Synchrony makes neurons fire in sequence, and stimulus properties determine who is ahead

Journal of Neuroscience

Volumn 31, Issue 23, 2011, Pages 8570-8584

  Havenith, Martha N ^a   Yu, Shan ^a   Biederlack, Julia ^a   Chen, Nan Hui ^b   Singer, Wolf ^a,c   Nikolic, Danko ^a,c  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b KUNMING INSTITUTE OF ZOOLOGY   (China)

^c FRANKFURT INSTITUTE FOR ADVANCED STUDIES   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; BETA OSCILLATION; CELL ACTIVITY; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; GAMMA OSCILLATION; HIPPOCAMPUS; NERVE CELL; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; STIMULUS RESPONSE; VISUAL CORTEX; VISUAL STIMULATION;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CATS; ELECTROPHYSIOLOGY; FEMALE; MALE; NEURONS; ORIENTATION; PHOTIC STIMULATION; VISUAL CORTEX;

EID: 79958246849     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2817-10.2011     Document Type: Article

References (60)

1. Ahissar E, Arieli A (2001) Figuring space by time. Neuron 32:185-201.
2. Alonso JM, Martinez LM (1998) Functional connectivity between simple cells and complex cells in cat striate cortex. Nat Neurosci 1:395-403.
3. Azouz R, Gray CM (2003) Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37:513-523.
4. Berényi A, Benedek G, Nagy A (2007) Double sliding-window technique: a new method to calculate the neuronal response onset latency. Brain Res 1178:141-148.
5. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynap-tic cell type. J Neurosci 18:10464-10472.
6. Biederlack J, Castelo-Branco M, Neuenschwander S, Wheeler DW, Singer W, Nikolić D (2006) Brightness induction: rate enhancement and neuronal synchronization as complementary codes. Neuron 52:1073-1083.
7. Branco T, Clark BA, Häusser M (2010) Dendritic discrimination of temporal input sequences in cortical neurons. Science 329:1671-1675.
8. Brody CD (1999) Correlations without synchrony. Neural Comput 11:1537-1551.
9. Buzsáki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neu-robiol 5:504-510.
10. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663-667.
11. 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.
12. Dragoi G, Buzsáki G (2006) Temporal encoding of place sequences by hip-pocampal cell assemblies. Neuron 50:145-157.
13. Dunn OJ (1961) Multiple comparisons among means. J Am Stat Assoc 56:52-57.
14. Engel AK, König P, Kreiter AK, Singer W (1991) Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 252:1177-1179.
15. Fries P, Nikolić D, Singer W (2007) The gamma cycle. Trends Neurosci 30:309-316.
16. Geisler C, Robbe D, Zugaro M, Sirota A, Buzsáki G (2007) Hippocampal place cell assemblies are speed-controlled oscillators. Proc Natl Acad Sci USA 104:8149-8154.
17. Gollisch T, Meister M (2008) Rapid neural coding in the retina with relative spike latencies. Science 319:1108-1111.
18. Gray CM, König P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334-337.
19. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurkó A, Buzsáki G (2002) Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417:738-741.
20. Harvey CD, Collman F, Dombeck DA, Tank DW (2009) Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461:941-946.
21. Hausselt SE, Euler T, Detwiler PB, Denk W (2007) A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biol 5:e185.
22. Havenith MN, Zemmar A, Yu S, Baudrexel SM, Singer W, Nikolić D (2009) Measuring sub-millisecond delays in spiking activity with millisecond time-bins. Neurosci Lett 450:296-300.
23. Heil P (2004) First-spike latency of auditory neurons revisited. Curr Opin Neurobiol 14:461-467.
24. Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160:106-154.
25. Jensen O, Kaiser J, Lachaux JP (2007) Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci 30: 317-324.
26. Johansson RS, Birznieks I (2004) First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 7:170-177.
27. Kayser C, Montemurro MA, Logothetis NK, Panzeri S (2009) Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 61:597-608.
28. Koepsell K, Wang X, Vaingankar V, Wei Y, Wang Q, Rathbun DL, Usrey WM, Hirsch JA, Sommer FT (2009) Retinal oscillations carry visual information to cortex. Front Syst Neurosci 3:4.
