Behavioral state modulates the ON visual motion pathway of <i>Drosophila</i>

ME Chiappe, JD Seelig, MB Reiser, V Jayaraman, Walking modulates speed sensitivity in Drosophila motion vision. Curr Biol 20, 1470–1475 (2010).

KD Longden, HG Krapp, State-dependent performance of optic-flow processing interneurons. J Neurophysiol 102, 3606–3618 (2009).

G Maimon, AD Straw, MH Dickinson, Active flight increases the gain of visual motion processing in Drosophila. Nat Neurosci 13, 393–399 (2010).

CM Niell, MP Stryker, Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472–479 (2010).

HG Krapp, R Hengstenberg, Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384, 463–466 (1996).

MP Suver, A Mamiya, MH Dickinson, Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Curr Biol 22, 2294–2302 (2012).

SN Jung, A Borst, J Haag, Flight activity alters velocity tuning of fly motion-sensitive neurons. J Neurosci 31, 9231–9237 (2011).

JR Cooper, FE Bloom, RH Roth The Biochemical Basis of Neuropharmacology (Oxford Univ Press, New York, 2003).

SA Adamo, CE Linn, RR Hoy, The role of neurohormonal octopamine during “fight or flight” behaviour in the field cricket Gryllus bimaculatus. J Exp Biol 198, 1691–1700 (1995).

KD Longden, HG Krapp, Octopaminergic modulation of temporal frequency coding in an identified optic flow-processing interneuron. Front Syst Neurosci 4, 153 (2010).

D Rien, R Kern, R Kurtz, Octopaminergic modulation of contrast gain adaptation in fly visual motion-sensitive neurons. Eur J Neurosci 36, 3030–3039 (2012).

JC Tuthill, A Nern, GM Rubin, MB Reiser, Wide-field feedback neurons dynamically tune early visual processing. Neuron 82, 887–895 (2014).

F van Breugel, MP Suver, MH Dickinson, Octopaminergic modulation of the visual flight speed regulator of Drosophila. J Exp Biol 217, 1737–1744 (2014).

S Busch, M Selcho, K Ito, H Tanimoto, A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513, 643–667 (2009).

A Borst, Fly visual course control: Behaviour, algorithms and circuits. Nat Rev Neurosci 15, 590–599 (2014).

K-F Fischbach, A Dittrich, The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258, 441–475 (1989).

SY Takemura, , A visual motion detection circuit suggested by Drosophila connectomics. Nature 500, 175–181 (2013).

R Behnia, DA Clark, AG Carter, TR Clandinin, C Desplan, Processing properties of ON and OFF pathways for Drosophila motion detection. Nature 512, 427–430 (2014).

DA Clark, L Bursztyn, MA Horowitz, MJ Schnitzer, TR Clandinin, Defining the computational structure of the motion detector in Drosophila. Neuron 70, 1165–1177 (2011).

M Joesch, B Schnell, SV Raghu, DF Reiff, A Borst, ON and OFF pathways in Drosophila motion vision. Nature 468, 300–304 (2010).

MS Maisak, , A directional tuning map of Drosophila elementary motion detectors. Nature 500, 212–216 (2013).

JA Strother, A Nern, MB Reiser, Direct observation of ON and OFF pathways in the Drosophila visual system. Curr Biol 24, 976–983 (2014).

JA Strother, , The emergence of directional selectivity in the visual motion pathway of Drosophila. Neuron 94, 168–182.e10 (2017).

YE Fisher, M Silies, TR Clandinin, Orientation selectivity sharpens motion detection in Drosophila. Neuron 88, 390–402 (2015).

E Serbe, M Meier, A Leonhardt, A Borst, Comprehensive characterization of the major presynaptic elements to the Drosophila OFF motion detector. Neuron 89, 829–841 (2016).

E Buchner, Elementary movement detectors in an insect visual system. Biol Cybern 24, 85–101 (1976).

SY Takemura, , The comprehensive connectome of a neural substrate for “ON” motion detection in Drosophila. Elife 6, e24394 (2017).

H Luan, NC Peabody, CR Vinson, BH White, Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52, 425–436 (2006).

BD Pfeiffer, , Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735–755 (2010).

SL Lai, T Lee, Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9, 703–709 (2006).

A Jenett, , A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2, 991–1001 (2012).

