Forschungsinteressen

1. Neural basis of polarization vision in the brain of desert 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. Neural basis of polarization vision in the brain of desert locusts

Miklós Bech, Jerome Beetz, Tim-Henning Humberg, Fabian Schmeling, Matthias Schön, Uwe Homberg

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 [1,2]. 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 [3]. We have characterized behavioral responses of locusts to polarized light [4,5] and have identified neural pathways in the locust brain that are involved in processing of polarized light information [6-8]. Polarization-sensitive (POL) interneurons were studied physiologically in the medulla [9], the anterior optic tubercle of the brain [10-14], the central complex of the median protocerebrum [15-18], and in the ventral nerve cord [19]. 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 (i) receptive-field properties of polarization-sensitive photoreceptors and brain interneurons, (ii) mechanisms underlying the topographical representation of celestial E-vectors in the central complex, and (iii) state-dependent changes in polarization sensitivity in the central complex.

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

Irina Bedoeva, Jerome Beetz, Tobias Bockhorst, Florian Dersch, Joss von Hadeln, Tim-Henning Humberg, Fatimeh Mamoudi, Ronny Rosner, Johannes Schuh, Uwe Homberg

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 [20]. 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 [21] and of neurons providing the columnar organization of the central complex [22]. 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 [23], dopamine [24], serotonin [25], histamine [26], nitric oxide/cGMP [27,28], and of peptides related to allatostatins [29], CCAP [30], tachykinins [31], and allatotropins [32] in distinct populations of central-complex neurons. Single cell recordings suggest that the central complex is involved in flight control [33] and serves a role as navigational center for direction finding and spatial orientation [2]. A network of polarization-sensitive neurons in the central complex suggests that it serves a role as an internal sky compass in the locust brain [15-18]. A digital 3D atlas of the central complex and associated neuropils aids in further characterization of its functional role in spatial orientation [34].

Current anatomical/immunocytochemical projects (i) are aimed at identifying octopaminergic and tyraminergic neurons of the central complex, (ii) establish 3 D reconstructions of all major cell types of the central complex and (iii) compile data towards an inventory of tangential cell types of the central complex. In a comparative project, we analyze the neurochemical organization of the central complex of the cockroach Rhyparobia maderae, a nocturnal species with reduced visual input to the central complex [22]. Physiological studies analyze visual signal processing in central complex-neurons, in particular responses to small translating targets and looming stimuli and investigate the role of motor activity on sensory signal processing.

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3. Anatomical and neurochemical organization of the insect brain

Irina Bedoeva, Linda Häger, Evelyn Rieber, Jutta Seyfarth, Uwe Homberg

The insect brain is supplied with an astounding diversity of signalling molecules including neurotransmitters, neuromodulators, and neuropeptides [35-37]. 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 [38], in the optic lobe [39,32] in the mushroom body [40,27] and in the central complex [23,27,30], and showed reproducible and widespread colocalization of transmitter substances in various brain areas [23,29,39,41-44]. For further anatomical studies, we generated standardized anatomical atlases of the locust brain [34,45], to serve as platforms for anatomical data bases and for neural network analysis in a common anatomical reference.

         Current projects further analyze the compartmentation of the locust brain, based on synapsin-immunostaining, backfills from peripheral nerves, and single cell labelling.

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4. Mechanisms of circadian rhythms in insects

Evelyn Rieber, Uwe Homberg

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 [46-49, 56]. Several 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 [50] but provide photic input through intercalated interneurons. An extraocular photoreceptor organ with immunoreactivity to the photopigment crypochrome [51] 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 [52]. Injection assays showed that part of this pathway acts through GABA- and allatostatin-immunoreactive pathways [53], while the neuropeptide orcokinin might play a role in light entrainment of the clock via the contralateral compound eye [42,54]. Recent analysis of myoinhibitory peptides in the cockroach showed colocalization with PDF and suggest an involvement in different aspects of the circadian system [55].

Current projects are aimed at establishing a circadian behavioural assay for the desert locust and investigate the distribution and possible function of orcokinin in the locust circadian system.

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References

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

[2]   Homberg U, Heinze S, Pfeiffer K, Kinoshita M, el Jundi B. 2011. Central neural coding of sky polarization in insects. Phil. Trans. R. Soc. B 366:680-687

[3]   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

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

[5]   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

[6]   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

[7]   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

[8]   el Jundi B, Homberg U (2010) Evidence for the possible existence of a second polariazation-vision pathway in the locust brain. J Insect Physiol 56:971-979

[9]   el Jundi B, Pfeiffer K, Homberg U (2011) A distinct layer of the medulla integrates sky compass signal in the brain of an insect. PLoS ONE 6:e27855

[10] 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

[11] 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

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

[13] Pfeiffer K, Negrello M, Homberg U (2011) Conditional perception under stimulus ambiguity: Polarization- and azimuth-sensitive neurons in the locust brain are inhibited by low degrees of polarization. J Neurophysiol 105:28-35

[14] el Jundi B, Homberg U (2012) Receptive field properties and intensity-response functios of polarization-sensitive neurons in the optic tubercle in gregarious and solitarious locusts. J Neurophysiol  108:1695-1710

[15] 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

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

[17] 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

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

[19] Träger U Homberg U (2011) Polarization-sensitive descending neurons in the locust: connecting the brain to thoracic ganglia. J Neurosci 31:2238-2247

[20] 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

[21] 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

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

[23] 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

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

[25] 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

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

[27] 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

[28] Siegl T, Schachtner J, Holstein GR, 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

[29] 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

[30] 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

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

[32] 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

[33] 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

[34] 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 Sys Neurosci 3:21

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

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

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

[38] 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

[39] 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

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

[41] 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

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

[43] 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

[44] 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

[45] 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

[46] 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

[47] 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

[48] 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

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

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

[51] 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

[52] 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

[53] 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

[54] 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

[55] Schulze J, Neupert S, Schmidt L, Predel R, Lamkemeyer T, Homberg U, Stengl M (2012) Myoinhibitory peptides in the brain of the cockroach Leucophaea maderae and colocalization  with pigment-dispersing factor in circadian pacemaker cells. J Comp Neurol 520: 1078-1097

[56] Wei J, el Jundi B, Homberg U, Stengl M (2010) Implemenatation of pigment-dispersing factor-immunoreactive neurons in a standardized atlas of the brain of the cockroach Leucophaea maderae. J Comp Neurol 518:4113-4133