A Genome-wide Screen Identifies PAPP-AA-Mediated IGFR Signaling as a Novel Regulator of Habituation Learning

Wolman, Marc A.; Jain, Roshan A.; Marsden, Kurt C.; Bell, Hannah; Skinner, Julianne; Hayer, Katharina E.; Hogenesch, John B.; Granato, Michael

doi:10.1016/j.neuron.2015.02.025

Cited by 87 publications

(113 citation statements)

References 102 publications

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“…In fact, we found that differences in the rate of habituation between individuals are maintained over days and are heritable, indicating that ASR habituation has a genetic or epigenetic component. The genetic implications are consistent with recent findings from a forward genetic screen in larval zebrafish, which identified several mutants that affect ASR habituation without affecting startle performance (Wolman et al, 2015). Two of these genes were identified: one encoding the metabolic enzyme pyruvate carboxylase and the other the pregnancy-associated plasma protein A, a secreted metalloprotease.…”

Section: Discussionsupporting

confidence: 88%

Neuromodulatory Regulation of Behavioral Individuality in Zebrafish

Pantoja

Hoagland

Carroll

et al. 2016

Neuron

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Summary Inter-individual behavioral variation is thought to increase fitness and aid adaptation to environmental change, but the underlying mechanisms are poorly understood. We find that variation between individuals in neuromodulatory input contributes to individuality in short-term habituation of the zebrafish (Danio Rerio) acoustic startle response (ASR). ASR habituation varies greatly between individuals, but differences are stable over days and are heritable. Acoustic stimuli that activate ASR-command Mauthner cells also activate dorsal raphe nucleus (DRN) serotonergic neurons, which project to the vicinity of the Mauthner cells and their inputs. DRN neuron activity decreases during habituation in proportion to habituation and a genetic manipulation that reduces serotonin content in DRN neurons increases habituation, whereas serotonergic agonism or DRN activation with ChR2 reduces habituation. Finally, level of rundown of DRN activity co-segregates with extent of behavioral habituation across generations. Thus, variation between individuals in neuromodulatory input contributes to individuality in a core adaptive behavior.

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Section: Discussionsupporting

confidence: 88%

Neuromodulatory Regulation of Behavioral Individuality in Zebrafish

Pantoja

Hoagland

Carroll

et al. 2016

Neuron

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“…Overall, these data suggest increased habituation or non-associative learning in AB over TL larvae. A recent study in zebrafish larvae showed that IGF1 increases acoustic startle habituation through activation of the IGF1 receptor thereby regulating synaptic strength [40], in line with the proposed role of IGF1 in neuronal plasticity [29]. Hence, we hypothesise here that the difference in habituation between AB and TL may be related to higher levels of expression of igf1 , that we observed in AB compared to TL larvae.…”

Section: Discussionsupporting

confidence: 80%

Further characterisation of differences between TL and AB zebrafish (Danio rerio): Gene expression, physiology and behaviour at day 5 of the larval stage

et al. 2017

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Zebrafish (Danio rerio) have become popular as model organism in research. Many strains are readily available, which not only differ morphologically, but also genetically, physiologically and behaviourally. Here, we focus on the AB and Tupfel long-fin (TL) strain for which we have previously shown that adults differ in baseline hypothalamus-pituitary-interrenal (HPI)-axis activity (AB higher than TL) affecting inhibitory avoidance behaviour (absent in AB). To assess whether strain differences are already present in early life stages, we compared baseline HPI-axis related gene expression as well as cortisol levels, (neuro)development related as well as (innate) immune system related gene expression, and light-dark as well as startle behaviour in larvae 5 days post fertilisation. The data show that AB and TL larvae differ in baseline HPI-axis activity (AB higher than TL), expression of (neuro)development and immune system related genes (AB higher than TL), habituation to acoustic/vibrational stimuli (AB habituate faster than TL) and light-dark induced changes in motor behaviour (AB stronger than TL). Our data show that already in larval stages differences exist between zebrafish of the AB and TL strain confirming and extending data of earlier studies. To what extent the mutation in connexin 41.8, leading to spots rather than stripes in TL, but also (possibly) affecting eye, heart and brain function, is involved in the expression of (some of) these differences needs to be studied. These results emphasise that differences between strains need to be taken into account to enhance reproducibility both within, and between, laboratories.

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“…More recently, a forward genetic screen provided interesting insights into habituation learning [66]. However, such an approach for the study of sleep presents several challenges.…”

Section: New Approaches and Genetic Pathwaysmentioning

confidence: 99%

Attacking sleep from a new angle: contributions from zebrafish

Oikonomou

Prober

2017

Current Opinion in Neurobiology

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Sleep consumes a third of our lifespan, but we are far from understanding how it is initiated, maintained and terminated, or what purposes it serves. To address these questions, alternative model systems have recently been recruited. The diurnal zebrafish holds the promise of bridging the gap between simple invertebrate systems, which show little neuroanatomical conservation with mammals, and well-established, but complex and nocturnal, murine systems. Zebrafish larvae can be monitored in a high-throughput fashion, pharmacologically tested by adding compounds into the water, genetically screened using transient transgenesis, and optogenetically manipulated in a non-invasive manner. Here we discuss work that has established the zebrafish as a powerful system for the study of sleep, as well as novel insights gained by exploiting its particular advantages.

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A Genome-wide Screen Identifies PAPP-AA-Mediated IGFR Signaling as a Novel Regulator of Habituation Learning

Cited by 87 publications

References 102 publications

Neuromodulatory Regulation of Behavioral Individuality in Zebrafish

Neuromodulatory Regulation of Behavioral Individuality in Zebrafish

Further characterisation of differences between TL and AB zebrafish (Danio rerio): Gene expression, physiology and behaviour at day 5 of the larval stage

Attacking sleep from a new angle: contributions from zebrafish

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