Forschungsinteressen

1. Polarization vision and sky compass navigation in locusts

2. Organization and function of the central complex in the insect brain

3. Anatomical and neurochemical organization of the insect brain

4. Mechanisms of circadian rhythms in insects

1. Polarization vision and sky compass navigation in locusts

Basil el Jundi, Fabian Schmeling, Johannes Schuh, Miklós Bech, Evelyn Rieber, Joss von Hadeln, Ulrike Träger, Uwe Homberg

Drawing_behavior Behavioral experiments in honeybees, ants, and other insects have shown that the polarization pattern of the blue sky serves an important role in insect compass navigation and spatial orientation. We investigate the neural mechanisms underlying polarized skylight navigation in the desert locust Schistocerca gregaria[1]. In S. gregaria, as in other insects, a small dorsal rim area of the compound eye is highly specialized for the detection of polarized light [2]. We have characterized behavioral responses of locusts to polarized light [3,4] and have identified neural pathways in the locust brain that are involved in processing of polarized light information [5,6]. Polarization-sensitive (POL) interneurons were studied physiologically in the anterior optic tubercle of the brain [7-9] and in the central complex of the median protocerebrum [10-13]. Most polarization-sensitive interneurons show polarization opponency, i.e. E-vectors leading to maximal excitation are perpendicular to E-vectors causing maximal inhibition. Current projects analyze the behavioural sensitivity of locusts to polarized light, peripheral mechanisms underlying polarization opponency, receptive field properties, chromatic and absolute sensitivities of POL neurons in the brain, and descending pathways to thoracic motor systems that are sensitive to polarized light.

References

[1] Homberg U (2004) In search of the sky compass in the insect brain. Naturwissenschaften 91:199-208

[2] Homberg U, Paech A (2002) Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev 30:271-280

[3] Mappes M, Homberg U (2004) Behavioral analysis of polarization vision in tethered flying locusts. J Comp Physiol A 190:61-68

[4] Mappes M, Homberg U (2007) Surgical lesion of the anterior optic tract abolishes polarotaxis in tethered flying locusts, Schistocerca gregaria. J Comp Physiol A 193:43-50

[5] Homberg U, Hofer S, Pfeiffer K, Gebhardt S (2003) Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J Comp Neurol 462:415-430

[6] Träger U, Wagner R, Bausenwein B, Homberg U (2008) A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J Comp Neurol 506:288-300

[7] Pfeiffer K, Kinoshita M, Homberg U (2005) Polarization-sensitive and light sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J Neurophyiol 94:3903-3915

[8] Kinoshita M, Pfeiffer K, Homberg U (2007) Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust, Schistocerca gregaria. J Exp Biol 310:1350-1361

[9] Pfeiffer K, Homberg U (2007) Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr Biol 17:960-965

[10] Vitzthum H, Müller M, Homberg U (2002) Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 22:1114-1125

[11] Heinze S, Homberg U (2007) Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315:995-997

[12] Heinze S, Homberg, U (2009) Linking the input to the output: new sets of neurons complement the polarization vision network of the locust central complex. J Neurosci 29:4911-4921

[13] Heinze S, Gotthardt S, Homberg U (2009) Transformation of polarized light information in the central complex of the locust. J Neurosci 29:11783-11793

2. Organization and function of the central complex in the insect brain

Ronny Rosner, Tobias Bockhorst, Basil el Jundi, Miklós Bech, Joss von Hadeln, Tim-Henning Humberg, Christoph Frick, Ulrike Träger, Uwe Homberg

