The ascending tectofugal visual system in amniotes: New insights
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1 Brain Research Bulletin 66 (2005) The ascending tectofugal visual system in amniotes: New insights Salvador Guirado,1,M a. Ángeles Real 1, José Carlos Dávila Department of Cell Biology, Genetics and Physiology, Faculty of Biology, University of Málaga, Málaga, Spain Available online 5 March 2005 Abstract Ascending tectal axons carrying visual information constitute a fiber pathway linking the mesencephalon with the dorsal thalamus and then with a number of telencephalic centers. The sauropsidian nucleus rotundus and its mammalian homologue(s) occupy a central position in this pathway. The aim of this study was analyzing the rotundic connections in reptiles and birds in relation with comparable connections in mammals, by using biotinylated dextran amines and the lipophilic carbocyanine dye DiI as tracing molecules. In general, rotundic connections in reptiles and birds are quite similar, especially with regards to pretectal and tectal afferences; as a novel finding, we describe varicose fibers arising from nucleus rotundus that reached the developing chick striatum. In addition, this study described the dorsal claustrum as a novel telencephalic target for the suprageniculate nucleus in mammals. Overall, telencephalic projections from the posterior/intralaminar complex of the mammalian thalamus can be compared with the telencephalic projections of the reptilian nucleus rotundus. With the exception of the isocortical connections, the mouse suprageniculate nucleus shares a number of afferent and efferent connections with the sauropsidian nucleus rotundus. Especially significant were the suprageniculate fibers reaching the striatum and then following to reach pallial derivatives such as the lateral amygdala (ventral pallium) and the dorsal claustrum (lateral pallium). These connections can be compared with the rotundic fibers reaching the ventromedial part of the anterior dorsal ventricular ridge in reptiles/entopallium in birds (ventral pallium) and the dorsolateral part of the anterior dorsal ventricular ridge in reptiles (lateral pallium), and probably the mesopallium in birds Elsevier Inc. All rights reserved. Keywords: Nucleus rotundus; Basal ganglia; Suprageniculate nucleus; Dorsal claustrum; Reptiles; Birds 1. Introduction Ascending tectal axons carrying visual information constitute a fiber pathway linking the mesencephalon with the dorsal thalamus and then with a number of telencephalic centers. Nucleus rotundus is the major relay station of this visual tectofugal pathway in the reptilian and avian dorsal thalamus [7,8,10]. For a number of years, the lateral posterior/pulvinar nucleus has been considered the mammalian homologue of the sauropsidian nucleus rotundus [9], mainly on the basis of the visual collicular afferences. However, it has been recently proposed that the reptilian nucleus rotundus may be the homologue as a field to parts of the posterior com- Corresponding author. Tel.: ; fax: address: guirado@uma.es (S. Guirado). 1 These authors contributed equally. plex/intralaminar nuclei of the dorsal thalamus in mammals, on the basis of topological and chemoarchitectonic criteria [3,15]. In this study, we analyzed the connections of nucleus rotundus in both reptiles and birds, in comparison with the connections of the mouse suprageniculate nucleus, a nucleus of the thalamic posterior complex which also receives visual collicular inputs [13], searching for hodological similarities among these nuclei. 2. Materials and methods Adult lizards and mice, as well as chick embryos were used in this study. Throughout the experimental work, animals were treated according to the European Communities Council Directive (86/609/EEC) for care and handling of animals in research /$ see front matter 2005 Elsevier Inc. All rights reserved. doi: /j.brainresbull
2 S. Guirado et al. / Brain Research Bulletin 66 (2005) BDA tracing method As tracing molecules for both lizards and mice we used biotinylated dextran amines (BDA 10K, Molecular Probes, Eugene, OR). After induction of deep anaesthesia with either a combination of ketamine (0.003 ml/g) and xylazine (0.001 ml/g) (mice) or diethyl ether (lizards), iontophoretic injections of BDA were performed by applying a 2 4 A positive-pulsed current for 20 min. After a survival time of 7 10 days, the animals were perfused transcardially with 0.1 M phosphate buffer (PB), containing 4% paraformaldehyde, M lysine and 0.01 M sodium periodate at room temperature, for 30 min. The brains were removed from the skulls and stored overnight at 4 C in the same fixative. Then, the brains were embedded in 4% agar, and 50 m-thick transverse or sagittal sections were obtained with a vibratome. To visualize the transported BDA, the sections were incubated in avidin biotin complex (Vectastain ABC standard kit; VEC- TOR), and