Jan-Marek Weislogel

Heidelberg University

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Hilmar Bading

Heidelberg University

Adam Claridge‐Chang

Duke-NUS Medical School

Tugce Yildizoglu

Max Planck Institute of Neurobiology

Pryseley Nkouibert Assam

Singapore Clinical Research Institute

Farhan Mohammad

Hamad bin Khalifa University

Mazahir T. Hasan

Max Planck Institute for Medical Research

Rico Tabor

Max Planck Institute for Medical Research

Stéphanie Goyon

Institut des Neurosciences Cellulaires et Intégratives

Ursula Weiß

Florida State University

Emre Yaksi

Norwegian University of Science and Technology

Cooperative Institutions

Heidelberg University

Max Planck Institute for Medical Research

German Cancer Research Center

Max Planck Society

Institut des Neurosciences Cellulaires et Intégratives

Université de Strasbourg

University Hospital Heidelberg

Centre National de la Recherche Scientifique

Central Institute of Mental Health

Duke-NUS Medical School

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Estimating information flow through a memory system: the utility of meta-analytic methods for genetics

bioRxiv (Cold Spring Harbor Laboratory) (2015)

Tugce Yildizoglu Jan-Marek Weislogel Farhan Mohammad Edwin SY Chan Pryseley Nkouibert Assam

ABSTRACT Critics of significance testing claim that this statistical framework promotes discrepancies by using arbitrary thresholds (α) to impose reject/accept dichotomies on continuous data, which is not reflective of the biological reality of quantitative phenotypes. Here we explore this idea and evaluate an alternative approach, demonstrating the potential for meta-analysis and related estimation methods to resolve discordance generated by the use of traditional significance tests. We selected a set of behavioral studies proposing differing models of the physiological basis of Drosophila olfactory memory and used systematic review and meta-analysis approaches to define the true role of lobular specialization within the brain. The mainstream view is that each of the three lobes of the Drosophila mushroom body play specialized roles in short-term aversive olfactory memory [1-5], but a number of studies have made divergent conclusions based on their discordant experimental findings [6-8]. Multivariate meta-regression models revealed that short-term memory lobular specialization is not in fact supported by the data, and identified the cellular extent of a transgenic driver as the major predictor of its effect on short-term memory. Our findings demonstrate that meta-analysis, meta-regression, hierarchical models and estimation methods in general can be successfully harnessed to identify knowledge gaps, synthesize divergent results, accommodate heterogeneous experimental design and quantify genetic mechanisms.

Information flow

10.1101/020586

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Requirement for Nuclear Calcium Signaling in Drosophila Long-Term Memory

Science Signaling (2013)

Jan-Marek Weislogel C. Peter Bengtson Michaela Müller Jan Niklas Hörtzsch Martina Bujard

Blocking nuclear calcium signaling reversibly inhibits long-term memory formation in flies.

Calcium Signaling

10.1126/scisignal.2003598

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Estimating Information Processing in a Memory System: The Utility of Meta-analytic Methods for Genetics

PLoS Genetics (2015)

Tugce Yildizoglu Jan-Marek Weislogel Farhan Mohammad Edwin Chan Pryseley Nkouibert Assam

Genetic studies in Drosophila reveal that olfactory memory relies on a brain structure called the mushroom body. The mainstream view is that each of the three lobes of the mushroom body play specialized roles in short-term aversive olfactory memory, but a number of studies have made divergent conclusions based on their varying experimental findings. Like many fields, neurogenetics uses null hypothesis significance testing for data analysis. Critics of significance testing claim that this method promotes discrepancies by using arbitrary thresholds (α) to apply reject/accept dichotomies to continuous data, which is not reflective of the biological reality of quantitative phenotypes. We explored using estimation statistics, an alternative data analysis framework, to examine published fly short-term memory data. Systematic review was used to identify behavioral experiments examining the physiological basis of olfactory memory and meta-analytic approaches were applied to assess the role of lobular specialization. Multivariate meta-regression models revealed that short-term memory lobular specialization is not supported by the data; it identified the cellular extent of a transgenic driver as the major predictor of its effect on short-term memory. These findings demonstrate that effect sizes, meta-analysis, meta-regression, hierarchical models and estimation methods in general can be successfully harnessed to identify knowledge gaps, synthesize divergent results, accommodate heterogeneous experimental design and quantify genetic mechanisms.