standard_CC The central complex is a group of interconnected neuropils in the center of the insect brain. It consists of the protocerebral bridge, the upper and lower divisions of the central body and a pair of posterior noduli. The most striking feature of this brain area is a highly modular arrangement of neural elements, forming series of layers and columns [1,2]. To understand the functional role of this brain area, we have analyzed the neuroarchitecture of the lower division of the central body of the locust [3] and of neurons providing the columnar organization of this brain area [4]. Immunocytochemical studies showed that a large variety of neurotransmitters and neuropeptides is present in the central complex. We have provided detailed maps for the distribution of GABA [5], dopamine [6], serotonin [7], histamine [8], nitric oxide/cGMP [9,10], and of peptides related to allatostatins [11], CCAP [12], tachykinins [13], and allatotropins [14] in distinct populations of central-complex neurons. Single cell recordings suggest that the central complex is involved in flight control [15] and serves a role as (a) navigational center for direction finding and spatial orientation [16]. Analysis of neural networks in the central complex that are sensitive to polarized light suggest that the central complex serves a role as an internal sky compass in the locust brain [17-20]. We have recently constructed a digital 3D atlas of the central complex and associated neuropils for further characterization of its functional role in spatial orientation [21].

References

[1] Homberg U (1987) Structure and functions of the central complex in insects. In: Arthropod brain: its evolution, development, structure, and functions (Gupta AP, ed), pp 347-367. New York: Wiley

[2] Homberg U (2008) Evolution of the central complex in the arthropod brain and its association with the visual system. Arthropod Struct Dev 37:347-362

[3] Müller M, Homberg U, Kühn A (1997) Neuroarchitecture of the lower division of the central body in the brain of the locust Schistocerca gregaria. Cell Tissue Res 288:159-176

[4] Heinze S, Homberg U (2008) Neuroarchitecture of the central complex of the desert locust: Intrinsic and columnar neurons. J Comp Neurol 511:454-478

[5] Homberg U, Vitzthum H, Müller M, Binkle U (1999) Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: Identification of immunoreactive cells and colocalization with neuropeptides. J Comp Neurol 409:495-507

[6] Wendt B, Homberg U (1992) Immunocytochemistry of dopamine in the brain of the locust Schistocerca gregaria. J Comp Neurol 321:387-403

[7] Homberg U (1991) Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol 303:245-254

[8] Gebhardt S, Homberg U (2004) Immunocytochemistry of histamine in the brain of the locust Schistocerca gregaria. Cell Tissue Res 317:195-205

[9] Kurylas AE, Ott SR, Schachtner J, Elphick MR, Williams L, Hombrg U (2005) Localization of nitric oxide synthase in the central complex and surrounding midbrain neuropils of the locust Schistocerca gregaria. J Comp Neurol 484:206-223

[10] Siegl, T., Schachtner, J., Holstein, G.R., and Homberg, U. (2009). NO/cGMP signalling: L-citrulline and cGMP immunostaining in the central complex of the desert locust Schistocerca gregaria. Cell Tissue Res 337: 327-340

[11] Vitzthum H, Homberg U, Agricola H (1996) Distribution of Dip-allatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex. J Comp Neurol 369:419-437

[12] Dircksen H, Homberg U (1995) Crustaceen cardioactive peptide-immunoreactive neurons innervating brain neuropils, retrocerebral complex and stomatogastric nervous system of the locust, Locusta migratoria. Cell Tissue Res 279:495-515

[13] Vitzthum H, Homberg U (1998) Locustatachykinin I/II-immunoreactive neurons in the central complex of the locust brain. J Comp Neurol 390:455-469

[14] Homberg U, Brandl C, Clynen E, Schoofs L, Veenstra JA (2004) Mas-allatotropin/Lom-AG-myotropin I immunostaining in the brain of the locust, Schistocerca gregaria. Cell Tissue Res 318:439-457

[15] Homberg U (1994) Flight-correlated activity changes in neurons of the lateral accessory lobes in the brain of the locust Schistocerca gregaria. J Comp Physiol A175:597-610

[16] Homberg U (2004) In search of the sky compass in the insect brain. Naturwissenschaften 91:199-208

[17] Träger U, Wagner R, Bausenwein B, Homberg U (2008) A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J Comp Neurol 506:288-300

[18] Heinze S, Homberg U (2007) Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315:995-997

