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Neurons of the Central Complex of the Locust Schistocerca Gregaria Are Sensitive to Polarized Light

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Neurons of the Central Complex of the Locust Schistocerca Gregaria Are Sensitive to Polarized Light The Journal of Neuroscience, February 1, 2002, 22(3):1114–1125 Neurons of the Central Complex of the Locust Schistocerca gregaria are Sensitive to Polarized Light Harm Vitzthum,1 Monika Mu¨ ller,1 and Uwe Homberg2 1Institut fu¨ r Zoologie, Universita¨ t Regensburg, D-93040 Regensburg, Germany, and 2Fachbereich Biologie, Tierphysiologie, Universita¨ t Marburg, D-35032 Marburg, Germany The central complex is a topographically ordered neuropil ized light, certain neurons showed tonic spike discharges to structure in the center of the insect brain. It consists of three unpolarized light. Most polarization-sensitive neurons were as- major subdivisions, the upper and lower divisions of the central sociated with the lower division of the central body, but one body and the protocerebral bridge. To further characterize the type of neuron with arborizations in the upper division of the role of this brain structure, we have recorded the responses of central body was also polarization-sensitive. Visual pathways identified neurons of the central complex of the desert locust signaling polarized light information to the central complex Schistocerca gregaria to visual stimuli. We report that particular include projections via the anterior optic tubercle. Considering types of central complex interneurons are sensitive to polarized the receptive fields of the neurons and the biological signifi- light. Neurons showed tonic responses to linearly polarized cance of polarized light in insects, the central complex might light with spike discharge frequencies depending on e-vector serve a function in sky compass-mediated spatial navigation of orientation. For all neurons tested, e-vector response curves the animals. showed polarization opponency. Receptive fields of the re- corded neurons were in the dorsal field of view with some Key words: polarized light; polarization vision; central com- neurons receiving input from both compound eyes and others, plex; compass navigation; head direction; insect brain; locust; only from the ipsilateral eye. In addition to responses to polar- Schistocerca gregaria Insects can detect the polarization pattern of the blue sky and use roach (Loesel and Homberg, 2001), and the desert ant (Labhart, it as a sensory cue for spatial navigation (for review, see Wehner 2000). 1992, 1994). The biological significance of polarization vision for In search for higher brain areas involved in sky compass ori- compass orientation has been most thoroughly studied in desert entation, we report here that certain interneurons in the locust ants (Wehner, 1994) and honeybees (Rossel and Wehner, 1986; central complex are polarization-sensitive. The central complex is Rossel, 1993), but polarized light-dependent orientation has also a group of interconnected neuropils in the center of the insect been demonstrated in several other insect species (for review, see brain and includes the protocerebral bridge, the upper and lower Stockhammer, 1959; Waterman, 1981). Photoreceptors in a small divisions of the central body, and the paired noduli (Homberg, dorsal rim area in the compound eye of many insects are partic- 1987) (see Fig. 1A). Its most striking feature is a highly stratified ularly adapted for polarized light detection and show high polar- internal organization consisting of well defined layers in the ization sensitivity (for review, see Labhart and Meyer, 1999). central body and, perpendicularly, an arrangement into sets of Polarization-sensitive interneurons in the insect brain were sixteen columns. Columnar neurons provide precise interhemi- first described in the optic lobe of the cricket, Gryllus campestris spheric connections and are the main output pathway from the (Labhart, 1988; Labhart and Petzold, 1993; Labhart et al., 2001; central complex to the adjacent lateral accessory lobes. While the Petzold, 2001). These neurons, like the photoreceptors of the anatomical organization of the central complex has been unrav- dorsal rim area, are most sensitive to blue light. The neurons eled in some detail (Hanesch et al., 1989; Homberg, 1985, 1987, show polarization opponency, i.e., e-vector orientations causing 1991; Wendt and Homberg, 1992; Vitzthum et al., 1996; Mu¨ller et ⌽ maximal excitation ( max) are oriented perpendicularly to al., 1997; Vitzthum and Homberg, 1998), its functional role is ⌽ e-vectors causing maximal inhibition ( min). This feature indi- little understood. In moths, descending neurons from the lateral cates that the neurons receive antagonistic inputs from perpen- accessory lobes are involved in motor control such as steering dicularly oriented e-vector