Ring attractor dynamics emerge from a spiking model of the entire protocerebral bridge

Frontiers in Behavioral Neuroscience

Volumn 11, Issue , 2017, Pages

  Kakaria, Kyobi S ^a   De Bivort, Benjamin L ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Central complex; Circuit model; Egocentric navigation; Ellipsoid body; Fan shaped body; Leaky integrate and fire model; Protocerebral bridge; Ring attractor

Indexed keywords

CALCIUM ION;

ACTION POTENTIAL; ARTICLE; BRAIN DEPTH STIMULATION; CONNECTOME; CONTROLLED STUDY; ELLIPSOID BODY; FIRING RATE; NERVE CELL NETWORK; NERVOUS SYSTEM; NERVOUS SYSTEM FUNCTION; OPTOGENETICS; PHENOTYPE; PREDICTION; PROBABILITY; PROTOCEREBRAL BRIDGE; RING ATTRACTOR DYNAMICS; SENSITIVITY ANALYSIS; SENSORY STIMULATION; SIMULATION; SPIKE WAVE; SYNAPSE;

EID: 85014044844     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2017.00008     Document Type: Article

References (57)

1. Arena, P., Maceo, S., and Patane, L. (2013). ‘‘A spiking network for spatial memory formation: towards a fly-inspired ellipsoid body model,’’ in Neural Networks (IJCNN), The 2013 International Joint Conference, (Dallas, TX).
2. Ayroles, J. F., Buchanan, S. M., O’Leary, C., Skutt-Kakaria, K., Grenier, J. K., Clark, A. G., et al. (2015). Behavioral idiosyncrasy reveals genetic control of phenotypic variability. Proc. Natl. Acad. Sci. U S A 112, 6706–6711. doi: 10.1073/pnas.1503830112
3. Berger, S. D., and Crook, S. M. (2015). Modeling the influence of ion channels on neuron dynamics in Drosophila. Front. Comput. Neurosci. 9:139. doi: 10.3389/fncom.2015.00139
4. de Bivort, B. L., and van Swinderen, B. (2016). Evidence for selective attention in the insect brain. Curr. Opin. Insect Sci. 15, 9–15. doi: 10.1016/j.cois.2016. 02.007
5. Bockhorst, T., and Homberg, U. (2015). Amplitude and dynamics of polarization-plane signaling in the central complex of the locust brain. J. Neurophysiol. 113, 3291–3311. doi: 10.1152/jn.00742.2014
6. Buchanan, S. M., Kain, J. S., and de Bivort, B. L. (2015). Neuronal control of locomotor handedness in Drosophila. Proc. Natl. Acad. Sci. U S A 112, 6700–6705. doi: 10.1073/pnas.1500804112
7. Chou, Y. H., Spletter, M. L., Yaksi, E., Leong, J. C., Wilson, R. I., and Luo, L. (2010). Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat. Neurosci. 13, 439–449. doi: 10.1038/nn.2489
8. Collett, T. S., and Graham, P. (2004). Animal navigation: path integration, visual landmarks and cognitive maps. Curr. Biol. 14, R475–R477. doi: 10.1016/j.cub. 2004.06.013
9. Daniels, R. W., Gelfand, M. V., Collins, C. A., and DiAntonio, A. (2008). Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS. J. Comp. Neurol. 508, 131–152. doi: 10.1002/cne.21670
10. Domenici, P., Booth, D., Blagburn, J. M., and Bacon, J. P. (2008). Cockroaches keep predators guessing by using preferred escape trajectories. Curr. Biol. 18, 1792–1796. doi: 10.1016/j.cub.2008.09.062
11. Etienne, A. S., and Jeffery, K. J. (2004). Path integration in mammals. Hippocampus 14, 180–192. doi: 10.1002/hipo.10173
12. Feinberg, E. H., Vanhoven, M. K., Bendesky, A., Wang, G., Fetter, R. D., Shen, K., et al. (2008). GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57, 353–363. doi: 10.1016/j.neuron.2007.11.030
13. Fişek, M., and Wilson, R. I. (2014). Stereotyped connectivity and computations in higher-order olfactory neurons. Nat. Neurosci. 17, 280–288. doi: 10.1038/nn.3613
14. Fruchterman, T. M. J., and Reingold, E. M. (1990). Graph Drawing by Force-Directed Placement. Urbana, IL: University of Illinois at Urbana-Champaign.
15. Gaudry, Q., Hong, E. J., Kain, J., de Bivort, B. L., and Wilson, R. I. (2013). Asymmetric neurotransmitter release enables rapid odour lateralization in Drosophila. Nature 493, 424–428. doi: 10.1038/nature11747
16. Gouwens, N. W., and Wilson, R. I. (2009). Signal propagation in Drosophila central neurons. J. Neurosci. 29, 6239–6249. doi: 10.1523/JNEUROSCI.0764-09.2009
17. Guo, P., and Ritzmann, R. E. (2013). Neural activity in the central complex of the cockroach brain is linked to turning behaviors. J. Exp. Biol. 216, 992–1002. doi: 10.1242/jeb.080473