[19] Heinze S, Homberg, U (2009) Linking the input to the output: new sets of neurons complement the polarization vision network of the locust central complex. J Neurosci 29:4911-4921

[20] Heinze S, Gotthardt S, Homberg U (2009) Transformation of polarized light information in the central complex of the locust. J Neurosci 29:11783-11793

[21] el Jundi B, Heinze S, Lenschow C, Kurylas A, Rohlfing T, Homberg U (2010) The locust standard brain: a 3D standard of the central complex as a platform for neural network analysis. Front Syst Neurosci 3:21

3. Anatomical and neurochemical organization of the insect brain

Alexandra Schindler, Katharina Bode, Jerome Beetz, Basil el Jundi, Jutta Seyfarth, Ulrike Träger, Uwe Homberg

The insect brain is supplied with an astounding diversity of signalling molecules including neurotransmitters, neuromodulators, and neuropeptides [1,2,3]. In order to understand the chemical compartmentalization of the brain and its constituent neuropils, we map the distribution of these substances using immunocytochemical and histochemical staining techniques. So far, these studies revealed novel chemically defined compartments in the antennal lobe [4], in the optic lobe [5,6] in the mushroom body [6,7] and in the central complex [8-10], and showed reproducible and widespread colocalization of transmitter substances in various brain areas [5,10-15]. Transmitter antisera, furthermore, served as valuable tools for developmental studies of the insect brain during metamorphosis [16,17]. For further anatomical studies, we generated standardized anatomical atlases of the ventral ganglion of Drosophila [18] and the locust brain [19], to serve as platforms for anatomical data bases and for neural network analysis in a common anatomical reference.

References

[1] Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189-209

[2] Homberg U, Müller U (1999) Neuroactive substances in the antennal lobe. In: BS. Hansson (ed) Insect Olfaction. Springer, Berlin, pp 181-206

[3] Nässel D, Homberg U (2006) Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1-24

[4] Homberg U, Hoskins SG, Hildebrand JG (1995) Distribution of acetylcholinesterase activity in the deutocerebrum of the sphinx moth Manduca sexta. Cell Tissue Res 279:249-259

[5] Würden S, Homberg U (1995) Immunocytochemical mapping of serotonin and neuropeptides in the accessory medulla of the locust, Schistocerca gregaria. J Comp Neurol 362:305-319

[6] Homberg U, Brandl C, Clynen E, Schoofs L, Veenstra JA (2004) Mas-allatotropin/Lom-AG-myotropin I immunostaining in the brain of the locust, Schistocerca gregaria. Cell Tissue Res 318:439-457

[7] Strausfeld NJ, Homberg U, Kloppenburg P (2000) Parallel organization in honey bee mushroom bodies by peptidergic Kenyon cells. J Comp Neurol 424:179-195

[8] Kurylas AE, Ott SR, Schachtner J, Elphick MR, Williams L, Hombrg U (2005) Localization of nitric oxide synthase in the central complex and surrounding midbrain neuropils of the locust Schistocerca gregaria. J Comp Neurol 484:206-223

[9] Dircksen H, Homberg U (1995) Crustacean cardioactive peptide-immunoreactive neurons innervating brain neuropils, retrocerebral complex and stomatogastric nervous system of the locust, Locusta migratoria. Cell Tissue Res 279:495-515

[10] Homberg U, Vitzthum H, Müller M, Binkle U (1999) Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: Identification of immunoreactive cells and colocalization with neuropeptides. J Comp Neurol 409:495-507

[12] Davis NT, Homberg U, Teal PEA, Altstein M, Hildebrand JG (1996) Neuroanatomy and immunocytochemistry of the neurosecretory system of the subesophageal ganglion of the tobacco hawkmoth, Manduca sexta: Immunoreactivity to PBAN and other neuropeptides. Microsc Res Tech 35:201-229

[13] Hofer S, Homberg U (2006) Orcokinin immunoreactivity in the accessory medulla of the cockroach Leucophaea maderae. Cell Tissue Res 325:589-600

