Disentangling the functional consequences of the connectivity between optic-flow processing neurons

Nature Neuroscience

Volumn 15, Issue 3, 2012, Pages 441-448

  Weber, Franz ^a,b   Machens, Christian K ^c,d   Borst, Alexander ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d CHAMPALIMAUD FOUNDATION   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CALLIPHORIDAE; NONHUMAN; OPTIC FLOW; PRIORITY JOURNAL; SENSORY NERVE CELL; SENSORY STIMULATION; SIGNAL NOISE RATIO; SPIKE WAVE; STIMULUS RESPONSE;

ACTION POTENTIALS; ANIMALS; DIPTERA; LINEAR MODELS; MODELS, NEUROLOGICAL; OPTIC FLOW; ROTATION; SENSORY RECEPTOR CELLS; SIGNAL-TO-NOISE RATIO; VISUAL FIELDS; VISUAL PATHWAYS;

EID: 84857649949     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3044     Document Type: Article

References (48)

1. Gilbert, C. D. & Wiesel, T. N. Intrinsic connectivity and receptive field properties in visual cortex. Vision Res. 25, 365-374 (1985).
2. DeVries, S. H. & Baylor, D. A. Synaptic circuitry of the retina and olfactory bulb. Cell 72(suppl.) 139-149 (1993).
3. Nassi, J. J. & Callaway, E. M. Parallel processing strategies of the primate visual system. Nat. Rev. Neurosci. 10, 360-372 (2009).
4. Borst, A., Haag, J. & Reiff, D. F. Fly motion vision. Annu. Rev. Neurosci. 33, 49-70 (2010).
5. Read, H. L., Winer, J. A. & Schreiner, C. E. Functional architecture of auditory cortex. Curr. Opin. Neurobiol. 12, 433-440 (2002).
6. Averbeck, B. B., Latham, P. E. & Pouget, A. Neural correlations, population coding and computation. Nat. Rev. Neurosci. 7, 358-366 (2006).
7. Usrey, W. M. & Reid, R. C. Synchronous activity in the visual system. Annu. Rev. Physiol. 61, 435-456 (1999).
8. Tkacik, G., Prentice, J. S., Balasubramanian, V. & Schneidman, E. Optimal population coding by noisy spiking neurons. Proc. Natl. Acad. Sci. USA 107, 14419-14424 (2010).
9. Farrow, K., Borst, A. & Haag, J. Sharing receptive fields with your neighbors: tuning the vertical system cells to wide field motion. J. Neurosci. 25, 3985-3993 (2005).
10. Olsen, S. R., Bhandawat, V. & Wilson, R. I. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54, 89-103 (2007).
11. Olsen, S. R. & Wilson, R. I. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452, 956-960 (2008).
12. Cafaro, J. & Rieke, F. Noise correlations improve response fidelity and stimulus encoding. Nature 468, 964-967 (2010).
13. Hausen, K. The lobula-complex of the fly: structure, function and significance in visual behavior. in Photoreception and Vision in Invertebrates (ed. M. A. Ali) 523-559 (Plenum Press, New York, 1984).
14. Krapp, H. G. & Hengstenberg, R. Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384, 463-466 (1996).
15. Borst, A. & Weber, F. Neural action fields for optic flow based navigation: a simulation study of the fly lobula plate network. PLoS ONE 6, e16303 (2011).
16. Haag, J. & Borst, A. Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons. Nat. Neurosci. 7, 628-634 (2004).
17. Pillow, J. W. et al. Spatio-temporal correlations and visual signaling in a complete neuronal population. Nature 454, 995-999 (2008).
18. Okatan, M., Wilson, M. A. & Brown, E. N. Analyzing functional connectivity using a network likelihood model of ensemble neural spiking activity. Neural Comput. 17, 1927-1961 (2005).
19. Paninski, L., Pillow, J. & Lewi, J. Statistical models for neural encoding, decoding, and optimal stimulus design. Prog. Brain Res. 165, 493-507 (2007).
20. Beersma, D. G. M., Stavenga, D. G. & Kuiper, J. W. Retinal lattice, visual field and binocularities in flies. J. Comp. Physiol. [A] 119, 207-220 (1977).
21. Haag, J. & Borst, A. Reciprocal inhibitory connections within a neural network for rotational optic-flow processing. Front. Neurosci. 1, 111-121 (2007).