18. Haferlach, T., Wessnitzer, J., Mangan, M., and Webb, B. (2007). Evolving a neural model of insect path integration. Adapt. Behav. 15, 273–287. doi: 10.1177/1059712307082080
19. Heinze, S. (2014). ‘‘Polarized-light processing in insect brains: recent insights from the desert locust, the monarch butterfly, the cricket and the fruit fly,’’ in Polarized Light and Polarization Vision in Animal Sciences, ed. G. Horváth (New York, NY: Springer Berlin Heidelberg), 61–111.
20. Heinze, S., and Homberg, U. (2007). Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315, 995–997. doi: 10.1126/science.1135531
21. Hodgkin, A. L., and Huxley, A. F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500–544. doi: 10.1113/jphysiol.1952.sp004764
22. Homberg, U., Heinze, S., Pfeiffer, K., Kinoshita, M., and el Jundi, B. (2011). Central neural coding of sky polarization in insects. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 680–687. doi: 10.1098/rstb.2010.0199
23. Kahsai, L., Carlsson, M. A., Winther, A. M., and Nässel, D. R. (2012). Distribution of metabotropic receptors of serotonin, dopamine, GABA, glutamate and short neuropeptide F in the central complex of Drosophila. Neuroscience 208, 11–26. doi: 10.1016/j.neuroscience.2012.02.007
24. Kahsai, L., and Winther, Å. M. E. (2011). Chemical neuroanatomy of the Drosophila central complex: distribution of multiple neuropeptides in relation to neurotransmitters. J. Comp. Neurol. 519, 290–315. doi: 10.1002/cne. 22520
25. Kasthuri, N., Hayworth, K. J., Berger, D. R., Schalek, R. L., Conchello, J. A., Knowles-Barley, S., et al. (2015). Saturated reconstruction of a volume of neocortex. Cell 162, 648–661. doi: 10.1016/j.cell.2015.06.054
26. Kim, A. J., Fitzgerald, J. K., and Maimon, G. (2015). Cellular evidence for efference copy in Drosophila visuomotor processing. Nat. Neurosci. 18, 1247–1255. doi: 10.1038/nn.4083
27. Knierim, J. J., and Zhang, K. (2012). Attractor dynamics of spatially correlated neural activity in the limbic system. Annu. Rev. Neurosci. 35, 267–285. doi: 10.1146/annurev-neuro-062111-150351
28. Kottler, B., Fiore, V. G., Ludlow, Z. N., Buhl, E., Vinatier, G., Faville, R., et al. (2017). A lineage-related reciprocal inhibition circuitry for sensory-motor action selection. BioRxiv doi: 10.1101/100420 [Epub ahead of print].
29. Lin, C.-Y., Chuang, C.-C., Hua, T.-E., Chen, C.-C., Dickson, B. J., Greenspan, R. J., et al. (2013). A comprehensive wiring diagram of the protocerebral bridge for visual information processing in the Drosophila brain. Cell Rep. 3, 1739–1753. doi: 10.1016/j.celrep.2013.04.022
30. Liu, W. W., and Wilson, R. I. (2013). Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system. Proc. Natl. Acad. Sci. U S A 110, 10294–10299. doi: 10.1073/pnas.1220560110
31. Marder, E. (2011). Variability, compensation and modulation in neurons and circuits. Proc. Natl. Acad. Sci. U S A 108, 15542–15548. doi: 10.1073/pnas. 1010674108
32. Martín-Peña, A., Acebes, A., Rodríguez, J.-R., Chevalier, V., Casas-Tinto, S., Triphan, T., et al. (2014). Cell types and coincident synapses in the ellipsoid body of Drosophila. Eur. J. Neurosci. 39, 1586–1601. doi: 10.1111/ejn. 12537
33. McNaughton, B. L., Chen, L. L., and Markus, E. J. (2007). ‘‘Dead reckoning,’’ landmark learning and the sense of direction: a neurophysiological and computational hypothesis. J. Cogn. Neurosci. 3, 190–202. doi: 10.1162/jocn. 1991.3.2.190
34. Mu, L., Ito, K., Bacon, J. P., and Strausfeld, N. J. (2012). Optic glomeruli and their inputs in Drosophila share an organizational ground pattern with the antennal lobes. J. Neurosci. 32, 6061–6071. doi: 10.1523/JNEUROSCI.0221-12.2012
35. Nagel, K. I., Hong, E. J., and Wilson, R. I. (2015). Synaptic and circuit mechanisms promoting broadband transmission of olfactory stimulus dynamics. Nat. Neurosci. 18, 56–65. doi: 10.1038/nn.3895
