Martin Heisenberg

University of Wuerzburg, Würzburg, Bavaria, Germany

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Publications (132)873.07 Total impact

  • Martin Heisenberg
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    ABSTRACT: An animal generates behavioral actions because of the effects of these actions in the future. Occasionally, the animal may generate an action in response to a certain event or situation. If the outcome of the action is adaptive, the animal may keep this stimulus-response link in its behavioral repertoire, in case the event or situation occurs again. If a responsive action is innate but the outcome happens to be less adaptive than it had been before, the link may be loosened. This adjustment of outcome expectations involves a particular kind of learning, which will be called "outcome learning." The present article discusses several examples of outcome learning in Drosophila. Learning and memory are intensely studied in flies, but the focus is on classical conditioning. Outcome learning, a particular form of operant learning, is of special significance, because it modulates outcome expectations that are operational components of action selection and intentionality. © 2015 Heisenberg; Published by Cold Spring Harbor Laboratory Press.
    Learning & memory (Cold Spring Harbor, N.Y.) 06/2015; 22(6):294-298. DOI:10.1101/lm.037481.114
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    ABSTRACT: The circadian clock enables organisms to anticipate daily environmental cycles and drives corresponding changes in behavior [1, 2]. Such endogenous oscillators also enable animals to display time-specific memory [1, 3-5]. For instance, mice and honeybees associate the location of a stimulus (like food or mate) with a certain time of day (time-place learning) [6, 7]. However, the mechanism underlying time-related learning and memory is not known. In the present study, we investigate time-specific odor learning. We use a genetically tractable animal, the fly Drosophila melanogaster. Starved flies are trained in the morning and afternoon to associate distinct odors with sucrose reward. The training is repeated the next day, and their time-dependent odor preference is tested on the third day. Our results indicate that Drosophila can express appetitive memory at the relevant time of day if the two conditioning events are separated by more than 4 hr. Flies can form time-odor associations in constant darkness (DD) as well as in a daily light-dark (LD) cycle, but not when kept under constant light (LL) conditions. Circadian clock mutants, period(01) (per(01)) and clock(AR) (clk(AR)), learned to associate sucrose reward with a certain odor but were unable to form time-odor associations. Our findings show that flies can utilize temporal information as an additional cue in appetitive learning. Time-odor learning in flies depends on a per- and clk-dependent endogenous mechanism that is independent of environmental light cues. Copyright © 2015 Elsevier Ltd. All rights reserved.
    Current biology: CB 05/2015; 25(12). DOI:10.1016/j.cub.2015.04.032
  • Narendra Solanki, Reinhard Wolf, Martin Heisenberg
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    ABSTRACT: Abstract Novelty choice, a visual paired-comparison task for the fly Drosophila melanogaster is studied with severely restrained single animals in a flight simulator. The virtual environment simulates free flight for rotation in the horizontal plane. The behavior has three functional components: visual azimuth orientation, working memory and pattern discrimination (perception). Here we study novelty choice in relation to its neural substrate in the brain and show that it requires the central complex and in particular the ring neurons of the ellipsoid body. Surprisingly, it also involves the mushroom bodies which are needed specifically in the comparison of patterns of different size.
    Journal of Neurogenetics 01/2015; 29(1):1-16. DOI:10.3109/01677063.2014.1002661
  • M Heisenberg
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    ABSTRACT: Abstract Behavior is not adequately described as a stimulus - response process. It is initiated by the animal and is generated because of its expected outcome in the future. The outcome can be good or bad for the animal. The brain is in charge of the selection process. This is the basic function of the brain. Taking Drosophila as a study case the essay discusses initiating activity, several examples of outcome expectations, trying out, the internal search for a suitable behavior, chaining of actions and the functional roles of chance in action selection. It takes mental processes and states such as goals, intentions, feelings, memories, cognition and attention as higher levels of behavioral control that have their origin in biological evolution.
    Journal of neurogenetics 04/2014; 28(3-4). DOI:10.3109/01677063.2014.912279
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    ABSTRACT: Despite the importance of the insect nervous system for functional and developmental neuroscience, descriptions of insect brains have suffered from a lack of uniform nomenclature. Ambiguous definitions of brain regions and fiber bundles have contributed to the variation of names used to describe the same structure. The lack of clearly determined neuropil boundaries has made it difficult to document precise locations of neuronal projections for connectomics study. To address such issues, a consortium of neurobiologists studying arthropod brains, the Insect Brain Name Working Group, has established the present hierarchical nomenclature system, using the brain of Drosophila melanogaster as the reference framework, while taking the brains of other taxa into careful consideration for maximum consistency and expandability. The following summarizes the consortium's nomenclature system and highlights examples of existing ambiguities and remedies for them. This nomenclature is intended to serve as a standard of reference for the study of the brain of Drosophila and other insects.