Mushroom bodies

10.1371/journal.pgen.1005718

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Citations (19)

A Fear Memory Engram and Its Plasticity in the Hypothalamic Oxytocin System

Neuron (2019)

Mazahir T. Hasan Ferdinand Althammer Miriam Silva da Gouveia Stéphanie Goyon Marina Eliava

Extinction (optical mineralogy)

Freezing behavior

Oxytocin receptor

Engram

10.1016/j.neuron.2019.04.029

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Nuclear Calcium Signaling Controls Methyl-CpG-binding Protein 2 (MeCP2) Phosphorylation on Serine 421 following Synaptic Activity

Journal of Biological Chemistry (2012)

Bettina Buchthal David T. W. Lau Ursula Weiß Jan-Marek Weislogel Hilmar Bading

The function of MeCP2, a methylated DNA-interacting protein that may act as a global chromatin modifier, is controlled by its phosphorylation on serine 421. Here we show that in hippocampal neurons, nuclear calcium signaling controls synaptic activity-induced phosphorylation of MeCP2 on serine 421. Pharmacological inhibition of calcium/calmodulin-dependent protein (CaM)kinases blocked activity-induced MeCP2 serine 421 phosphorylation. CaM kinase II (CaMKII) but not CaMKIV, the major nuclear CaM kinase in hippocampal neurons, appeared to mediate this phosphorylation event. Biochemical subcellular fractionations and immunolocalization studies revealed that several isoforms of CaMKII (i.e. CaMKIIα, -β, -γ, and -δ) are expressed in the cytosol but are also detectable in the cell nucleus of hippocampal neurons, suggesting that nuclear CaMKII catalyzes MeCP2 serine 421 phosphorylation. Thus, in addition to the classical nuclear calcium-CaMKIV-CREB/CBP (cAMP-response element-binding protein/CREB-binding protein) pathway that regulates transcription of specific target genes, nuclear calcium may also modulate genome-wide the chromatin state in response to synaptic activity via nuclear CaMKII-MeCP2 signaling.

10.1074/jbc.m112.382507

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Citations (50)

Visualisation of nuclear calcium signals using rekombinant calcium indicators in in vivo systems

Jan-Marek Weislogel

The generation of calcium signals following synaptic activity is a fundamental property of neurons that controls many neuronal processes including cell survival, learning and memory. In cultured neurons, increases in nuclear calcium concentrations are known to be critical for the activation of gene expression mediated by the transcription factor CREB. CREB has been implicated in transcription-dependent plasticity (late phase LTP). It is still unclear whether nuclear calcium signals are also responsible for CREB mediated gene transcription in vivo. The goal of the study was to visualise nuclear calcium signals in vivo. Investigating the importance of nuclear Ca2+ signalling in the intact brain is impeded by the restrictions and complexities of in vivo experimentation. However, D. melanogaster provides an excellent system to explore the role nuclear Ca2+ in an intact behaving animal. Since Ca2+ signalling of the nucleus is of particular interest transgenic flies expressing the nuclear localised Ca2+ indicator UAS GCaMP NLS to visualise nuclear Ca2+ signals and the nuclear Ca2+/CaM inhibitor UAS 2xM13 myc to interfere with nuclear Ca2+ signalling were generated. Using these flies, it could be shown that nuclear Ca2+ signalling could play a role in LTM. Further, using rAAV-mediated gene transfer the nuclear Ca2+ indicator rAAV GCaMP 2.0 NLS was expressed in CA1 pyramidal neurons of juvenile rats two weeks after in vivo injection. In acute slices from these juvenile rats an increase in nuclear Ca2+ concentration was visualised evoked by LTP inducing electrical stimulation. Using this method a correlation between LTP and increase in nuclear Ca2+ concentration could be shown. It is still unclear whether nuclear Ca2+ signals are necessary to induce LTP in acute slice. The major challenge of Ca2+ imaging in vivo either in flies or in rodents based on difficulties to detect signals through the intransparent skulls. The freshwater polyp H. vulgaris is completely transparent. Therefore, Ca2+ imaging of transgenic hydras expressing the Ca2+-indicators hyGCaMP or hyGCaMP NLS was done. Increase in nuclear Ca2+ signals was observed in ectodermal cells expressing hyGCaMP NLS. At the moment, the role of Ca2+ signals, especially of nuclear Ca2+ signals in hydra is unknown.

Calcium Signaling

10.11588/heidok.00008603

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Processing of Odor Mixtures in the Zebrafish Olfactory Bulb

Journal of Neuroscience (2004)

Rico Tabor Emre Yaksi Jan-Marek Weislogel Rainer W. Friedrich

Components of odor mixtures often are not perceived individually, suggesting that neural representations of mixtures are not simple combinations of the representations of the components. We studied odor responses to binary mixtures of amino acids and food extracts at different processing stages in the olfactory bulb (OB) of zebrafish. Odor-evoked input to the OB was measured by imaging Ca 2+ signals in afferents to olfactory glomeruli. Activity patterns evoked by mixtures were predictable within narrow limits from the component patterns, indicating that mixture interactions in the peripheral olfactory system are weak. OB output neurons, the mitral cells (MCs), were recorded extra- and intracellularly and responded to odors with stimulus-dependent temporal firing rate modulations. Responses to mixtures of amino acids often were dominated by one of the component responses. Responses to mixtures of food extracts, in contrast, were more distinct from both component responses. These results show that mixture interactions can result from processing in the OB. Moreover, our data indicate that mixture interactions in the OB become more pronounced with increasing overlap of input activity patterns evoked by the components. Emerging from these results are rules of mixture interactions that may explain behavioral data and provide a basis for understanding the processing of natural odor stimuli in the OB.

Stimulus (psychology)

10.1523/jneurosci.1834-04.2004

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Citations (141)