Ring attractor dynamics in the Drosophila central brain

Representing direction in the fly A population of cells called compass neurons represents a fruitfly's heading direction. Kim et al. used imaging and optogenetics in behaving flies to elucidate the functional architecture of the underlying neuronal network. They observed local excitation and global inhibition between the compass neurons. The features of the network were best explained by a ring attractor network model. Until now, this hypothesized network structure has been difficult to demonstrate in a real brain. Science, this issue p. 849 A neuronal network in the fly brain uses global inhibition and local excitation to enforce an internal representation of heading direction. Ring attractors are a class of recurrent networks hypothesized to underlie the representation of heading direction. Such network structures, schematized as a ring of neurons whose connectivity depends on their heading preferences, can sustain a bump-like activity pattern whose location can be updated by continuous shifts along either turn direction. We recently reported that a population of fly neurons represents the animal’s heading via bump-like activity dynamics. We combined two-photon calcium imaging in head-fixed flying flies with optogenetics to overwrite the existing population representation with an artificial one, which was then maintained by the circuit with naturalistic dynamics. A network with local excitation and global inhibition enforces this unique and persistent heading representation. Ring attractor networks have long been invoked in theoretical work; our study provides physiological evidence of their existence and functional architecture.

[1]  A. Turing The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[2]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Bruce L. McNaughton,et al.  A Model of the Neural Basis of the Rat's Sense of Direction , 1994, NIPS.

[4]  D. Fitzpatrick,et al.  Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns , 1995, Neuron.

[5]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Berend Smit,et al.  Understanding molecular simulation: from algorithms to applications , 1996 .

[7]  K. Zhang,et al.  Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  H S Seung,et al.  How the brain keeps the eyes still. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[9]  M. Heisenberg,et al.  Conditioned visual flight orientation in Drosophila: dependence on age, practice, and diet. , 1996, Learning & memory.

[10]  C. Koch,et al.  Methods in Neuronal Modeling: From Ions to Networks , 1998 .

[11]  M. Dickinson,et al.  Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[12]  Richard H R Hahnloser,et al.  Double-ring network model of the head-direction system. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[13]  Karel Svoboda,et al.  ScanImage: Flexible software for operating laser scanning microscopes , 2003, Biomedical engineering online.

[14]  S. Amari Dynamics of pattern formation in lateral-inhibition type neural fields , 1977, Biological Cybernetics.

[15]  M. Heisenberg,et al.  Neuronal architecture of the central complex in Drosophila melanogaster , 2004, Cell and Tissue Research.

[16]  D. Tank,et al.  Persistent neural activity: prevalence and mechanisms , 2004, Current Opinion in Neurobiology.

[17]  Xiao-Jing Wang,et al.  Angular Path Integration by Moving “Hill of Activity”: A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System , 2005, The Journal of Neuroscience.

[18]  Haojiang Luan,et al.  Refined Spatial Manipulation of Neuronal Function by Combinatorial Restriction of Transgene Expression , 2006, Neuron.

[19]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[20]  J. Taube The head direction signal: origins and sensory-motor integration. , 2007, Annual review of neuroscience.

[21]  D. Tank,et al.  Functional dissection of circuitry in a neural integrator , 2007, Nature Neuroscience.

[22]  Michael H. Dickinson,et al.  A modular display system for insect behavioral neuroscience , 2008, Journal of Neuroscience Methods.

[23]  Michael E Hasselmo,et al.  Persistent Firing Supported by an Intrinsic Cellular Mechanism in a Component of the Head Direction System , 2009, The Journal of Neuroscience.

[24]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[25]  Evan S. Schaffer,et al.  Inhibitory Stabilization of the Cortical Network Underlies Visual Surround Suppression , 2009, Neuron.

[26]  Michael B. Reiser,et al.  Two-photon calcium imaging from motion-sensitive neurons in head-fixed Drosophila during optomotor walking behavior , 2010, Nature Methods.

[27]  M. Dickinson,et al.  Active flight increases the gain of visual motion processing in Drosophila , 2010, Nature Neuroscience.

[28]  G. Rubin,et al.  Refinement of Tools for Targeted Gene Expression in Drosophila , 2010, Genetics.

[29]  Eric I. Knudsen,et al.  Global Inhibition and Stimulus Competition in the Owl Optic Tectum , 2010, The Journal of Neuroscience.

[30]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

[31]  J. Knierim,et al.  Attractor dynamics of spatially correlated neural activity in the limbic system. , 2012, Annual review of neuroscience.

[32]  Rachel I. Wilson Early olfactory processing in Drosophila: mechanisms and principles. , 2013, Annual review of neuroscience.

[33]  Ann-Shyn Chiang,et al.  A comprehensive wiring diagram of the protocerebral bridge for visual information processing in the Drosophila brain. , 2013, Cell reports.

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

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

[36]  Alexander Borst,et al.  Object tracking in motion-blind flies , 2013, Nature Neuroscience.

[37]  A. Compte,et al.  Bump attractor dynamics in prefrontal cortex explains behavioral precision in spatial working memory , 2014, Nature Neuroscience.

[38]  D. Tank,et al.  Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields , 2014, Nature Neuroscience.

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

[40]  Michael Häusser,et al.  Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo , 2014, Nature Methods.

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

[42]  A. Borst,et al.  Common circuit design in fly and mammalian motion vision , 2015, Nature Neuroscience.

[43]  G. Buzsáki,et al.  Internally-organized mechanisms of the head direction sense , 2015, Nature Neuroscience.

[44]  G. Rubin,et al.  Neuroarchitecture and neuroanatomy of the Drosophila central complex: A GAL4-based dissection of protocerebral bridge neurons and circuits , 2014, The Journal of comparative neurology.

[45]  Rishidev Chaudhuri,et al.  Computational principles of memory , 2016, Nature Neuroscience.

[46]  Benjamin L. de Bivort,et al.  Ring Attractor Dynamics Emerge from a Spiking Model of the Entire Protocerebral Bridge , 2016, bioRxiv.