Asymmetric innervation of the habenula in zebrafish

Department of Biological Sciences, National University of Singapore, Tumasik, 00, Singapore
The Journal of Comparative Neurology (Impact Factor: 3.23). 06/2007; 502(4):611-9. DOI: 10.1002/cne.21339
Source: PubMed
The habenular complex is a paired structure found in the diencephalon of all vertebrates, linking the forebrain and midbrain. Habenulae are asymmetrical and may contribute to lateralized behavior. Recent studies in zebrafish have characterized molecular pathways that give rise to the habenular asymmetry and the distinct projections of the left and right habenula to the midbrain. However, it is unclear whether there are asymmetries in habenula afferents from the forebrain. By lipophilic dye tracing, we find that axons innervating the habenula derive primarily from a region in the lateral diencephalon containing migrated neurons of the eminentia thalami (EmT). EmT neurons terminate in neuropils in both ipsilateral and contralateral habenula. These axons, together with axons from migrated neurons of the posterior tuberculum and pallial neurons, cross the midline via the habenular commissure. Subsets of pallial neurons terminate only in the medial right habenula, regardless of which side of the brain they originate from. These include an unusual type of forebrain projection: axons that cross the midline twice, at both the anterior and habenular commissures. Our data establish that there is asymmetric innervation of the habenula from the telencephalon, suggesting a mechanism by which habenula asymmetry might contribute to lateralized behavior.

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    • "Despite this caveat, results in other species seem to support this connection, as potentially homologous nuclei were described in the dorsal thalamus of a shark (Giuliani et al., 2002) and a lizard (Díaz and Puelles, 1992). A further habenulopetal population was observed in the posterior tuberculum/posterior hypothalamic lobe of zebrafish (Hendricks and Jesuthasan, 2007; present results), which is similar to that reported in trout (Yáñez and Anadón, 1996). Histaminergic neurons have been observed in this region of the zebrafish posterior tuberculum/posterior hypothalamic lobe, and conspicuous histaminergic fibers innervate the ventral region of the zebrafish habenula (Kaslin and Panula, 2001). "
    [Show abstract] [Hide abstract] ABSTRACT: The habenulae are bilateral nuclei located in the dorsal diencephalon that are conserved across vertebrates. Here we describe the main afferents to the habenulae in larval and adult zebrafish. We observe afferents from the subpallium, nucleus rostrolateralis, posterior tuberculum, posterior hypothalamic lobe, median raphe; we also see asymmetric afferents from olfactory bulb to the right habenula, and from the parapineal to the left habenula. In addition, we find afferents from a ventrolateral telencephalic nucleus that neurochemical and hodological data identify as the ventral entopeduncular nucleus (vENT), confirming and extending observations of Amo et al. (2014). Fate map and marker studies suggest that vENT originates from the diencephalic prethalamic eminence and extends into the lateral telencephalon from 48 to 120 hour post-fertilization (hpf). No afferents to the habenula were observed from the dorsal entopeduncular nucleus (dENT). Consequently, we confirm that the vENT (and not the dENT) should be considered as the entopeduncular nucleus “proper” in zebrafish. Furthermore, comparison with data in other vertebrates suggests that the vENT is a conserved basal ganglia nucleus, being homologous to the entopeduncular nucleus of mammals (internal segment of the globus pallidus of primates) by both embryonic origin and projections, as previously suggested by Amo et al. (2014).
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    • "These results suggest that the visual pathway may directly modulate the output of the habenula during these behaviors. We are not yet able to resolve the complete neural circuit from RGC to habenula, but the likely intermediate area is the EmT, the main source of input to the habenula in zebrafish (Hendricks and Jesuthasan, 2007 ). EmT labeling in our samples was frequently observed. "
    Full-text · Dataset · Jul 2015
    • "Repeating a similar approach for olfactory target structures in the telencephalon (Yaksi et al., 2009), they showed differences in coding between subpallial and pallial regions, with the former showing broad odor tuning, and the latter containing cells that responded more specifically to particular odor combinations. The habenula, a key relay station between the forebrain and neuromodulator systems, has received considerable attention in the zebrafish, due to its pronounced asymmetries in morphology, gene expression, innervation, axonal projections and functional responses (Concha et al., 2000; Hendricks and Jesuthasan, 2007; Kuan et al., 2007; Bianco et al., 2008; Miyasaka et al., 2009; deCarvalho et al., 2014; Dreosti et al., 2014), as well as its apparent central role in determining behavioral choices (Agetsuma et al., 2010; Lee et al., 2010). Krishnan et al. developed a simple, wide-field epifluorescence system for rapid three-dimensional imaging using fast focusing and deconvolution, and applied this method to reveal, with single-cell resolution, the dynamics in response to different concentrations of multiple odors throughout the whole habenula (Krishnan et al., 2014 ). "
    [Show abstract] [Hide abstract] ABSTRACT: In recent years, the zebrafish has emerged as an appealing model system to tackle questions relating to the neural circuit basis of behavior. This can be attributed not just to the growing use of genetically tractable model organisms, but also in large part to the rapid advances in optical techniques for neuroscience, which are ideally suited for application to the small, transparent brain of the larval fish. Many characteristic features of vertebrate brains, from gross anatomy down to particular circuit motifs and cell-types, as well as conserved behaviors, can be found in zebrafish even just a few days post fertilization, and, at this early stage, the physical size of the brain makes it possible to analyze neural activity in a comprehensive fashion. In a recent study, we used a systematic and unbiased imaging method to record the pattern of activity dynamics throughout the whole brain of larval zebrafish during a simple visual behavior, the optokinetic response (OKR). This approach revealed the broadly distributed network of neurons that were active during the behavior and provided insights into the fine-scale functional architecture in the brain, inter-individual variability, and the spatial distribution of behaviorally relevant signals. Combined with mapping anatomical and functional connectivity, targeted electrophysiological recordings, and genetic labeling of specific populations, this comprehensive approach in zebrafish provides an unparalleled opportunity to study complete circuits in a behaving vertebrate animal. Copyright © 2014. Published by Elsevier Ltd.
    No preview · Article · Nov 2014 · Neuroscience
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