revealed with nickel-enhanced diaminobenzidine (DAB; SIGMA). After a thorough wash in PBS, the sections were mounted on polylysinated slides, air-dried, counterstained with 1% toluidine blue in distilled water, dehydrated in ethanol, cleared in xylene, and cover-slipped with DPX (BDH, Poole, England) DiI tracing method The lipophilic carbocyanine dye DiI (Molecular Probes) was used as the tracing molecule for the chick embryos. Embryos of the embryonic day 14 (E14) were cold anesthetized and then were transcardially perfused with 0.1 M phosphate buffer saline (PBS), ph 7.4, followed by 2% paraformaldehyde and 1% glutaraldehyde in 0.1 M PB, ph 7.4. Then, brains were removed and postfixed in 4% paraformaldehyde overnight at 4 C. Brains were cut in the transverse plane, proceeding caudo-rostrally just to expose nucleus rotundus, and then a minute DiI crystal was deposited on it. Immediately, the surface of the tissue was covered with a drop of 4% agar to prevent crystal movements, and brains were incubated in 4% paraformaldehyde in PBS at C in the dark for days. Then, 100 m-thick, transverse or parasagittal sections were cut on a vibratome, collected in PB, mounted on slides and coverslipped. Sections were subsequently examined and photographed with a Nikon microscope equipped with epifluorescence and a digital camera. 3. Results In reptiles, selective injections of BDA into the nucleus rotundus gave rise to retrograde labelling in several neuronal groups in both the mesencephalon and diencephalon (Fig. 1A and B). Retrogradely labelled neurons were observed consistently within the optic tectum and the nucleus subpretectalis in the pretectum, as well as in several nuclei in the dorsal thalamus and part of the reticular complex in the ventral thalamus. Nucleus rotundus received most tectal visual afferents from neurons localized to the stratum griseum centrale. These tectorotundal neurons were multipolar with divergent ascending dendrites, which crossed the upper strata, ending in the stratum griseum et fibrosum superficiale. In its turn, nucleus rotundus projected to telencephalic targets, including the lateral amygdala, central amygdala, globus pallidus, lateral striatum and two parts of the anterior dorsal ventricular ridge: a dorsolateral part and a ventromedial part (dl, vm, Fig. 1B) [7]. Deposit of DiI crystals in the nucleus rotundus of embryonic chick brains (Fig. 1C), resulted in a strong fiber labelling in several telencephalic regions (Fig. 1D). Numerous stained fibers were observed in entopallium (formerly ectostriatum, a ventral pallial derivative which is part of the traditionally named dorsal ventricular ridge, DVR), as well as in other not described targets such as the lateral striatum and globus pallidus. Numerous fine processes displaying varicosities were clearly observed crossing both striatum and globus pallidus in parasagittal sections of the brain (Fig. 1E and F). A few axons bearing varicosities appeared to enter the perientopallial belt likely reaching the mesopallium (a lateral pallial derivative within the avian DVR; not shown). Regarding mammals, we carried out BDA injections in the mouse posterior thalamus, specifically in some nuclei bordering the medial geniculate nucleus known to receive visual input from intermediate/deep layers of the superior colliculus. After injections into the suprageniculate nucleus (Fig. 2A), retrogradely labelled neurons were consistently observed in collicular and pretectal cell populations. Within the superior colliculus, retrogradely labelled neurons were observed bilaterally (though they were mainly ipsilateral) in stratum griseum intermedium, and ipsilaterally in the stratum opticum (Fig. 2B). Labelled cells displayed wide dendritic arbors extending superficially (Fig. 2B, inset). Besides, retrogradely labelled cells were found in the reticular nucleus, lateral globus pallidus as well as the ectorhinal cortex and temporal association cortex. A strong to moderate anterograde fiber labelling was observed in several caudal telencephalic regions after BDA injections in the suprageniculate nucleus (Fig. 2C). These regions included the amygdalostriatal transition area, the caudatus-putamen, the lateral globus pallidus, the lateral amygdala (Fig. 2C E), and the ectorhinal and temporal association cortices. Especially prominent were the numerous varicose axons traversing (and probably forming synapses) the striatum (Fig. 2D). More rostrally in the telencephalon, a fine plexus of labelled axons was observed restricted to intermediate rostrocaudal levels of the dorsal claustrum (Fig. 2F, inset). Closer examination of this plexus showed numerous fine and varicose axons dispersed among claustral cells (Fig. 2G). Labelled axons within the dorsal claustrum were homogeneously distributed, and no differences in the innervation between the shell/core claustral compartments were
