Functional properties of habenular neurons are determined by developmental stage and sequential neurogenesis

Abstract

The developing brain undergoes drastic alterations. Here, we investigated developmental changes in the habenula, a brain region that mediates behavioral flexibility during learning, social interactions, and aversive experiences. We showed that developing habenular circuits exhibit multiple alterations that lead to an increase in the structural and functional diversity of cell types, inputs, and functional modules. As the habenula develops, it sequentially transforms into a multisensory brain region that can process visual, olfactory, mechanosensory, and aversive stimuli. Moreover, we observed that the habenular neurons display spatiotemporally structured spontaneous activity that shows prominent alterations and refinement with age. These alterations in habenular activity are accompanied by sequential neurogenesis and the integration of distinct neural clusters across development. Last, we revealed that habenular neurons with distinct functional properties are born sequentially at distinct developmental time windows. Our results highlight a strong link between the functional properties of habenular neurons and their precise birthdate.

Diversity and Function of Motile Ciliated Cell Types within Ependymal Lineages of the Zebrafish Brain

“…Therefore, it is not surprising that these two structures could rely on the same ciliogenic transcriptional program. While at the larval stage the TC/ ChP comprise a flat monolayer, its posterior part (located above the habenula [85,86]) folds into a structure composed of several cavities as development progresses, with cells pointing their cilia toward the cavities. Interestingly, as the ChP folds within multiple cavities, there remains a spatial organization of mono-versus MCCs.…”

Radial glia in the zebrafish brain: Functional, structural, and physiological comparison with the mammalian glia

“…Moreover, registration of transgenic and experimental brains on standardized atlases (Kunst et al, 2019; Randlett et al, 2015; Tabor et al, 2019) enables scientists to identify neuronal populations involved in specific behaviors (Haesemeyer, Robson, Li, Schier, & Engert, 2018; Randlett et al, 2015; Wee et al, 2019) or diseases (Thyme et al, 2019) in an unbiased manner. Beside investigations at larval stages, recent studies at juvenile zebrafish (2–5 weeks) showed that this relatively transparent (Fore, Cosacak, Verdugo, Kizil, & Yaksi, 2019) development stage allows non‐invasive imaging (Jetti, Vendrell‐Llopis, & Yaksi, 2014; Vendrell‐Llopis & Yaksi, 2015) and exhibit cognitively demanding behaviors such as learning (Palumbo, Serneels, Pelgrims, & Yaksi, 2019; Valente, Huang, Portugues, & Engert, 2012; Yashina, Tejero‐Cantero, Herz, & Baier, 2019) and social interactions (Dreosti, Lopes, Kampff, & Wilson, 2015; Hinz & de Polavieja, 2017; Larsch & Baier, 2018; Tunbak, Vazquez‐Prada, Ryan, Kampff, & Dreosti, 2020). Altogether, we are certain that applying the wide range of methodologies described above to measure and interfere with astroglia activity will reveal exciting findings on the mechanisms and dynamics underlying neuro‐glia interactions in the context of complex behaviors and brain diseases.…”

Teratogenic, Oxidative Stress and Behavioural Outcomes of Three Fungicides of Natural Origin (Equisetum arvense, Mimosa tenuiflora, Thymol) on Zebrafish (Danio rerio)

“…The disruption of this structure was found to increase fear [ 79 ] and contribute to anxiety disorders [ 80 ], as observed following exposure to Thymol. The correct function and development of habenular circuits in zebrafish has a strong association with the correct embryo neurogenesis [ 81 ]. This is dependent upon complex intrinsic and extrinsic signalling factors interactions [ 82 ], with neurogenesis impairment being associated with various brain disorders.…”