36. Nern, A., Pfeiffer, B. D., and Rubin, G. M. (2015). Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proc. Natl. Acad. Sci. U S A 112, E2967–E2976. doi: 10.1073/pnas. 1506763112
37. Ofstad, T. A., Zuker, C. S., and Reiser, M. B. (2011). Visual place learning in Drosophila melanogaster. Nature 474, 204–207. doi: 10.1038/nature 10131
38. Pereda, A. E. (2014). Electrical synapses and their functional interactions with chemical synapses. Nat. Rev. Neurosci. 15, 250–263. doi: 10.1038/nrn3708
39. Pfeiffer, K., and Homberg, U. (2014). Organization and functional roles of the central complex in the insect brain. Annu. Rev. Entomol. 59, 165–184. doi: 10.1146/annurev-ento-011613-162031
40. Pimentel, D., Donlea, J. M., Talbot, C. B., Song, S. M., Thurston, A. J. F., and Miesenböck, G. (2016). Operation of a homeostatic sleep switch. Nature 536, 333–337. doi: 10.1038/nature19055
41. Ratté, S., Hong, S., De Schutter, E., and Prescott, S. A. (2013). Impact of neuronal properties on network coding: roles of spike initiation dynamics and robust synchrony transfer. Neuron 78, 758–772. doi: 10.1016/j.neuron.2013.05.030
42. Rohrbough, J., and Broadie, K. (2002). Electrophysiological analysis of synaptic transmission in central neurons of Drosophila larvae. J. Neurophysiol. 88, 847–860. doi: 10.1152/jn.01010.2001
43. Rolls, M. M. (2011). Neuronal polarity in Drosophila: sorting out axons and dendrites. Dev. Neurobiol. 71, 419–429. doi: 10.1002/dneu.20836
44. Schneider-Mizell, C. M., Gerhard, S., Longair, M., Kazimiers, T., Li, F., Zwart, M. F., et al. (2016). Quantitative neuroanatomy for connectomics in Drosophila. Elife 5:e12059. doi: 10.7554/eLife.12059
45. Seelig, J. D., and Jayaraman, V. (2013). Feature detection and orientation tuning in the Drosophila central complex. Nature 503, 262–266. doi: 10.1038/nature12601
46. Seelig, J. D., and Jayaraman, V. (2015). Neural dynamics for landmark orientation and angular path integration. Nature 521, 186–191. doi: 10.1038/nature14446
47. Sheeba, V., Gu, H., Sharma, V. K., O’Dowd, D. K., and Holmes, T. C. (2008). Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J. Neurophysiol. 99, 976–988. doi: 10.1152/jn.00930.2007
48. Skaggs, W., Knierim, W., Kudrimoti, H. S., and McNaughton, B. L. (1995). ‘‘A model of the neural basis of the rat’s sense of direction,’’ in Advances in Neural Information Processing Systems, (Vol. 7) eds G. Tesauro, D. S. Touretzky and T. K. Leen, (Cambridge, MA: MIT Press), 173–180.
49. Solovyeva, K. P., Karandashev, I. M., Zhavoronkov, A., and Dunin-Barkowski, W. L. (2016). Models of innate neural attractors and their applications for neural information processing. Front. Syst. Neurosci. 9:178. doi: 10.3389/fnsys.2015.00178
50. Song, P., and Wang, X.-J. (2005). Angular path integration by moving ‘‘hill of activity’’: A spiking neuron model without recurrent excitation of the head-direction system. J. Neurosci. 25, 1002–1014. doi: 10.1523/JNEUROSCI. 4172-04.2005
51. Stein, R. B. (1967). Some models of neuronal variability. Biophys. J. 7, 37–68. doi: 10.1016/s0006-3495(67)86574-3
52. Strausfeld, N. J. (1976). ‘‘The primary compartments of the brain,’’ in Atlas of an Insect Brain, ed. N. J. Strausfeld (New York, NY: Springer Berlin Heidelberg), 31–40.
53. Taube, J. S. (2007). The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181–207. doi: 10.1146/annurev.neuro.29. 051605.112854
54. Varga, A. G., and Ritzmann, R. E. (2016). Cellular basis of head direction and contextual cues in the insect brain. Curr. Biol. 26, 1816–1828. doi: 10.1016/j. cub.2016.05.037
55. Weir, P. T., and Dickinson, M. H. (2015). Functional divisions for visual processing in the central brain of flying Drosophila. Proc. Natl. Acad. Sci. U S A 112, E5523–E5532. doi: 10.1073/pnas.1514415112
56. Wolff, T., Iyer, N. A., and Rubin, G. M. (2015). Neuroarchitecture and neuroanatomy of the Drosophila central complex: a GAL4-based dissection of protocerebral bridge neurons and circuits. J. Comp. Neurol. 523, 997–1037. doi: 10.1002/cne.23705
57. Zhang, K. (1996). Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 16, 2112–2126.