3 292 S. Guirado et al. / Brain Research Bulletin 66 (2005) Fig. 1. (A) Transverse section at a middle diencephalic level of the lizard brain, showing a BDA injection in nucleus rotundus (Rot). Scale bar: 250 m. (B) Parasagittal section of the lizard brain, showing neuron and fiber labelling in the major regions involved in the tecto-thalamo-telencephalic pathway. Scale bar: 500 m. (C) Transverse section at a middle diencephalic level of the embryonic chick brain, showing the DiI application site in Rot. Scale bar: 500 m. (D) Parasagittal section of a E14 embryonic chick brain. Strong fiber staining can be observed in entopallium (E), lateral striatum (St), and globus pallidus (GP). Scale bar: 200 m. (E) Detail of fine processes with varicosities crossing St. Scale bar: 100 m. (F) Fiber staining in globus pallidus and striatum. Scale bar: 75 m. observed. To corroborate that labelled axons in the dorsal claustrum arise from the suprageniculate nucleus, we made control injections into the dorsal claustrum resulting in retrogradely labelled neurons in the suprageniculate nucleus (as well as in other nuclei bordering the medial geniculate body, such as the posterior thalamic and posterior intralaminar nuclei). 4. Discussion In the present report, we summarize previous studies on the rotundic connections in lizards [4,7] and describe comparable connections in birds and mammals. In addition, this study demonstrates novel telencephalic targets for thalamic fibers in both birds and mammals. We will begin the discus-
4 S. Guirado et al. / Brain Research Bulletin 66 (2005) Fig. 2. (A) Transverse section of the mouse brain showing a BDA injection site in the suprageniculate nucleus (SG). Scale bar: 250 m. (B) Low-magnification photomicrograph of the superior colliculus. Scale bar: 250 m. Inset: Detail of the boxed area showing retrogradely labelled neurons in the stratum griseum intermedium (SGI) of the contralateral colliculus. Scale bar: 50 m. (C) Low power photomicrograph of a transverse section at a caudal telencephalic level. Positive axons can be observed in the amygdalostriatal transition area (AStr), caudatus-putamen (CPu), lateral globus pallidus (LGP) and lateral amygdala (La). Scale bar: 250 m. (D) Many labelled axons with varicosities can be observed in CPu. Scale bar: 100 m. (E) Detail of labelled fibers in La. Scale bar: 100 m. (F) Low power photomicrograph of a transverse section at an intermediate telencephalic level. Scale bar: 250 m. Inset: Detail of dorsal claustrum (Cl). Scale bar: 50 m. (G) High power photomicrograph showing some very fine varicose axons among claustral cells. Scale bar: 20 m. sion comparing connections of nucleus rotundus of reptiles and birds, and then comparing both with mammals. The reptilian and avian nucleus rotundus are considered homologous structures on the basis of a number of topological, chemical and hodological features. Nucleus rotundus is considered the major thalamic relay station of the visual tecto-telencephalic pathway in sauropsids. This thalamic nucleus receives a bilateral (though predominantly ipsilateral) visual input from neurons located in the stratum griseum centrale of the optic tectum [4,14,16], and its neurons project to the telencephalon, where they target discrete pallial regions of the dorsal ventricular ridge [7,8,10]. In reptiles, the rotundal projection terminates in two separate radial regions of the ADVR showing distinct cytoarchitecture and connections: a
5 294 S. Guirado et al. / Brain Research Bulletin 66 (2005) dorsolateral region (putative lateral pallial derivative) and a ventromedial region (putative ventral pallial derivative) [7]. Overall, rotundic connections in reptiles and birds are quite similar, especially with regards to pretectal and tectal afferences [4]; however, some differences appeared when the telencephalic targets were considered. An important difference concerned the rotundic input to the striatum. We have recently demonstrated that rotundic axons made numerous, probably en passant, excitatory contacts on striatal neurons in lizards [7], but this rotundo-striatal projection has not been recognized in birds [10]. Our DiI tracing data in the E14 embryonic chick brain (long-time after the rotundotelencephalic connections are established [19]) showed that numerous fine and varicose processes arising from nucleus rotundus crossed the lateral striatum in their pathway towards the entopallium. Although electron microscope studies are necessary to demonstrate actual synaptic contacts, the presence of axons bearing varicosities within the lateral striatum is suggestive of such synapses. Further studies in later developmental stages and adult chicks are necessary to check Fig. 3. (A) Schematic representation of the tecto-rotundic connections in reptiles and birds, and the superior colliculus-posterior thalamic connections in mammals. (B) Schematic representation of our proposed ascending tectofugal visual system in amniotes.
