, CGRP expression is found in areas ventral and medial to ovoidalis. Additional thalamic regions, including parts of the nucleus dorsointermedius posterior and the nucleus dorsolateralis posterior, are labeled in chick and quail, which suggests that species differences may occur [3,23]. With the exception of CGRP-containing cells in the nucleus dorsolateralis posterior of chick and quail, these populations are colocalized within a subset of the ErbB4-expressing neurons. In rats, CGRP expression has been reported in the posterior thalamic region ventral and medial to the medial geniculate nucleus, including the peripeduncular nucleus, posterior intralaminar nucleus, subparafascicular nucleus pars lateralis, and subparafascicular nucleus [44], nuclei that also express ErbB4. Furthermore, in both rats and birds, these neurons project to diffuse targets in the striatum, amygdalar nuclei (including neostriatum of birds), and cortical regions [3,23,44].
Overlap of ErbB4 Expression and Areas That Project Diffusely to Telencephalon The ErbB4-expressing thalamic areas in rat and chick have similar efferent projection targets. They project to diffuse areas in the cortex, the amygdala/neostriatum, and the striatum [2,3,11,21, 23,24,27–29,39,44]. Possible Homologues of ErbB4-Expressing Neurons in the Dorsal Thalamus Dorsomedial-midline thalamic group. Previous studies have suggested homologues for some of the nuclei that contain ErbB4-expressing cells based on connectional and histochemical data [40]. Specifically, the mediodorsal portion of the dorsomedialis posterior, the subhabenular nucleus, and the dorsointermedius posterior nucleus of birds may be homologous with the medial part of the centromedial thalamic nucleus, the intermediodorsal thalamic nucleus, the posterior part of the paraventricular thalamic nucleus, and the posterior part of the parafascicular nucleus of rats [40]. Our results are largely consistent with these suggestions. Pararotundal-posterior intralaminar thalamic groups. Based on the similar afferent and efferent connections, histochemistry, and expression of ErbB4 mRNA detailed in the paragraphs above, we suggest that ErbB4-expressing neurons in the pararotundal thalamic groups of birds (including the nucleus subrotundus, suprarotundal lamina, the nucleus triangularis, and the nucleus rotundus pars posteromedialis) may be comparable to the posterior
ErbB4 EXPRESSION IN THALAMUS intralaminar thalamic nuclei of mammals (including the suprageniculate nucleus, the medial geniculate nucleus, pars medialis, the posterior intralaminar nucleus, the peripeduncular nucleus, and the subparafascicular nucleus). Futhermore, the similar pattern of afferent and efferent projections that originate from ErbB4-expressing regions of the mammalian and bird dorsal thalamus suggests that they may be derived from a single anlage that migrates into multiple thalamic regions that are derived from a different proliferative zone. A tangential cell migration from the medial and lateral ganglionic eminences into cortex has been described [1], but it is not known to occur in the thalamus so far. Nucleus tractus septomesencephalici compared with the lateral posterior and posterior nuclei. A remaining group of ErbB4-expressing cells in the dorsal thalamus of chicks and rats, in the tractus septomesencephalici and the medial portions of the lateral posterior nucleus and posterior nucleus, respectively, may be comparable cell groups. In addition to the ErbB4 expression, both groups appear to receive superficial tectal projections [17,28,38], and project to cortical and amygdalar/ neostriatal areas [21,27], but they are not known to project to the striatum. They also have similar topographical locations lateral to the habenula and near the surface of the dorsal thalamus. Together, these similarities suggest that portions of these nuclei may be comparable. Possible Mammalian Homologues of the Avian Rotundus and Ovoidalis Nuclei The lack of ErbB4 expression in most cells in the rotundus and ovoidalis nuclei suggests several possible evolutionary courses. 1. The ancestral anlage of the nuclei rotundus and ovoidalis expressed ErbB4 in mammals and birds, and then lost expression in the avian lineage. In this case, the ErbB4 labeling is not useful for identifying thalamic homologies. 