    Neuron 02/2014; 81(4):755-765. DOI:10.1016/j.neuron.2013.12.017
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    ABSTRACT: In a wide range of animals, uncontrollable stressful events can induce a condition called "learned helplessness." In mammals it is associated with low general activity, poor learning, disorders of sleep and feeding, ulcers, and reduced immune status, as well as with increased serotonin in parts of the brain. It is considered an animal model of depression in humans [1-4]. Here we investigate learned helplessness in Drosophila, showing that this behavioral state consists of a cognitive and a modulatory, possibly mood-like, component. A fly, getting heated as soon as it stops walking, reliably resumes walking to escape the heat. If, in contrast, the fly is not in control of the heat, it learns that its behavior has no effect and quits responding. In this state, the fly walks slowly and takes longer and more frequent rests, as if it were "depressed." This downregulation of walking behavior is more pronounced in females than in males. Learned helplessness in Drosophila is an example of how, in a certain situation, behavior is organized according to its expected consequences.
    Current biology: CB 04/2013; 74(9). DOI:10.1016/j.cub.2013.03.054
  • M Heisenberg
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    ABSTRACT: This essay is dedicated to Obaid on the occasion of his 80th birthday. We both worked on the behavior of Drosophila and on what underlies behavior in the fly brain. Is that the fly's mind? The essay is about some limitations of brain science. It is just a little piece of writing. It is meant to honor Obaid for his contributions to Drosophila neurogenetics in 40 years and to science in India. I hope he takes it instead of a bowl of flowers-adding to the praise.
    Journal of neurogenetics 05/2012; 26(3-4). DOI:10.3109/01677063.2012.687796
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    Satoko Yamaguchi, Martin Heisenberg
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    ABSTRACT: Visual behavior of insects has long been studied, but it is only recently that a wide variety of genetic tools has become available for its analysis. Perhaps the most basic visual behaviour is phototaxis, locomotion towards a source of light. It is known in many insects and has been studied for over a century but the neural network underlying it is little understood. We recently described in the fruit fly Drosophila how different photoreceptor types contribute to phototaxis. By blocking subsets of them we showed that at least four of the five types are involved. In this short review, we compare phototactic behaviour in fruit flies and other insects (especially honeybees), and discuss what is known about the underlying neural circuitry. :
    Fly 10/2011; 5(4). DOI:10.4161/fly.5.4.16419
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    Preeti Sareen, Reinhard Wolf, Martin Heisenberg
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    ABSTRACT: Organisms with complex visual systems rarely respond to just the sum of all visual stimuli impinging on their eyes. Often, they restrict their responses to stimuli in a temporarily selected region of the visual field (selective visual attention). Here, we investigate visual attention in the fly Drosophila during tethered flight at a torque meter. Flies can actively shift their attention; however, their attention can be guided to a certain location by external cues. Using visual cues, we can direct the attention of the fly to one or the other of the two visual half-fields. The cue can precede the test stimulus by several seconds and may also be spatially separated from the test by at least 20° and yet attract attention. This kind of external guidance of attention is found only in the lower visual field.
    Proceedings of the National Academy of Sciences 04/2011; 108(17):7230-5. DOI:10.1073/pnas.1102522108
  • Martin Heisenberg
    Journal of neurogenetics 09/2010; 24(3):93-4. DOI:10.3109/01677063.2010.499979
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    ABSTRACT: Current imaging methods such as Magnetic Resonance Imaging (MRI), Confocal microscopy, Electron Microscopy (EM) or Selective Plane Illumination Microscopy (SPIM) yield three-dimensional (3D) data sets in need of appropriate computational methods for their analysis. The reconstruction, segmentation and registration are best approached from the 3D representation of the data set. Here we present a platform-independent framework based on Java and Java 3D for accelerated rendering of biological images. Our framework is seamlessly integrated into ImageJ, a free image processing package with a vast collection of community-developed biological image analysis tools. Our framework enriches the ImageJ software libraries with methods that greatly reduce the complexity of developing image analysis tools in an interactive 3D visualization environment. In particular, we provide high-level access to volume rendering, volume editing, surface extraction, and image annotation. The ability to rely on a library that removes the low-level details enables concentrating software development efforts on the algorithm implementation parts. Our framework enables biomedical image software development to be built with 3D visualization capabilities with very little effort. We offer the source code and convenient binary packages along with extensive documentation at http://3dviewer.neurofly.de.
