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First published online March 31, 2007
Journal of Experimental Biology 210, 1350-1361 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02744
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Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria

Michiyo Kinoshita1, Keram Pfeiffer2,* and Uwe Homberg2,{dagger}

1 School of Advanced Sciences, The Graduate University for Advanced Studies, Shonan Village, Hayama, Kanagawa 240-1930, Japan
2 Department of Biology, Animal Physiology, University of Marburg, D-35032 Marburg, Germany


Figure 1
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Fig. 1. Morphology and physiology of a LoTu1 neuron. (A) Schematic representation of the locust brain with arborization pattern of the polarized-light sensitive LoTu1 neuron. AL, antennal lobe; AOTu, anterior optic tubercle; Ca, calyces of mushroom body; CB, central body; LAL, lateral accessory lobe; Lo, lobula; Me, medulla. Scale bar: 200 µm. (B) Top trace shows mean spiking activity (moving average, bin width 0.5 s), middle trace shows intracellular recording of a LoTu1 neuron during zenithal stimulation with polarized light (Dors pol-light). Rotation of the polarizer through 360° (bottom trace) leads to e-vector-dependent changes in spiking activity. (C) Mean spiking activity and intracellular recording of responses to unpolarized white light applied from contralateral (C), ipsilateral (I), frontal (F) and dorsal (D) directions (150 W halogen bulb, spectral range: ~400–800 nm; visual angle: 3°; frontal: 13 µW cm–2; contralateral, ipsilateral, dorsal: 2–4 µW cm–2). Positive deflections in the bottom trace indicate duration of light stimuli.

 

Figure 2
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Fig. 2. Responses of LoTu1 to dorsally presented polarized light (Dors pol-light). (A) Intracellular recording traces during stimulation with three polarized monochromatic light stimuli at 9.0x109 photons cm–2 s–1. Bars below the recording traces indicate the duration of the stimuli and the direction of rotation. (B) Relative spiking activities at {Phi}max (open bars) and response strength R (solid black bars; for definition, see Materials and methods) in response to three polarized monochromatic lights (means ± s.e.m.). Relative spiking activity at {Phi}max and R are significantly larger in response to polarized blue light than to UV and green light, *P<0.05; **P<0.01 (t-test). (C,D) Intensity/response curves of neural activity at {Phi}max (C) and R (D) in response to polarized blue (450 nm) light (means ± s.e.m.). Maximum light intensity (logI=0) is 10.6x1012 photons cm–2 s–1. Solid lines show fits of Naka–Rushton functions with the fitting parameters rAmax=0.98, K=–3.33 log units, n=0.83 (C) and rRmax=0.99, K=–3.28 log units, n=0.4 (D). Broken lines indicate background activity (C) and no-stimulus R value (D).

 

Figure 3
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Fig. 3. Responses of LoTu1 to unpolarized monochromatic lights applied from three different directions. (A) Intracellular recording traces of responses to three unpolarized monochromatic lights (UV, 350 nm; B, 430 nm; G, 530 nm) at different intensities. Positive deflections in the traces below the spike trains indicate duration of light stimuli. Maximum intensity of each monochromatic light stimulus (0 log) was 16.5x1012 photons cm–2 s–1. Stimuli were given from the zenith (Dors), ipsilateral (Ipsi, 30–45° elevation) and contralateral (Contra, 30–45° elevation) directions. Blue light from dorsal and contralateral directions leads to inhibition (arrows) followed by rebound excitation after stimulation (open arrowheads). When light stimuli were applied from the ipsilateral direction, the neuron was inhibited by UV light (arrowhead) and excited by green light (double arrowhead). (B) Responses to three unpolarized monochromatic lights at 16.5x1010 photons cm–2 s–1. In each graph, activities to the three monochromatic lights are shown before stimulus onset (Pre, open bars), during stimulation (Stim, black bars), and after stimulation (Post, grey bars). LoTu1 is significantly inhibited by dorsal blue and green light and is excited by ipsilateral green light: *P<0.05; **P<0.01 (t-test). (C) Intracellular recording showing the responses to nine unpolarized monochromatic lights from the ipsilateral direction at 16.5x1010 photons cm–2 s–1. Lights at short wavelengths (330–430 nm) inhibit (arrowheads) and green lights (500–550 nm) excite the neuron (double arrowheads).