[14] Berg B, Schachtner J, Utz S, Homberg U (2007) Distribution of neuropeptides in the primary olfactory centre of the heliothine moth Heliothis virescens. Cell Tissue Res 327:385-398

[15] Berg B, Schachtner J, Homberg U (2009) g-Aminobutyric-acid immunostaining in the antennal lobe of the moth Heliothis virescens and its colocalization with neuropeptides. Cell Tissue Res 335:593-605

[16] Kirchhof BS, Homberg U, Mercer AR (1999) Development of dopamine-immunoreactive neurons associated with the antennal lobes of the honey bee, Apis mellifera. J Comp Neurol 411:643-653

[17] Schachtner J, Homberg U, Truman, JW (1999) Regulation of cyclic GMP elevation in the developing antennal lobe of the sphinx moth, Manduca sexta. J Neurobiol 41:359-375

[18] Santos JG, Vömel M, Struck R, Homberg U, Nässel DR, Wegener C (2007) Neuroarchitecture of peptidergic systems in the larval ventral ganglion of Drosophila melanogaster. Plos One 8:e695

[19] Kurylas A, Rohlfing T, Krofczik S, Jenett A, Homberg U (2008) Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell Tissue Res 333:125-145

4. Mechanisms of circadian rhythms in insects

Ulrike Träger, Uwe Homberg

accessory_medulla Based on the highly unique pattern of immunostaining with antisera against pigment-dispersing hormone, we hypothesized that the accessory medulla is the internal clock in the brain of Orthoptera, Blattaria and Diptera [1-4]. More recent studies focussed on light entrainment pathways of the clock in the cockroach Leucophaea maderae. Histamine-immunoreactive photoreceptor neurons of the compound eye do not directly contact the accessory medulla [5] but provide photic input through intercalated interneurons. An extraocular photoreceptor organ with immunoreactivity to the photopigment crypochrome [6] might provide additional photic input to the clock. In electrophysiological studies we showed that neurons resembling pigment-dispersing hormone immunoreactive neurons are likely to be output elements of the clock, while neurons with processes in the lamina and medulla proper are probably involved in light entrainment pathways to the clock [7]. Injection assays showed that part of this pathway acts through GABA- and allatostatin-immunoreactive pathways [8]. Experiments to analyze the role of the neuropeptide orcokinin in the circadian system suggest a role in light entrainment of the clock via the contralateral compound eye [9,10]. Current projects analyze neural mechanisms underlying time-compensation in sky compass navigation of desert locusts.

References

[1] Homberg U, Würden S, Dircksen H, Rao KR (1991) Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Res 266:343-357

[2] Helfrich-Förster C, Homberg U (1993) Pigment-dispersing hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 337:177-190

[3] Stengl M, Homberg U (1994) Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol A175:203-213

[4] Helfrich-Förster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15:567-594

[5] Loesel R, Homberg U (1999) Histamine-immunoreactive neurons in the brain of the cockroach Leucophaea maderae. Brain Res 842:408-418

[6] Fleissner Ge, Loesel R, Fleissner Gü, Waterkamp M, Kleiner O, Batschauer A, Homberg U (2001) Candidates for extraocular photoreceptors in the cockroach suggest homology to the lamina and lobula organs in beetles. J Comp Neurol 433:401-414

[7] Loesel R, Homberg U (2001) Anatomy and physiology of neurons with processes in the accessory medulla of the cockroach Leucophaea maderae. J Comp Neurol 439:193-207

[8] Petri B, Homberg U, Loesel R, Stengl M (2002) Evidence for a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. J Exp Biol 205:1459-1469

[9] Hofer S, Homberg U (2006) Orcokinin immunoreactivity in the accessory medulla of the cockroach Leucophaea maderae. Cell Tissue Res 325:589-600

[10] Hofer S, Homberg U (2006) Evidence for a role of orcokinin-related peptides in the circadian clock controlling locomotor activity of the cockroach Leucophaea maderae. J Exp Biol 209:2794-803