    BMC Bioinformatics 05/2010; 11:274. DOI:10.1186/1471-2105-11-274
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    Satoko Yamaguchi, Claude Desplan, Martin Heisenberg
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    ABSTRACT: The visual systems of most species contain photoreceptors with distinct spectral sensitivities that allow animals to distinguish lights by their spectral composition. In Drosophila, photoreceptors R1-R6 have the same spectral sensitivity throughout the eye and are responsible for motion detection. In contrast, photoreceptors R7 and R8 exhibit heterogeneity and are important for color vision. We investigated how photoreceptor types contribute to the attractiveness of light by blocking the function of certain subsets and by measuring differential phototaxis between spectrally different lights. In a "UV vs. blue" choice, flies with only R1-R6, as well as flies with only R7/R8 photoreceptors, preferred blue, suggesting a nonadditive interaction between the two major subsystems. Flies defective for UV-sensitive R7 function preferred blue, whereas flies defective for either type of R8 (blue- or green-sensitive) preferred UV. In a "blue vs. green" choice, flies defective for R8 (blue) preferred green, whereas those defective for R8 (green) preferred blue. Involvement of all photoreceptors [R1-R6, R7, R8 (blue), R8 (green)] distinguishes phototaxis from motion detection that is mediated exclusively by R1-R6.
    Proceedings of the National Academy of Sciences 03/2010; 107(12):5634-9. DOI:10.1073/pnas.0809398107
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    ABSTRACT: Most insertional mutagenesis screens of Drosophila performed to date have not used target chromosomes that have been checked for their suitability for phenotypic screens for viable phenotypes. To address this, we have generated a selection of stocks carrying either isogenized second chromosomes or isogenized third chromosomes, in a genetic background derived from a Canton-S wild-type strain. We have tested these stocks for a range of behavioral and other viable phenotypes. As expected, most lines are statistically indistinguishable from Canton-S in most phenotypes tested. The lines generated are now being used as target chromosomes in mutagenesis screens, and the characterization reported here will facilitate their use in screens of these lines for behavioral and other viable phenotypes.
    Journal of Neurogenetics 07/2009; 19(2):57-85. DOI:10.1080/01677060591007155
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    ABSTRACT: Two Drosophila mutants are described in which the connections between the input to and the output from the mushroom bodies is largely interrupted. In all forms of the flies (larva, imago, male, female) showing the structural defect, olfactory conditioning is impaired. Learning is completely abolished when electroshock is used as reinforcement and partially suppressed in reward learning with sucrose. No influence of the mushroom body defect on the perception of the conditioning stimuli or on spontaneous olfactory behavior is observed. The defect seems not to impair learning of color discrimination tasks or operant learning involving visual cues.
    Journal of Neurogenetics 07/2009; 2(1):1-30. DOI:10.3109/01677068509100140
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    ABSTRACT: Mutations in Ribosomal s6 kinase 2 (Rsk2) are associated with severe neuronal dysfunction in Coffin-Lowry syndrome (CLS) patients, flies and mice. So far, the mechanisms of how Rsk2 regulates development, maintenance and activity of neurons are not understood. We have investigated the consequences of Rsk2 deficiency in mouse spinal motoneurons. Survival of isolated Rsk2 deficient motoneurons is not reduced, but these cells grow significantly longer neurites. Conversely, overexpression of a constitutively active form of Rsk2 leads to reduced axon growth. Increased axon growth in Rsk2 deficient neurons was accompanied by higher Erk 1/2 phosphorylation, and the knockout phenotype could be rescued by pharmacological inhibition of MAPK/Erk kinase (Mek). These data indicate that Rsk2 negatively regulates axon elongation via the MAPK pathway. Thus, the functional defects observed in the nervous system of CLS patients and animal models with Rsk2 deficiency might be caused by dysregulated neurite growth rather than primary neurodegeneration.
    Molecular and Cellular Neuroscience 07/2009; 42(2):134-41. DOI:10.1016/j.mcn.2009.06.006
  • Martin Heisenberg
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    ABSTRACT: Scientists and philosophers are using new discoveries in neuroscience to question the idea of free will. They are misguided, says Martin Heisenberg. Examining animal behaviour shows how our actions can be free.
    Nature 06/2009; 459(7244):164-5. DOI:10.1038/459164a