29. König P (1994) A method for the quantification of synchrony and oscillatory properties of neuronal activity. J Neurosci Methods 54:31-37.
30. König P, Engel AK, Singer W (1995a) Relation between oscillatory activity and long-range synchronization in cat visual cortex. Proc Natl Acad Sci USA 92:290-294.
31. König P, Engel AK, Roelfsema PR, Singer W (1995b) How precise is neuro-nal synchronization? Neural Comput 7:469-485.
32. London M, Häusser M (2005) Dendritic computation. Annu Rev Neurosci 28:503-532.
33. Magee JC (2001) Dendritic mechanisms of phase precession in hippocam-pal CA1 pyramidal neurons. J Neurophysiol 86:528-532.
34. Maldonado PE, Friedman-Hill S, Gray CM (2000) Dynamics of striate cortical activity in the alert macaque: II. Fast time scale synchronization. Cereb Cortex 10:1117-1131.
35. Mehta MR, Lee AK, Wilson MA (2002) Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417:741-746.
36. Meliza CD, Dan Y (2006) Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking. Neuron 49:183-189.
37. Movshon JA, Thompson ID, Tolhurst DJ (1978a) Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J Physiol 283:53-77.
38. Movshon JA, Thompson ID, Tolhurst DJ (1978b) Spatial and temporal contrast sensitivityofneuronesinareas17and 18ofthe cat's visual cortex. J Physiol 283:101-120.
39. Muresan RC, Jurjut OF, Moca VV, Singer W, Nikolić D (2008) The oscillation score: an efficient method for estimating oscillation strength in neu-ronal activity. J Neurophysiol 99:1333-1353.
40. Nikolić D (2007) Non-parametric detection of temporal order across pair-wise measurements of time delays. J Comput Neurosci 22:5-19.
41. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
42. Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys J 7:419-440.
43. Rodriguez R, Kallenbach U, Singer W, Munk MH (2010) Stabilization of visual responses through cholinergic activation. Neuroscience 165: 944-954.
44. Roelfsema PR, Engel AK, König P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385:157-161.
45. Schneider G, Nikolić D (2006) Detection and assessmentofnear-zero delays in neuronal spiking activity. J Neurosci Methods 152:97-106.
46. Schneider G, Havenith MN, Nikolić D (2006) Spatiotemporal structure in large neuronal networks detected from cross-correlation. Neural Comput 18:2387-2413.
47. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870-3896.
48. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.
49. Skottun BC, De Valois RL, Grosof DH, Movshon JA, Albrecht DG, Bonds AB (1991) Classifying simple and complex cells on the basis of response modulation. Vision Res 31:1079-1086.
50. Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334-350.
51. Tallon-Baudry C (2009) The roles of gamma-band oscillatory synchrony in human visual cognition. Front Biosci 14:321-332.
52. Tiesinga P, Fellous JM, Sejnowski TJ (2008) Regulation of spike timing in visual cortical circuits. Nat Rev Neurosci 9:97-107.
53. Tsubo Y, Takada M, Reyes AD, Fukai T (2007) Layer and frequency dependencies of phase response properties of pyramidal neurons in rat motor cortex. Eur J Neurosci 25:3429-3441.
54. Usrey WM, Alonso JM, Reid RC (2000) Synaptic interactions between tha-lamic inputs to simple cells in cat visual cortex. J Neurosci 20:5461-5467.
55. VanRullen R, Guyonneau R, Thorpe SJ (2005) Spike times make sense. Trends Neurosci 28:1-4.
56. Vinck M, Lima B, Womelsdorf T, Oostenveld R, Singer W, Neuenschwander S, Fries P (2010) Gamma-phase shifting in awake monkey visual cortex. J Neurosci 30:1250-1257.
57. Womelsdorf T, Fries P (2007) The role of neuronal synchronization in selective attention. Curr Opin Neurobiol 17:154-160.
58. Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007) Modulationof neuronal interactions through neuro-nal synchronization. Science 316:1609-1612.
59. Yao H, Dan Y (2001) Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron 32:315-323.
60. Yao H, Shen Y, Dan Y (2004) Intracortical mechanism of stimulus-timing-dependent plasticity in visual cortical orientation tuning. Proc Natl Acad Sci USA 101:5081-5086.