 

Figure 4
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Fig. 4. Comparison of sensitivities to polarized light and unpolarized light in LoTu1. (A) Intracellular recording traces during stimulation with dorsal polarized blue (450 nm) light (Dors pol-light) at three intensities. (B) Intracellular recording of responses to unpolarized monochromatic light stimuli with increasing intensity. Inhibition to dorsal blue light becomes obvious at logI=–1.5 (arrow); it is followed by rebound excitation (open arrowhead). Ipsilateral UV light at logI=–2 inhibits the neuron (arrowhead). At logI=–1, the neuron is completely inhibited including the inter-stimulus intervals (double open arrowhead). Ipsilateral green light leads to excitation beginning at logI=–2 (double arrowhead). Maximum light intensity for all stimuli (logI=0) was 10.6x1012 photons cm–2 s–1. (C) Intensity/response curves for dorsal polarized blue (450 nm) light at {Phi}max (Dors-pol B), dorsal unpolarized blue light (Dors-B), and unpolarized ipsilateral green light (Ipsi-G). The inhibitory responses to Dors-B are shown as normalized values of activity during stimulation minus activity before stimulation for better comparison. Solid lines are fits of Naka–Rushton functions with the fitting parameters rAmax=0.94, K=–3.25 log units, n=1.54 (Dors-pol B), rAmax= 1.03, K=–0.81 log units, n=2.27 (Dors B), and rAmax=1.63, K=–0.23 log units, n=0.88 (Ipsi G). Broken line indicates background activity.

 

Figure 5
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Fig. 5. Responses of TuTu1 to dorsal polarized light. (A) Intracellular recording traces of a TuTu1 during stimulation with three polarized monochromatic lights at 9.0x109 photons cm–2 s–1. (B) Relative spiking activities at {Phi}max (open bars) and response strength R (solid black bars) in response to three polarized monochromatic lights (means ± s.e.m.), *P<0.05; **P<0.01 (t-test). (C,D) Intensity/response curves of neural activity at {Phi}max (C) and response value R (D) in response to dorsally presented polarized blue (450 nm) light. Symbol shapes represent different recordings. Maximum intensity (logI=0) is 10.6x1012 photons cm–2 s–1. Solid lines show fits of Naka–Rushton functions with the fitting parameters rAmax=0.96, K=–4.26 log units, n=0.58 (C) and rRmax=0.90, K=–3.19 log units, n=0.66 (D). Broken line in C indicates background activity.

 

Figure 6
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Fig. 6. Intracellular recording traces of responses to three unpolarized monochromatic light stimuli in TuTu1 neurons. (A) TuTu1 is excited by UV light (double arrowhead) and is inhibited by green light (open arrowhead) when stimuli are applied from the ipsilateral direction (Ipsi). The neuron shows inhibitory responses (arrows) with rebound excitation (double open arrowheads) to UV and blue light applied from the contralateral direction (Contra). (B) In another recording TuTu1 is inhibited by dorsal (Dors) and contralateral blue light (arrows). Ipsilateral UV and blue light lead to excitations (arrowheads). Positive deflections in the bottom trace indicate duration of light stimuli. Maximum intensity (0 log) is 16.5x1012 photons cm–2 s–1.

 

Figure 7
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Fig. 7. Summary diagram of response properties of LoTu1 and TuTu1. (A) LoTu1 neurons are excited by ipsilateral unpolarized green light at elevations between 30 and 45° (Green +). Unpolarized UV light from the same range of directions leads to inhibition (UV –). The neurons are also inhibited by dorsal unpolarized blue light (Blue –). Dorsal polarized blue light activates LoTu1 neurons (Pol Blue +); the strength of activation is dependent on the e-vector orientation. (B) TuTu1 neurons are excited by ipsilateral unpolarized UV light at elevations between 30 and 45° (UV +). Unpolarized green light from the same directions leads to inhibition (Green –, observed in half of the recordings). Contralateral blue light at elevations between 30 and 45° (Blue –) inhibits TuTu1 neurons. Dorsal polarized blue light leads to sinusoidal modulation of the neuronal activity with excitatory and inhibitory components depending on the e-vector orientation (Pol Blue ±).

 





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