Neural signatures of dynamic stimulus selection in Drosophila

Many animals orient using visual cues, but how a single cue is selected from among many is poorly understood. Here we show that Drosophila ring neurons—central brain neurons implicated in navigation—display visual stimulus selection. Using in vivo two-color two-photon imaging with genetically encoded calcium indicators, we demonstrate that individual ring neurons inherit simple-cell-like receptive fields from their upstream partners. Stimuli in the contralateral visual field suppressed responses to ipsilateral stimuli in both populations. Suppression strength depended on when and where the contralateral stimulus was presented, an effect stronger in ring neurons than in their upstream inputs. This history-dependent effect on the temporal structure of visual responses, which was well modeled by a simple biphasic filter, may determine how visual references are selected for the fly's internal compass. Our approach highlights how two-color calcium imaging can help identify and localize the origins of sensory transformations across synaptically connected neural populations.

[1]  Ranulfo Romo,et al.  Flexible Control of Mutual Inhibition: A Neural Model of Two-Interval Discrimination , 2005, Science.

[2]  Jonathan D. Victor,et al.  Subpopulations of neurons in visual area V 2 perform differentiation and integration operations in space and time , 2022 .

[3]  A. Borst Fly visual course control: behaviour, algorithms and circuits , 2014, Nature Reviews Neuroscience.

[4]  M. Heisenberg,et al.  Attracting the attention of a fly , 2011, Proceedings of the National Academy of Sciences.

[5]  Charles R. Gerfen,et al.  High-performance probes for light and electron microscopy , 2015, Nature Methods.

[6]  Bart G Borghuis,et al.  Temporal dynamics of direction tuning in motion-sensitive macaque area MT. , 2005, Journal of neurophysiology.

[7]  Michael B. Reiser,et al.  Visual Place Learning in Drosophila melanogaster , 2011, Nature.

[8]  G. DeAngelis,et al.  Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. , 1997, Journal of neurophysiology.

[9]  U. Homberg,et al.  Organization and functional roles of the central complex in the insect brain. , 2014, Annual review of entomology.

[10]  Michael M. Halassa,et al.  Thalamic control of sensory selection in divided attention , 2015, Nature.

[11]  Johannes D. Seelig,et al.  Neural dynamics for landmark orientation and angular path integration , 2015, Nature.

[12]  Uwe Homberg,et al.  A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain , 2008, The Journal of comparative neurology.

[13]  P. Hiesinger,et al.  Three‐dimensional reconstruction of the antennal lobe in Drosophila melanogaster , 1999, The Journal of comparative neurology.

[14]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[15]  Uwe Homberg,et al.  Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. , 2005, Journal of neurophysiology.

[16]  Amy Hu,et al.  Sensitive red protein calcium indicators for imaging neural activity , 2016, bioRxiv.

[17]  Thomas R Clandinin,et al.  Motion-detecting circuits in flies: coming into view. , 2014, Annual review of neuroscience.

[18]  T. S. Collett,et al.  How ladybirds approach nearby stalks: a study of visual selectivity and attention , 1988, Journal of Comparative Physiology A.

[19]  Susumu Tonegawa,et al.  Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons , 2015, Nature Neuroscience.

[20]  G. Rubin,et al.  The neuronal architecture of the mushroom body provides a logic for associative learning , 2014, eLife.

[21]  Julie H. Simpson,et al.  A GAL4-driver line resource for Drosophila neurobiology. , 2012, Cell reports.

[22]  B. Dickson,et al.  Genome-scale functional characterization of Drosophila developmental enhancers in vivo , 2014, Nature.

[23]  Tirin Moore,et al.  Prefrontal contributions to visual selective attention. , 2013, Annual review of neuroscience.

[24]  E. Knudsen Fundamental components of attention. , 2007, Annual review of neuroscience.

[25]  Yiming Li,et al.  Transformation of odor selectivity from projection neurons to single mushroom body neurons mapped with dual-color calcium imaging , 2013, Proceedings of the National Academy of Sciences.

[26]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[27]  R. Strauss,et al.  Analysis of a spatial orientation memory in Drosophila , 2008, Nature.

[28]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[29]  Hanchuan Peng,et al.  V3D enables real-time 3D visualization and quantitative analysis of large-scale biological image data sets , 2010, Nature Biotechnology.

[30]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[31]  Richard Axel,et al.  A dimorphic pheromone circuit in Drosophila from sensory input to descending output , 2010, Nature.

[32]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[33]  Aljoscha Nern,et al.  Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system , 2015, Proceedings of the National Academy of Sciences.

[34]  Yueqing Peng,et al.  Dopamine-Mushroom Body Circuit Regulates Saliency-Based Decision-Making in Drosophila , 2007, Science.

[35]  J. Victor,et al.  Responses to Orientation Discontinuities in V1 and V2: Physiological Dissociations and Functional Implications , 2014, The Journal of Neuroscience.

[36]  Edward M. Callaway,et al.  A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex , 2014 .

[37]  Gregory C. DeAngelis,et al.  Receptive-field dynamics in the central visual pathways , 1995, Trends in Neurosciences.

[38]  Y. Dan,et al.  Long-range and local circuits for top-down modulation of visual cortex processing , 2014, Science.

[39]  Balázs Rózsa,et al.  Single-cell–initiated monosynaptic tracing reveals layer-specific cortical network modules , 2015, Science.

[40]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.

[41]  Uwe Homberg,et al.  Microglomerular Synaptic Complexes in the Sky-Compass Network of the Honeybee Connect Parallel Pathways from the Anterior Optic Tubercle to the Central Complex , 2016, Front. Behav. Neurosci..

[42]  Kaori Ikeda,et al.  Sublinear integration underlies binocular processing in primary visual cortex , 2013, Nature Neuroscience.

[43]  J. Atick,et al.  Temporal decorrelation: a theory of lagged and nonlagged responses in the lateral geniculate nucleus , 1995 .

[44]  E. Knudsen,et al.  Reciprocal Inhibition of Inhibition: A Circuit Motif for Flexible Categorization in Stimulus Selection , 2012, Neuron.

[45]  Gilles Laurent,et al.  Transformation of Olfactory Representations in the Drosophila Antennal Lobe , 2004, Science.

[46]  John H. R. Maunsell,et al.  Neuronal Mechanisms of Visual Attention. , 2015, Annual review of vision science.

[47]  Stefan R. Pulver,et al.  Independent Optical Excitation of Distinct Neural Populations , 2014, Nature Methods.

[48]  Volker Hartenstein,et al.  Visual Input to the Drosophila Central Complex by Developmentally and Functionally Distinct Neuronal Populations , 2017, Current Biology.

[49]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[50]  Yvette E. Fisher,et al.  Orientation Selectivity Sharpens Motion Detection in Drosophila , 2015, Neuron.

[51]  M. Goldberg,et al.  Attention, intention, and priority in the parietal lobe. , 2010, Annual review of neuroscience.

[52]  Benjamin L. de Bivort,et al.  Evidence for selective attention in the insect brain , 2016, bioRxiv.

[53]  Johannes D. Seelig,et al.  Feature detection and orientation tuning in the Drosophila central complex , 2013, Nature.

[54]  A Guo,et al.  Choice Behavior of Drosophila Facing Contradictory Visual Cues , 2001, Science.