Ongoing habenular activity is driven by forebrain networks and modulated by olfactory stimuli

Bartoszek, Ewelina; Ostenrath, Anna Maria; Jetti, Suresh Kumar; Serneels, Bram; Mutlu, Aytac Kadir; Chau, Khac Thanh Phong; Yaksi, Emre

doi:10.1016/j.cub.2021.08.021

Cited by 24 publications

(28 citation statements)

References 110 publications

(312 reference statements)

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“…Our results indicate differentiation of neurons in the olfactory bulb first, while areas of the pallium and subpallium show considerable expansion after 5dpf suggesting late maturation of these regions. This is in agreement with behavioural studies, which have shown that complex behaviours appear from 2 to 6 weeks post-fertilization (Valente et al, 2012; Aoki et al, 2013; Cheng et al, 2014; Dreosti et al, 2015; Lal et al, 2018; Stednitz et al, 2018; Tunbak et al, 2020; Bartoszek et al, 2021). As a consequence, most functional studies likely involving the role of the telencephalon, such as fear conditioning, social interaction, learning and memory, performed on older zebrafish.…”

Section: Discussionsupporting

confidence: 92%

A structural atlas of the developing zebrafish telencephalon based on spatially-restricted transgene expression

Turner

Hawkins

Henriques

et al. 2022

Preprint

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Zebrafish telencephalon acquires an everted morphology by a two-step process that occurs from 1 to 5 days post-fertilization (dpf). Little is known about how this process affects the positioning of discrete telencephalic cell populations, hindering our understanding of how eversion impacts telencephalic structural organisation. In this study, we characterise the neurochemistry, cycle state and morphology of an EGFP positive (+) cell population in the telencephalon of Et(gata2:EGFP)bi105 transgenic fish during eversion and up to 20dpf. We map the transgene insertion to the early-growth-response-gene-3 (egr3) locus and show that EGFP expression recapitulates endogenous egr3 expression throughout much of the pallial telencephalon. Using the gata2:EGFPbi105 transgene, in combination with other well-characterised transgenes and structural markers, we track the development of various cell populations in the zebrafish telencephalon as it undergoes the morphological changes underlying eversion. These datasets were registered to reference brains to form an atlas of telencephalic development at key stages of the eversion process (1dpf, 2dpf and 5dpf) and compared to expression in adulthood. Finally, we registered gata2:EGFPbi105 expression to the Zebrafish Brain Browser 6dpf reference brain (ZBB, see Marquart et al., 2015, 2017; Tabor et al. 2019), to allow comparison of this expression pattern with anatomical data already in ZBB.

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Section: Discussionsupporting

confidence: 92%

A structural atlas of the developing zebrafish telencephalon based on spatially-restricted transgene expression

Turner

Hawkins

Henriques

et al. 2022

Preprint

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“…Although the selective origin from or terminal projection sites within the habenula nuclei remains uncharacterized in fish, neural tracer studies in fish have revealed afferent connectivity of the habenula with some nodes of the fish SDMN such as the Vv (the teleostean homolog of the LS), Vd (the homolog of mammalian striatum), and POA ( Villani et al, 1996 ; Yañez and Anadón, 1996 ; Turner et al, 2016 ; Figure 1B ). A recent functional study demonstrated that microstimulation of the Dl and Dm (the homolog of mammalian hippocampus and BLA) elicit significant activation in the habenula neurons in juvenile zebrafish ( Bartoszek et al, 2021 ). Further, ongoing neural activities in the dHb are significantly correlated with the neural activities in the Dm and olfactory bulb, while vHb activity correlates more with the activity in the Dl rather than those in the Dm ( Bartoszek et al, 2021 ).…”