2. The ancestral anlage of the rotundus and ovoidalis nuclei did not express ErbB4, which suggests the following alternatives: a. The rotundus and ovoidalis nuclei are a population of cells unique to reptiles and birds. b. Unlabeled cells homologous to the rotundus and ovoidalis nuclei are intermingled with ErbB4 neurons in mammals. This possibility is discussed below. c. The rotundus and ovoidalis nuclei are homologous to a population of unlabeled ErbB4 neurons located among the unlabeled thalamic nuclei of mammals. Although the rotundus and ovoidalis nuclei of birds are traditionally compared with the mammalian nucleus lateralis posterior and medial geniculate nucleus, pars dorsalis and ventralis, respectively [18], significant connectional differences make these comparisons tenuous. For example, these avian nuclei project to the striatum and to a specific area of the dorsal ventricular ridge, whereas most neurons in these mammalian nuclei do not project to the striatum and project to multiple areas of the cortex. Further studies of the connections, development, histochemistry, and genetic expression of the dorsal thalamus are needed to distinguish between these possibilities. Based on the following data, however, it appears likely that the mammalian homologues of the rotundus and ovoidalis nuclei are intermingled with ErbB4-expressing cells in the posterior/intralaminar thalamus. First, visual and auditory information from the superficial superior colliculus and inferior colliculus terminates preferentially in the suprageniculate nucleus and in the medial geniculate nucleus, pars medialis, and
459 peripeduncular nucleus, respectively [25,26]. Some of the neurons in the suprageniculate nucleus in turn project predominantly to the ventrolateral part of the lateral amygdala, the medial geniculate nucleus, pars medialis to the dorsal part, and the peripeduncular nucleus to the medial part [12,27,39]. Other neurons project to the isocortex. Thus, the lateral amygdala (and striatum) receive partially segregated visual and auditory information from the posterior thalamus, reminiscent of the highly specific projection from the nuclei rotundus and ovoidalis to the striatum and neostriatum of birds. 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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ABBREVIATIONS APT, CL, DIP, DLL, DLM, DLP, DMA, DMP, fr, Glv, IMD, LGd, LGv, LHb, LP, MD, MGd, MGm, MHb, MGv, OPT, OT, OTr, Ov, PC, Pf, PIN, PLi, Po, PPN, PVP, Rpm, RSd, RSv, Rt, SG, SHb, SNc, SPC, SPF, SPFL,
anterior pretectal nucleus central lateral thalamic nucleus nucleus dorsointermedius posterior thalami nucleus dorsolateralis anterior, pars lateralis nucleus dorsolateralis anterior, pars medialis nucleus dorsolateralis posterior nucleus dorsomedialis anterior nucleus dorsomedialis posterior fasciculus retroflexus nucleus geniculatus lateralis, pars ventralis intermediodorsal thalamic nucleus lateral geniculate nucleus, pars dorsalis lateral geniculate nucleus, pars ventralis lateral habenular nucleus nucleus lateralis posterior nucleus medialis dorsalis medial geniculate nucleus, pars dorsalis medial geniculate nucleus, pars medialis medial habenular nucleus medial geniculate nucleus, pars ventralis olivary pretectal nucleus optic tectum optic tract nucleus ovoidalis paracentral thalamic nucleus parafascicular thalamic nucleus posterior intralaminar nucleus posterior limitans nucleus posterior thalamic nucleus peripeduncular nucleus paraventricular thalamic nucleus, pars posterior nucleus rotundus pars posteromedialis nucleus reticularis superior pars dorsalis nucleus reticularis superior pars ventralis nucleus rotundus suprageniculate nucleus subhabenular nucleus substantia nigra pars compacta nucleus tractus septomesencephalici subparafascicular nucleus subparafascicular nucleus, lateral part
ErbB4 EXPRESSION IN THALAMUS SRt, SRL, T, VLT,
nucleus subrotundus suprarotundal lamina nucleus triangularis nucleus ventrolateralis thalami
461 VPM, VPL, VPPC, ZI,
ventroposterior medial thalamic nucleus ventroposterior lateral thalamic nucleus ventroposterior thalamic nucleus, pars parvocellularis zona incerta