analyzers. Recently, polarization- maneuvers during walking and flight (Kanzaki et al., 1991, 1994), opponent interneurons were also found in the optic lobe of the and behavioral analysis of Drosophila melanogaster mutants with desert locust (Homberg and Wu¨rden, 1997), the Madeira cock- structural defects in the central complex also support a role of the central complex in motor control (Strauss and Heisenberg, 1993; Ilius et al., 1994). Received July 17, 2001; revised Oct. 29, 2001; accepted Nov. 14, 2001. This study demonstrates a novel sensory aspect of signaling in This work was supported by Grants Ho 950/4 and Ho 950/13 from the Deutsche Forschungsgemeinschaft. We thank Dr. Monika Stengl for insightful discussions and the central complex. We show that neurons of the locust central suggestions on this manuscript. complex are sensitive to dorsally presented polarized light and Correspondence should be addressed to Dr. Uwe Homberg, Fachbereich Biologie, suggest an involvement of this brain structure in sky compass Tierphysiologie, Universita¨t Marburg, D-35032 Marburg, Germany. E-mail: [email protected]. orientation. Copyright © 2002 Society for Neuroscience 0270-6474/02/221114-12$15.00/0 Parts of this study have been published in abstract form (Mu¨ller Vitzthum et al. • Polarized Light-Sensitive Neurons J. Neurosci., February 1, 2002, 22(3):1114–1125 1115 and Homberg, 1994; Homberg and Mu¨ller, 1995; Vitzthum et al., anol series, cleared in methyl salicylate, and examined with a fluores- 1997). cence microscope (Zeiss). For detailed anatomical examination, the brains were subsequently processed for Lucifer yellow immunocyto- MATERIALS AND METHODS chemistry by means of the indirect peroxidase antiperoxidase (PAP) technique (Sternberger, 1986), as described by Homberg and Wu¨rden Preparation. Experiments were performed on adult locusts (Schistocerca (1997). The Neurobiotin-injected brains were rinsed in PBS (0.01 M gregaria) obtained from a crowded laboratory colony. Animals were phosphate buffer; 0.45 M NaCl) with 0.1% Triton X-100 (Sigma, Deisen- anesthetized by cooling and were waxed anterior uppermost to a metal hofen, Germany), embedded in gelatin–albumin, and sectioned at 30 ␮m holder. The heads of the locusts were immobilized by a wax–rosin with a Vibratome (Technical Products, St. Louis, MO). The free-floating mixture, and their legs were removed. For intracellular recordings from sections were incubated for at least 18 hr with Streptavidin conjugated to the central protocerebrum, a small window was cut into the head capsule a polymere of horseradish peroxidase (Sigma), diluted at 1:2000 or with between the two compound eyes. The right antenna and the median Streptavidin conjugated to horseradish peroxidase (Amersham Buchler, ocellus of the animal were removed. After removing fat and some Braunschweig, Germany) at 1:200 in PBS with 0.5% Triton X-100. The tracheal sacs, the midbrain was supported and slightly lifted by a stainless sections were subsequently treated for 10–20 min with a solution of steel platform that served as the indifferent electrode. A small area of the 3,3Ј-diaminobenzidine tetrahydrochloride (0.3 mg/ml) in 0.05 M Tris– midbrain was desheathed to facilitate microelectrode penetration. In HCl buffer, pH 7.4, with 0.3% nickel ammonium sulfate and H2O2 some preparations, the recording site was stabilized further by a stainless (0.015%). The sections were mounted and cleared like the Lucifer steel ring that was gently pushed onto the brain. In some recordings, yellow-injected brains (Homberg and Wu¨rden, 1997). All neurons were especially when hemolymph pumping movements prevented stable re- reconstructed from serial frontal sections by using a Zeiss microscope cordings, the animals’ head was cut off from the thorax. Successful with camera lucida attachment. The terminology for brain structures recordings from isolated heads were possible for up to 3 hr by perfusing largely follows the nomenclature of Strausfeld (1976) and, for central the preparation regularly with locust saline (Clements and May, 1974). ⍀ complex subdivisions, Williams (1975), Homberg (1991), and Mu¨ller et Electrophysiology. Electrodes (resistance in the tissue, 80–200 M ) al. (1997). Positional information is given with respect to the body axis of were drawn from glass capillaries (Hilgenberg, Malsfeld, Germany). the animal. They were filled either with 5% Lucifer yellow (Molecular Probes, Eugene, OR) or with 4% Neurobiotin (Vector Laboratories, Burlingame, CA) at the tip. Lucifer-filled electrodes were backed up with 0.1 M LiCl, RESULTS and electrodes filled with Neurobiotin were backed up with 1 M KCl. This study is based on the characterization of 41 polarization- Electrodes were aimed at neural processes in the center of the brain close sensitive interneurons (POL neurons) of 140 neurons recorded to the stump of the median ocellus at a depth of 150–200 ␮m from
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