Nonlinear computations underlying temporal and population sparseness in the auditory system of the grasshopper

Journal of Neuroscience

Volumn 32, Issue 29, 2012, Pages 10053-10062

  Clemens, Jan ^a,b   Wohlgemuth, Sandra ^a,c   Ronacher, Bernhard ^a,b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b BERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCE   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTIC NERVE FIBER; ADAPTATION; AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; AUDITORY SYSTEM; COMPUTER MODEL; ELECTROPHYSIOLOGY; GRASSHOPPER; LOCUST; MALE; NONHUMAN; PRIORITY JOURNAL; SPIKE;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY PATHWAYS; COMPUTER SIMULATION; GRASSHOPPERS; MODELS, NEUROLOGICAL; NEURONS;

EID: 84863908478     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5911-11.2012     Document Type: Article

References (48)

1. Assisi C, Stopfer M, Laurent G, Bazhenov M (2007) Adaptive regulation of sparseness by feedforward inhibition. Nat Neurosci 10:1176-1184.
2. Atencio CA, Sharpee TO, Schreiner CE (2008) Cooperative nonlinearities in auditory cortical neurons. Neuron 58:956-966.
3. Barlow H (2001) Redundancy reduction revisited. Network 12:241-253.
4. Benda J, Bethge M, Hennig RM, Pawelzik KR, Herz AVM (2001) Spikefrequency adaptation: phenomenological model and experimental tests. Neurocomputing 38:105-110.
5. Borst A, Flanagin VL, Sompolinsky H (2005) Adaptation without parameter change: dynamic gain control in motion detection. Proc Natl Acad Sci U S A 102:6172-6176.
6. Brenner N, Bialek W, de Ruyter van Steveninck R (2000) Adaptive rescaling maximizes information transmission. Neuron 26:695-702.
7. Chacron MJ, Longtin A, Maler L (2011) Efficient computation via sparse coding in electrosensory neural networks. Curr Opin Neurobiol 21:752-760.
8. Clemens J, Kutzki O, Ronacher B, Schreiber S, Wohlgemuth S (2011) Efficient transformation of an auditory population code in a small sensory system. Proc Natl Acad Sci U S A 108:13812-13817.
9. Creutzig F, Wohlgemuth S, Stumpner A, Benda J, Ronacher B, Herz AV (2009) Timescale-invariant representation of acoustic communication signals by a bursting neuron. J Neurosci 29:2575-2580.
10. Desbordes G, Jin J, Weng C, Lesica NA, Stanley GB, Alonso JM (2008) Timing precision in population coding of natural scenes in the early visual system. PLoS Biol 6:e324+.
11. Dimitrov AG, Gedeon T (2006) Effects of stimulus transformations on estimates of sensory neuron selectivity. J Comput Neurosci 20:265-283.
12. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412:787-792.
13. Fairhall AL, Burlingame CA, Narasimhan R, Harris RA, Puchalla JL, Berry MJ 2nd (2006) Selectivity for multiple stimulus features in retinal ganglion cells. J Neurophysiol 96:2724-2738.
14. Farkhooi F, Muller E, Nawrot MP (2009) Sequential sparsing by successive adapting neural populations. BMC Neurosci 10 [Suppl I]:O10.
15. Fitzgerald JD, Sincich LC, Sharpee TO (2011) Minimal models of multidimensional computations. PLoS Comput Biol 7:e1001111.
16. Fox JL, Fairhall AL, Daniel TL (2010) Encoding properties of haltere neurons enable motion feature detection in a biological gyroscope. Proc Natl Acad Sci U S A 107:3840-3845.
17. George AA, Lyons-Warren AM, Ma X, Carlson BA (2011) A diversity of synaptic filters are created by temporal summation of excitation and inhibition. J Neurosci 31:14721-14734.
18. Gollisch T, Schütze H, Benda J, Herz AV (2002) Energy integration describes sound-intensity coding in an insect auditory system. J Neurosci 22:10434-10448.
19. Hildebrandt KJ, Benda J, Hennig RM (2009) The origin of adaptation in the auditory pathway of locusts is specific to cell type and function. J Neurosci 29:2626-2636.
20. Houghton C (2009) Studying spike trains using a van Rossum metric with a synapse-like filter. J Comput Neurosci 26:149-155.
21. Kim AJ, Lazar AA, Slutskiy YB (2011) System identification of Drosophila olfactory sensory neurons. J Comput Neurosci 30:143-161.
