Single neuron firing properties impact correlation-based population coding

Journal of Neuroscience

Volumn 32, Issue 4, 2012, Pages 1413-1428

  Hong, Sungho ^a   Ratté, Stéphanie ^b   Prescott, Steven A ^b   de Schutter, Erik ^a,c  

^a OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2, 3 QUINOXALINEDIONE; BICUCULLINE METHIODIDE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CORRELATION ANALYSIS; ELECTROPHYSIOLOGY; HIPPOCAMPUS; MALE; MATHEMATICAL MODEL; NERVE FUNCTION; NERVE STIMULATION; NEUROMODULATION; NEURON FIRING; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIMULATION; SPIKE;

ACTION POTENTIALS; ANIMALS; MALE; MODELS, NEUROLOGICAL; NEURONS; NORMAL DISTRIBUTION; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84856290193     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3735-11.2012     Document Type: Article

References (71)

1. Abeles M (1982) Role of the cortical neuron: integrator or coincidence detector? Isr J Med Sci 18:83-92.
2. Abeles M (1991) Corticonics: neural circuits of the cerebral cortex. Cambridge, MA: Cambridge UP.
3. Aertsen A, Diesmann M, Gewaltig MO (1996) Propagation of synchronous spiking activity in feedforward neural networks. J Physiol Paris 90:243-247.
4. Agmon-Snir H, Carr CE, Rinzel J (1998) The role of dendrites in auditory coincidence detection. Nature 393:268-272.
5. Arsiero M, Lüscher HR, Lundstrom BN, Giugliano M (2007) The impact of input fluctuations on the frequency-current relationships of layer 5 pyramidal neurons in the rat medial prefrontal cortex. J Neurosci 27:3274-3284.
6. Averbeck BB, Latham PE, Pouget A (2006) Neural correlations, population coding and computation. Nat Rev Neurosci 7:358-366.
7. Bair W, Zohary E, Newsome WT (2001) Correlated firing in macaque visual area MT: time scales and relationship to behavior. J Neurosci 21:1676-1697.
8. Barreiro AK, Shea-Brown E, Thilo EL (2010) Time scales of spike-train correlation for neural oscillators with common drive. Phys Rev E Stat Nonlin Soft Matter Phys 81:011916.
9. Bialek W, de Ruyter Van Steveninck RR (1988) Real-time performance of a movement-sensitive neuron in the blowfly visual system: coding and information transfer in short spike sequences. Proc R Soc Lond B Biol Sci 234:379-414.
10. Brown DA, Passmore GM (2009) Neural KCNQ (Kv7) channels. Br J Pharmacol 156:1185-1195.
11. Burak Y, Lewallen S, Sompolinsky H (2009) Stimulus-dependent correlations in threshold-crossing spiking neurons. Neural Comput 21:2269-2308.
12. Cafaro J, Rieke F (2010) Noise correlations improve response fidelity and stimulus encoding. Nature 468:964-967.
13. Cao XJ, Shatadal S, Oertel D (2007) Voltage-sensitive conductances of bushy cells of the mammalian ventral cochlear nucleus. J Neurophysiol 97:3961-3975.
14. Chialvo DR, Longtin A, Müller-Gerking J (1997) Stochastic resonance in models of neuronal ensembles. Phys Rev E Stat Nonlin Soft Matter Phys 55:1798-1808.
15. da Costa NM, Martin KA (2011) How thalamus connects to spiny stellate cells in the cat's visual cortex. J Neurosci 31:2925-2937.
16. de la Rocha J, Doiron B, Shea-Brown E, Josić K, Reyes A (2007) Correlation between neural spike trains increases with firing rate. Nature 448:802-806.
17. Destexhe A, Rudolph M, Fellous JM, Sejnowski TJ (2001) Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience 107:13-24.
18. Destexhe A, Rudolph M, Paré D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4:739-751.
19. Douglas RJ, Martin KA (2007) Mapping the matrix: the ways of neocortex. Neuron 56:226-238.
20. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420:173-178.
21. Engel AK, Roelfsema PR, Fries P, Brecht M, Singer W (1997) Role of the temporal domain for response selection and perceptual binding. Cereb Cortex 7:571-582.
22. Fellous JM, Rudolph M, Destexhe A, Sejnowski TJ (2003) Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 122:811-829.
23. Fourcaud-Trocmé N, Hansel D, van Vreeswijk C, Brunel N (2003) How spike generation mechanisms determine the neuronal response to fluctuating inputs. J Neurosci 23:11628-11640.
24. Gerstner W, Kreiter AK, Markram H, Herz AV (1997) Neural codes: firing rates and beyond. Proc Natl Acad Sci U S A 94:12740-12741.
25. Guan D, Higgs MH, Horton LR, Spain WJ, Foehring RC (2011) Contributions of Kv7-mediated potassium current to sub- and suprathreshold responses of rat layer II/III neocortical pyramidal neurons. J Neurophysiol 106:1722-1733.
26. Higgs MH, Slee SJ, Spain WJ (2006) Diversity of gain modulation by noise in neocortical neurons: regulation by the slow afterhyperpolarization conductance. J Neurosci 26:8787-8799.