6 S. Guirado et al. / Brain Research Bulletin 66 (2005) whether the observed rotundo-striatal connections are transient features or not. Nevertheless, it is relevant that the ascending rotundic connections in the embryonic chick brain are very similar to those found in the adult reptile. On the basis of topological, chemoarchitectonic, and hodological evidence, it has been suggested that the reptilian nucleus rotundus is similar to parts of the posterior complex/intralaminar nuclei of the dorsal thalamus in mammals [1,3,15]. This proposal represents an alternative view to the more widespread one considering the sauropsidian nucleus rotundus and the mammalian lateral posterior/pulvinar nucleus as homologous, mainly on the basis of the visual tectal input [9]. Mammals have well documented collicular projections to the suprageniculate nucleus (as well as to other parts of the posterior nuclear group, intralaminar and midline nuclei; [11,12]), but in contrast to the tectal projection to the lateral posterior/pulvinar, which originates from neurons located to the stratum griseum superficiale, the superior colliculusposterior thalamus projections arise from intermediate/deep strata [12]. The mammalian intermediate stratum (SGI) of the superior colliculus can be compared with the sauropsidian stratum griseum centrale, where tecto-rotundic neurons are found, according to its topography deep to retinal terminal neuropiles and functional properties [17]. In this context, it is interesting to note that intermediate layers of the optic tectum in reptiles and birds, as in mammals, receive somatosensory and auditory inputs, in addition to the visual ones [2,18]. With regards to the ascending connections, it has been shown that nuclei in the posterior thalamus of the rat (including the suprageniculate nucleus, the medial division of the medial geniculate body, the posterior intralaminar nucleus, and the peripeduncular nucleus) project upon the striatum and the pallial claustroamygdaloid complex, in addition to specific areas of cortex [5,6,13]. Therefore, telencephalic projections from the posterior/intralaminar complex of the mammalian thalamus can be also compared with the telencephalic projections of the reptilian nucleus rotundus [7]. Thus, with the exception of the isocortical connections, the mouse suprageniculate nucleus shares a number of afferent and efferent connections with the sauropsidian nucleus rotundus. Especially significant is that many fibers enter the striatum (forming synapses en passant ) and then follow to reach pallial derivatives such as the lateral amygdala (ventral pallium) and the dorsal claustrum (lateral pallium), and these connections can be compared with those reaching the ventromedial part of ADVR in reptiles/entopallium in birds (ventral pallium) and the dorsolateral part of ADVR in reptiles (lateral pallium), and likely also reaching the mesopallium in birds. Of course, the mammalian lateral posterior/pulvinar nucleus projects to the striatum, lateral amygdala and isocortex, but it lacks connections with the dorsal claustrum. If our previous proposal (based on topological and chemoarchitectural features) that a number of nuclei in the posterior dorsal thalamus in the limit with the pretectum, including the suprageniculate, posterior intralaminar, and posterior thalamic nuclei represent, as a field, the mammalian homologue of the sauropsidian nucleus rotundus is certain, then a number of common basic patterns for the ascending tectofugal visual system in amniotes can be formulated, many of which have been shown to be true. We summarize these common features in Fig. 3. Alternatively, if the mammalian lateral posterior nucleus is homologous to the sauropsidian nucleus rotundus, then a number of anatomical (and embryological) characters remain to be explained. Acknowledgements Authors wish to thank J. Suárez and E. Matas for their technical assistance. This work was supported by BFI C References [1] L.L. Bruce, T.J. 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