Section: Possible Connection Between the Habenula And The Social Deci...mentioning

confidence: 99%

“…A recent functional study demonstrated that microstimulation of the Dl and Dm (the homolog of mammalian hippocampus and BLA) elicit significant activation in the habenula neurons in juvenile zebrafish ( Bartoszek et al, 2021 ). Further, ongoing neural activities in the dHb are significantly correlated with the neural activities in the Dm and olfactory bulb, while vHb activity correlates more with the activity in the Dl rather than those in the Dm ( Bartoszek et al, 2021 ). Although no direct anatomical projections from the Dl or the Dm have been identified to innervate the habenula in fish, the primary afferents of the vHb originates from the ventral entopeduncular nucleus (vENT = teleostean basal ganglia) in zebrafish ( Amo et al, 2014 ; Turner et al, 2016 ).…”

Section: Possible Connection Between the Habenula And The Social Deci...mentioning

confidence: 99%

Role of Habenula in Social and Reproductive Behaviors in Fish: Comparison With Mammals

Ogawa

Parhar

2022

Front. Behav. Neurosci.

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Social behaviors such as mating, parenting, fighting, and avoiding are essential functions as a communication tool in social animals, and are critical for the survival of individuals and species. Social behaviors are controlled by a complex circuitry that comprises several key social brain regions, which is called the social behavior network (SBN). The SBN further integrates social information with external and internal factors to select appropriate behavioral responses to social circumstances, called social decision-making. The social decision-making network (SDMN) and SBN are structurally, neurochemically and functionally conserved in vertebrates. The social decision-making process is also closely influenced by emotional assessment. The habenula has recently been recognized as a crucial center for emotion-associated adaptation behaviors. Here we review the potential role of the habenula in social function with a special emphasis on fish studies. Further, based on evolutional, molecular, morphological, and behavioral perspectives, we discuss the crucial role of the habenula in the vertebrate SDMN.

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“…However, a study on zebrafish could not find similar connectivity (Yáñez et al, 2017 ). In juvenile and adult zebrafish, calcium imaging studies show that Dm is activated in response to odors (Diaz-Verdugo et al, 2019 ; Bartoszek et al, 2021 ). Thus, the teleost Dm receives sensory input similar to the mammalian BLA.…”

Section: Conserved Neural Connectivity Between Zebrafish and Mammalia...mentioning

confidence: 99%

Integrated Behavioral, Genetic and Brain Circuit Visualization Methods to Unravel Functional Anatomy of Zebrafish Amygdala

Lal

Kawakami

2022

Front. Neuroanat.

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The mammalian amygdala is a complex forebrain structure consisting of a heterogeneous group of nuclei derived from the pallial and subpallial telencephalon. It plays a critical role in a broad range of behaviors such as emotion, cognition, and social behavior; within the amygdala each nucleus has a distinct role in these behavioral processes. Topological, hodological, molecular, and functional studies suggest the presence of an amygdala-like structure in the zebrafish brain. It has been suggested that the pallial amygdala homolog corresponds to the medial zone of the dorsal telencephalon (Dm) and the subpallial amygdala homolog corresponds to the nuclei in the ventral telencephalon located close to and topographically basal to Dm. However, these brain regions are broad and understanding the functional anatomy of the zebrafish amygdala requires investigating the role of specific populations of neurons in brain function and behavior. In zebrafish, the highly efficient Tol2 transposon-mediated transgenesis method together with the targeted gene expression by the Gal4-UAS system has been a powerful tool in labeling, visualizing, and manipulating the function of specific cell types in the brain. The transgenic resource combined with neuronal activity imaging, optogenetics, pharmacology, and quantitative behavioral analyses enables functional analyses of neuronal circuits. Here, we review earlier studies focused on teleost amygdala anatomy and function and discuss how the transgenic resource and tools can help unravel the functional anatomy of the zebrafish amygdala.

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Ongoing habenular activity is driven by forebrain networks and modulated by olfactory stimuli

Cited by 24 publications

References 110 publications

A structural atlas of the developing zebrafish telencephalon based on spatially-restricted transgene expression

A structural atlas of the developing zebrafish telencephalon based on spatially-restricted transgene expression

Role of Habenula in Social and Reproductive Behaviors in Fish: Comparison With Mammals

Integrated Behavioral, Genetic and Brain Circuit Visualization Methods to Unravel Functional Anatomy of Zebrafish Amygdala

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