Distributed Plasticity Drives Visual Habituation Learning in Larval Zebrafish

Randlett, Owen; Haesemeyer, Martin; Forkin, Greg; Shoenhard, Hannah; Schier, Alexander F.; Engert, Florian; Granato, Michael

doi:10.1016/j.cub.2019.02.039

Cited by 84 publications

(125 citation statements)

References 33 publications

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“…Series of recent studies highlight the increasing popularity of zebrafish for studying diverse aspects of animal behavior [30][31][32][33][34][35][36][37][38][39], including the more complex behaviors such as learning [25,26,[40][41][42][43][44][45][46] and social behaviors [47,48]. While studying complex behaviors in adult zebrafish allow investigation of brain function in a fully mature brain, larval and juvenile zebrafish has the tremendous advantage of a small and transparent brain, when it comes to studying brain A B C1 T1 C2 T2 T3 C3 T4 C4 T5 T6 control dHb activity [33,38,[49][50][51][52][53][54][55][56][57][58]. Hence, we investigated the ontogeny of a complex operant behavior, namely CPA learning, and showed that the learning performance of young zebrafish improves across development.…”

Section: Discussionmentioning

confidence: 99%

The zebrafish dorsolateral habenula is required for updating learned behaviors

Palumbo

Serneels

Pelgrims

et al. 2019

Preprint

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Operant conditioning requires multiple cognitive processes, such as learning, consolidation, prediction of potential outcomes and decision making. It is less clear how interactions of these processes led to behavioral adaptations that allows animal to cope with changing environment. We first showed that juvenile zebrafish can perform conditioned place avoidance learning, with improving performance across development. Next, we disentangled operant conditioning from contextual fear and anxiety. Our results revealed that animals' decisions and learning performance is shaped by the available information and animals' experience. Ablation of dorsal habenula (dHb), a brain region involved in learning and prediction of outcomes, led to an unexpected improvement in animals learning performance and delayed memory extinction. Interestingly, while the control animals' exhibit rapid adaptation to changing learning rules, dHb ablated animals failed to adapt. Altogether, our results showed that dHb plays a central role in switching animals' strategies while integrating new evidences with prior experience. Eggen, M. Andresen, V. Nguyen, A Nygard and our fish facility support team for technical assistance. We thank Nathalie Jurisch-Yaksi and Stephanie Fore for helpful comments on the text. We thank all Yaksi lab members for stimulating discussions. This work was funded by ERC starting grant 335561 (F.P., R.P., E.Y.) and RCN FRIPRO Research Grant 239973 (E.Y.). Work in the E.Y. lab is funded by the Kavli Institute for Systems Neuroscience at NTNU. AUTHOR CONTRIBUTIONSConceptualization, F.P., E.Y.; Methodology and data, F.P., B.S.; Recording software F.P., R.P.; Data

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Section: Discussionmentioning

confidence: 99%

The zebrafish dorsolateral habenula is required for updating learned behaviors

Palumbo

Serneels

Pelgrims

et al. 2019

Preprint

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“…Our observations that flies initially reacted to vibration with vigorous locomotion and that they can be awakened with salient changes in the visual environment also confirm that VIS is unrelated to other types of suppressed locomotion such as that induced by wind or fear in flies (Gibson et al, 2015;Yorozu et al, 2009) or tonic immobility in birds (Gallup, 1977). The habituation model of how sensory stimulation promotes sleep proposes that habituation to repetitive, unimportant stimuli leads to reduced arousal (Pavlov, 1927;Sokolov, 1963;Bohlin, 1971 (Flavell et al, 2013;McDiarmid et al, 2019;Randlett et al, 2019). These findings led to a recent proposal that habituation is more than simply learning to ignore and that it allows organisms to switch between alternative behaviors depending on the Hz stimulation may promote sleep in part through the synchronization mechanism.…”

Section: Discussionmentioning

confidence: 92%

Sleep Induction by Mechanosensory Stimulation inDrosophila

Öztürk-Çolak

McClanahan

Buchler

et al. 2020

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2 Summary People tend to fall asleep when gently rocked or vibrated. Experimental studies have shown rocking promotes sleep in humans and mice. The prevailing "synchronization" model proposes synchronization of brain activity to mechanosensory stimuli mediates the phenomenon. The alternative "habituation" model proposes habituation, a form of non-associative learning, mediates sleep induction by monotonous stimulation. Here we show that gentle vibration promotes sleep in Drosophila in part through habituation. Vibration-induced sleep (VIS) leads to the accrual of homeostatic sleep credit, is associated with reduced arousability, and can be suppressed by heightened arousal. Sleep induction improves over successive blocks of vibration and exhibits stimulus specificity, supporting the habituation model. Multiple mechanosensory organs mediate VIS, and the magnitude of sleep gain depends on the vibration frequency and genetic background. Our findings suggest habituation is a major contributor to VIS, but synchronization of brain activity may play a role under certain stimulus conditions.

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“…For example, we quantified multiple features of habituation as we have previously shown that they habituate to different extents and with different time courses (Figure 1F-I) and because there is growing evidence that different components of a single habituating response are mediated by different molecular mechanisms. 61,79,80 Systematic quantification of the pairwise correlation between all possible phenotypic feature pairs revealed expected moderate correlations (e.g. between length and width) and clustering that reflected the feature categories we predefined ( Figure 1K).…”

Section: Asd-associated Genes Are Highly Conserved To C Elegansmentioning

confidence: 89%

Systematic phenomics analysis of ASD-associated genes reveals shared functions and parallel networks underlying reversible impairments in habituation learning

McDiarmid

Belmadani

Liang

et al. 2019

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A major challenge facing the genetics of Autism Spectrum Disorders (ASD) is the large and growing number of candidate risk genes and gene variants of unknown functional significance.Here, we used Caenorhabditis elegans to systematically functionally characterize ASDassociated genes in vivo. Using our custom machine vision system we quantified 26 phenotypes spanning morphology, locomotion, tactile sensitivity, and habituation learning in 87 strains each carrying a mutation in an ortholog of an ASD-associated gene. We identified hundreds of novel genotype-phenotype relationships ranging from severe developmental delays and uncoordinated movement to subtle deficits in sensory and learning behaviors. We clustered genes by similarity in phenomic profiles and used epistasis analysis to discover parallel networks centered on CHD8•chd-7 and NLGN3•nlg-1 that underlie mechanosensory hyper-responsivity and impaired habituation learning. We then leveraged our data for in vivo functional assays to gauge missense variant effect. Expression of wild-type NLG-1 in nlg-1 mutant C. elegans rescued their sensory and learning impairments. Testing the rescuing ability of all conserved ASD-associated neuroligin variants revealed varied partial loss-of-function despite proper subcellular localization. Finally, we used CRISPR-Cas9 auxin inducible degradation to determine that phenotypic abnormalities caused by developmental loss of NLG-1 can be reversed by adult expression. This work charts the phenotypic landscape of ASDassociated genes, offers novel in vivo variant functional assays, and potential therapeutic targets for ASD.

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Distributed Plasticity Drives Visual Habituation Learning in Larval Zebrafish

Cited by 84 publications

References 33 publications

The zebrafish dorsolateral habenula is required for updating learned behaviors

The zebrafish dorsolateral habenula is required for updating learned behaviors

Sleep Induction by Mechanosensory Stimulation inDrosophila

Systematic phenomics analysis of ASD-associated genes reveals shared functions and parallel networks underlying reversible impairments in habituation learning

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