22. Lundstrom BN, Higgs MH, Spain WJ, Fairhall AL (2008) Fractional differentiation by neocortical pyramidal neurons. Nat Neurosci 11:1335-1342.
23. Luo SX, Axel R, Abbott LF (2010) Generating sparse and selective thirdorder responses in the olfactory system of the fly. Proc Natl Acad SciU S A 107:10713-10718.
24. Machens CK, Stemmler MB, Prinz P, Krahe R, Ronacher B, Herz AV (2001) Representation of acoustic communication signals by insect auditory receptor neurons. J Neurosci 21:3215-3227.
25. Nawrot MP (2012) Dynamics of sensory processing in the dual olfactory pathway of the honeybee. Apidologie 43:1-23.
26. Neuhofer D, Wohlgemuth S, Stumpner A, Ronacher B (2008) Evolutionarily conserved coding properties of auditory neurons across grasshopper species. Proc R Soc B 275:1965-1974.
27. Olshausen BA, Field DJ (2004) Sparse coding of sensory inputs. Curr Opin Neurobiol 14:481-487.
28. Osborne LC, Palmer SE, Lisberger SG, Bialek W (2008) The neural basis for combinatorial coding in a cortical population response. J Neurosci 28:13522-13531.
29. Papadopoulou M, Cassenaer S, Nowotny T, Laurent G (2011) Normalization for sparse encoding of odors by a wide-field interneuron. Science 332:721-725.
30. Petersen RS, Brambilla M, Bale MR, Alenda A, Panzeri S, Montemurro MA, Maravall M (2008) Diverse and temporally precise kinetic feature selectivity in the VPm thalamic nucleus. Neuron 60:890-903.
31. Pitkow X, Meister M (2012) Decorrelation and efficient coding by retinal ganglion cells. Nat Neurosci 15:628-635.
32. Rokem A, Watzl S, Gollisch T, Stemmler M, Herz AV, Samengo I (2006) Spike-timing precision underlies the coding efficiency of auditory receptor neurons. J Neurophysiol 95:2541-2552.
33. Römer H, Marquart V (1984) Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust. J Comp Phys A 155:249-262.
34. Ronacher B, Stumpner A (1988) Filtering of behaviourally relevant temporal parameters of a grasshopper's song by an auditory interneuron. J Comp Phys A 163:517-523.
35. Rust NC, Schwartz O, Movshon JA, Simoncelli EP (2005) Spatiotemporal elements of macaque v1 receptive fields. Neuron 46:945-956.
36. Schmuker M, Schneider G (2007) Processing and classification of chemical data inspired by insect olfaction. Proc Natl Acad Sci U S A 104:20285-20289.
37. Schneidman E, Puchalla JL, Segev R, Harris RA, Bialek W, Berry MJ 2nd (2011) Synergy from silence in a combinatorial neural code. J Neurosci 31:15732-15741.
38. Schwartz O, Pillow JW, Rust NC, Simoncelli EP (2006) Spike-triggered neural characterization. J Vis 6:484-507.
39. Sharpee TO, Nagel KI, Doupe AJ (2011) Two-dimensional adaptation in the auditory forebrain. J Neurophysiol 106:1841-1861.
40. Slee SJ, Higgs MH, Fairhall AL, Spain WJ (2005) Two-dimensional time coding in the auditory brainstem. J Neurosci 25:9978-9988.
41. Stumpner A (1989) Physiological variability of auditory neurons in a grasshopper. Naturwissenschaften 76:427-429.
42. Stumpner A, Ronacher B (1991) Auditory interneurones in the metathoracic ganglion of the grasshopper Chorthippus biguttulus: I. Morphological and physiological characterization. J Exp Biol 158:391-410.
43. Tripp BP, Eliasmith C (2010) Population models of temporal differentiation. Neural Comput 22:621-659.
44. Vogel A, Hennig RM, Ronacher B (2005) Increase of neuronal response variability at higher processing levels as revealed by simultaneous recordings. J Neurophysiol 93:3548-3559.
45. Wang XJ, Liu Y, Sanchez-Vives MV, McCormick DA (2003) Adaptation and temporal decorrelation by single neurons in the primary visual cortex. J Neurophysiol 89:3279-3293.
46. Wiechert MT, Judkewitz B, Riecke H, Friedrich RW (2010) Mechanisms of pattern decorrelation by recurrent neuronal circuits. Nat Neurosci 13:1003-1010.
47. Willmore BD, Tolhurst DJ (2001) Characterizing the sparseness of neural codes. Network 12:255-270.
48. Willmore BD, Mazer JA, Gallant JL (2011) Sparse coding in striate and extrastriate visual cortex. J Neurophysiol 105:2907-2919.