22. Haag, J. & Borst, A. Dendro-dendritic interactions between motion-sensitive largefield neurons in the fly. J. Neurosci. 22, 3227-3233 (2002).
23. Haag, J. & Borst, A. Orientation tuning of motion-sensitive neurons shaped by verticalhorizontal network interactions. J. Comp. Physiol. [A] 189, 363-370 (2003).
24. Borst, A. & Theunissen, F. E. Information theory and neural coding. Nat. Neurosci. 2, 947-957 (1999).
25. Reichardt, W. Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. in Principles of Sensory Communication (ed. W. A. Rosenblith) 303-317 (MIT Press and John Wiley & Sons, 1961).
26. Haag, J., Denk, W. & Borst, A. Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. Proc. Natl. Acad. Sci. USA 101, 16333-16338 (2004).
27. Gerwinn, S., Macke, J. H. & Bethge, M. Bayesian inference for generalized linear models for spiking neurons. Front. Comput. Neurosci. 4, 12 (2010).
28. Weber, F., Machens, C. K. & Borst, A. Spatiotemporal response properties of opticflow processing neurons. Neuron 67, 629-642 (2010).
29. Rieke, F., Bialek, W. & Warland, D. Spikes (Mit Press, 1999).
30. Machens, C. K. et al. Representation of acoustic communication signals by insect auditory receptor neurons. J. Neurosci. 21, 3215-3227 (2001).
31. Bialek, W., Rieke, F., de Ruyter van Steveninck, R. & Warland, D. Reading a neural code. Science 252, 1854-1857 (1991).
32. Bair, W., Zohary, E. & Newsome, W. T. Correlated firing in macaque visual area MT: time scales and relationship to behavior. J. Neurosci. 21, 1676-1697 (2001).
33. Zohary, E., Shadlen, M. N. & Newsome, W. T. Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370, 140-143 (1994).
34. Moore, G. P., Segundo, J. P., Perkel, D. H. & Levitan, H. Statistical signs of synaptic interaction in neurons. Biophys. J. 10, 876-900 (1970).
35. Kohn, A. & Smith, M. A. Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J. Neurosci. 25, 3661-3673 (2005).
36. Smith, M. A. & Kohn, A. Spatial and temporal scales of neuronal correlation in primary visual cortex. J. Neurosci. 28, 12591-12603 (2008).
37. Takeuchi, D., Hirabayashi, T., Tamura, K. & Miyashita, Y. Reversal of interlaminar signal between sensory and memory processing in monkey temporal cortex. Science 331, 1443-1447 (2011).
38. Brody, C. D. Correlations without synchrony. Neural Comput. 11, 1537-1551 (1999).
39. Cohen, M. R. & Kohn, A. Measuring and interpreting neuronal correlations. Nat. Neurosci. 14, 811-819 (2011).
40. de la Rocha, J., Doiron, B., Shea-Brown, E., Josic, K. & Reyes, A. Correlation between neural spike trains increases with firing rate. Nature 448, 802-806 (2007).
41. Cohen, M. R. & Maunsell, J. H. R. Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 12, 1594-1600 (2009).
42. Schneidman, E., Berry, M. J., Segev, R. & Bialek, W. Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440, 1007-1012 (2006).
43. Shlens, J. et al. The structure of multi-neuron firing patterns in primate retina. J. Neurosci. 26, 8254-8266 (2006).
44. Stevenson, I. H. & Kording, K. P. How advances in neural recording affect data analysis. Nat. Neurosci. 14, 139-142 (2011).
45. Nauhaus, I., Busse, L., Carandini, M. & Ringach, D. L. Stimulus contrast modulates functional connectivity in visual cortex. Nat. Neurosci. 12, 70-76 (2009).
46. Schilstra, C. & Hateren, J. H. Blowfly flight and optic flow. I. Thorax kinematics and flight dynamics. J. Exp. Biol. 202, 1481-1490 (1999).
47. Ko, H. et al. Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87-91 (2011).
48. Elyada, Y. M., Haag, J. & Borst, A. Different receptive fields in axons and dendrites underlie robust coding in motion-sensitive neurons. Nat. Neurosci. 12, 327-332 (2009).