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    ABSTRACT: Ribosomal S6 kinases (RSKs) are growth factor-regulated serine-threonine kinases participating in the RAS-ERK signaling pathway. RSKs have been implicated in memory formation in mammals and flies. To characterize the function of RSK at the synapse level, we investigated the effect of mutations in the rsk gene on the neuromuscular junction (NMJ) in Drosophila larvae. Immunostaining revealed transgenic expressed RSK in presynaptic regions. In mutants with a full deletion or an N-terminal partial deletion of rsk, an increased bouton number was found. Restoring the wild-type rsk function in the null mutant with a genomic rescue construct reverted the synaptic phenotype, and overexpression of the rsk-cDNA in motoneurons reduced bouton numbers. Based on previous observations that RSK interacts with the Drosophila ERK homologue Rolled, genetic epistasis experiments were performed with loss- and gain-of-function mutations in Rolled. These experiments provided evidence that RSK mediates its negative effect on bouton formation at the Drosophila NMJ by inhibition of ERK signaling.
    Developmental Neurobiology 03/2009; 69(4):212-20. DOI:10.1002/dneu.20700
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    Pavel Masek, Martin Heisenberg
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    ABSTRACT: Even in a simple Pavlovian memory task an animal may form several associations that can be independently assessed by the appropriate tests. Studying conditioned odor discrimination of the fruit fly Drosophila melanogaster we found that animals store quality and intensity of an odor as separate memory traces. The trace of odor intensity is short-lived, decaying in <3 h. Only the last intensity value is stored. In contrast to odor-quality memory, odor-intensity memory does not require the rutabaga-dependent cAMP signaling pathway. Flies rely on their memory of intensity in a narrow concentration range in which they can generalize intensity. Larger concentration differences they treat like different qualities. This study shows that the perceptual identity of an odor is based on at least three lines of processing in the brain: (i) a memory of odor quality, (ii) a memory of odor intensity, and (iii) a range of intensities (and qualities), in which the odor is generalized.
    Proceedings of the National Academy of Sciences 10/2008; 105(41):15985-90. DOI:10.1073/pnas.0804086105
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    ABSTRACT: Whether motion vision uses color contrast is a controversial issue that has been investigated in several species, from insects to humans. We used Drosophila to answer this question, monitoring the optomotor response to moving color stimuli in WT and genetic variants. In the fly eye, a motion channel (outer photoreceptors R1-R6) and a color channel (inner photoreceptors R7 and R8) have been distinguished. With moving bars of alternating colors and high color contrast, a brightness ratio of the two colors can be found, at which the optomotor response is largely missing (point of equiluminance). Under these conditions, mutant flies lacking functional rhodopsin in R1-R6 cells do not respond at all. Furthermore, genetically eliminating the function of photoreceptors R7 and R8 neither alters the strength of the optomotor response nor shifts the point of equiluminance. We conclude that the color channel (R7/R8) does not contribute to motion detection as monitored by the optomotor response.
    Proceedings of the National Academy of Sciences 04/2008; 105(12):4910-5. DOI:10.1073/pnas.0711484105
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    ABSTRACT: In mammals and humans, noradrenaline is a key modulator of aggression. Octopamine, a closely related biogenic amine, has been proposed to have a similar function in arthropods. However, the effect of octopamine on aggressive behavior is little understood. An automated video analysis of aggression in male Drosophila has been developed, rendering aggression accessible to high-throughput studies. The software detects the lunge, a conspicuous behavioral act unique to aggression. In lunging, the aggressor rears up on his hind legs and snaps down on his opponent. By using the software to eliminate confounding effects, we now show that aggression is almost abolished in mutant males lacking octopamine. This suppression is independent of whether tyramine, the precursor of octopamine, is increased or also depleted. Restoring octopamine synthesis in the brain either throughout life or in adulthood leads to a partial rescue of aggression. Finally, neuronal silencing of octopaminergic and tyraminergic neurons almost completely abolishes lunges. Octopamine modulates Drosophila aggression. Genetically depleting the animal of octopamine downregulates lunge frequency without a sizable effect on the lunge motor program. This study provides access to the neuronal circuitry mediating this modulation.
    Current Biology 03/2008; 18(3):159-67. DOI:10.1016/j.cub.2007.12.052

Publication Stats

9k Citations
873.07 Total Impact Points

Institutions

  • 1978–2014
    • University of Wuerzburg
      • • Rudolf Virchow Center
      • • Department of Neurobiology and Genetics
      • • Institute for Hygiene and Microbiology
      • • Institute for Medical Radiation and Cell Research
      • • Theodor-Boveri-Institute
      Würzburg, Bavaria, Germany
  • 2001
    • Russian Academy of Sciences
      • Pavlov Institute of Physiology
      Moscow, Moscow, Russia
  • 1997
    • University at Albany, The State University of New York
      • Department of Biological Sciences
      New York, New York, United States
  • 1996
    • Academia Sinica
      • Institute of Physics
      T’ai-pei, Taipei, Taiwan
  • 1972–1977
    • Max Planck Institute for Biological Cybernetics
      Tübingen, Baden-Württemberg, Germany