TW Chen, , Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013).

MP Suver Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila melanogaster. PhD thesis (California Institute of Technology Pasadena CA). (2014).

T Fujiwara, TL Cruz, JP Bohnslav, ME Chiappe, A faithful internal representation of walking movements in the Drosophila visual system. Nat Neurosci 20, 72–81 (2017).

AJ Kim, JK Fitzgerald, G Maimon, Cellular evidence for efference copy in Drosophila visuomotor processing. Nat Neurosci 18, 1247–1255 (2015).

B Schnell, PT Weir, E Roth, AL Fairhall, MH Dickinson, Cellular mechanisms for integral feedback in visually guided behavior. Proc Natl Acad Sci USA 111, 5700–5705 (2014).

K Shinomiya, , Candidate neural substrates for off-edge motion detection in Drosophila. Curr Biol 24, 1062–1070 (2014).

SH Cole, , Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: Distinct roles for neural tyramine and octopamine in female fertility. J Biol Chem 280, 14948–14955 (2005).

JD Seelig, , Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nat Methods 7, 535–540 (2010).

MB Reiser, MH Dickinson, A modular display system for insect behavioral neuroscience. J Neurosci Methods 167, 127–139 (2008).

A Arenz, MS Drews, FG Richter, G Ammer, A Borst, The temporal tuning of the Drosophila motion detectors is determined by the dynamics of their input elements. Curr Biol 27, 929–944 (2017).

Z Yao, AM Macara, KR Lelito, TY Minosyan, OT Shafer, Analysis of functional neuronal connectivity in the Drosophila brain. J Neurophysiol 108, 684–696 (2012).

S Balfanz, T Strünker, S Frings, A Baumann, A family of octopamine [corrected] receptors that specifically induce cyclic AMP production or Ca2+ release in Drosophila melanogaster. J Neurochem 93, 440–451, and erratum (2005) 94:1168 (2005).

PD Evans, B Maqueira, Insect octopamine receptors: A new classification scheme based on studies of cloned Drosophila G-protein coupled receptors. Invert Neurosci 5, 111–118 (2005).

AH Brand, N Perrimon, Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993).

NC Klapoetke, , Independent optical excitation of distinct neural populations. Nat Methods 11, 338–346 (2014).

JC Tuthill, A Nern, SL Holtz, GM Rubin, MB Reiser, Contributions of the 12 neuron classes in the fly lamina to motion vision. Neuron 79, 128–140 (2013).

L Hiripi, L Nagy, RM Hollingworth, In vitro and in vivo effects of formamidines in locust (Locusta migratoria migratorioides). Acta Biol Hung 50, 81–87 (1999).

JJ Atick, AN Redlich, Towards a theory of early visual processing. Neural Comput 2, 308–320 (1990).

HB Barlow, Possible principles underlying the transformations of sensory messages. Sensory Communication, ed WA Rosenblith (MIT Press, Cambridge, MA), pp. 217–234 (1961).

S Laughlin, A simple coding procedure enhances a neuron’s information capacity. Z Naturforsch C 36, 910–912 (1981).

VB Hassenstein, W Reichardt, Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Z Naturforsch B 11, 513–524 (1956).

J Haag, A Arenz, E Serbe, F Gabbiani, A Borst, Complementary mechanisms create direction selectivity in the fly. Elife 5, e17421 (2016).

E Salazar-Gatzimas, , Direct measurement of correlation responses in Drosophila elementary motion detectors reveals fast timescale tuning. Neuron 92, 227–239 (2016).

HB Barlow, WR Levick, The mechanism of directionally selective units in rabbit’s retina. J Physiol 178, 477–504 (1965).

JM Pakan, , Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex. Elife 5, e14985 (2016).

A Nern, BD Pfeiffer, GM Rubin, Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proc Natl Acad Sci USA 112, E2967–E2976 (2015).

Y Iwai, , Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19, 77–89 (1997).

DA Wagh, , Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49, 833–844 (2006).

CR von Reyn, , A spike-timing mechanism for action selection. Nat Neurosci 17, 962–970 (2014).

Y Benjamini, Y Hochberg, Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57, 289–300 (1995).

RI Wilson, GC Turner, G Laurent, Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366–370 (2004).

M Demerec Biology of Drosophila (Hafner, New York, 1965).