27. Higley MJ, Contreras D (2006) Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci 26:448-457.
28. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
29. Hong S, Lundstrom BN, Fairhall AL (2008) Intrinsic gain modulation and adaptive neural coding. PLoS Comput Biol 4:e1000119.
30. Hu H, Vervaeke K, Storm JF (2007) M-channels (Kv7/KCNQ channels) that regulate synaptic integration, excitability, and spike pattern of CA1 pyramidal cells are located in the perisomatic region. J Neurosci 27:1853-1867.
31. König P, Engel AK, Singer W (1996) Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci 19:130-137.
32. Kremkow J, Aertsen A, Kumar A (2010) Gating of signal propagation in spiking neural networks by balanced and correlated excitation and inhibition. J Neurosci 30:15760-15768.
33. Kumar A, Rotter S, Aertsen A (2010) Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding. Nat Rev Neurosci 11:615-627.
34. Lundstrom BN, Hong S, Higgs MH, Fairhall AL (2008) Two computational regimes of a single-compartment neuron separated by a planar boundary in conductance space. Neural Comput 20:1239-1260.
35. Maex R, Vos BP, De Schutter E (2000) Weak common parallel fibre synapses explain the loose synchrony observed between rat cerebellar Golgi cells. J Physiol 523:175-192.
36. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268:1503-1506.
37. Manis PB, Marx SO (1991) Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci 11:2865-2880.
38. Mathews PJ, Jercog PE, Rinzel J, Scott LL, Golding NL (2010) Control of submillisecond synaptic timing in binaural coincidence detectors by Kv1 channels. Nat Neurosci 13:601-609.
39. Meister M, Berry MJ (1999) The neural code of the retina. Neuron 22:435-450.
40. Murphy BK, Miller KD (2009) Balanced amplification: a new mechanism of selective amplification of neural activity patterns. Neuron 61:635-648.
41. Ostojic S, Brunel N, Hakim V (2009) How connectivity, background activity, and synaptic properties shape the cross-correlation between spike trains. J Neurosci 29:10234-10253.
42. Palanca BJ, DeAngelis GC (2005) Does neuronal synchrony underlie visual feature grouping? Neuron 46:333-346.
43. Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys J 7:419-440.
44. Pinto RD, Elson RC, Szücs A, Rabinovich MI, Selverston AI, Abarbanel HD (2001) Extended dynamic clamp: controlling up to four neurons using a single desktop computer and interface. J Neurosci Methods 108:39-48.
45. Prescott SA, De Koninck Y (2009) Impact of background synaptic activity on neuronal response properties revealed by stepwise replication of in vivo-like conditions in vitro In: The dynamic clamp: from principles to applications (Destexhe A, Bal T, eds), pp 89-114. New York: Springer.
46. Prescott SA, Sejnowski TJ (2008) Spike-rate coding and spike-time coding are affected oppositely by different adaptation mechanisms. J Neurosci 28:13649-13661.
47. Prescott SA, Ratté S, De Koninck Y, Sejnowski TJ (2006) Nonlinear interaction between shunting and adaptation controls a switch between integration and coincidence detection in pyramidal neurons. J Neurosci 26:9084-9097.
48. Prescott SA, De Koninck Y, Sejnowski TJ (2008a) Biophysical basis for three distinct dynamical mechanisms of action potential initiation. PLoS Comput Biol 4:e1000198.
49. Prescott SA, Ratté S, De Koninck Y, Sejnowski TJ (2008b) Pyramidal neurons switch from integrators in vitro to resonators under in vivo-like conditions. J Neurophysiol 100:3030-3042.
50. Reyes AD (2003) Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro. Nat Neurosci 6:593-599.
51. Rieke F, Warland D, Bialek W (1999) Spikes: exploring the neural code. Cambridge, MA: MIT.
52. Rudolph M, Destexhe A (2003) Tuning neocortical pyramidal neurons between integrators and coincidence detectors. J Comput Neurosci 14:239-251.
53. Salinas E, Sejnowski TJ (2001) Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2:539-550.
54. Schneidman E, Berry MJ 2nd, Segev R, Bialek W (2006) Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440:1007-1012.
55. Schreiber S, Fellous JM, Tiesinga P, Sejnowski TJ (2004) Influence of ionic conductances on spike timing reliability of cortical neurons for suprathreshold rhythmic inputs. J Neurophysiol 91:194-205.
56. Shadlen MN, Movshon JA (1999) Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24:67-77, 111-125.
57. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870-3896.
58. Shea-Brown E, Josić K, de la Rocha J, Doiron B (2008) Correlation and synchrony transfer in integrate-and-fire neurons: basic properties and consequences for coding. Phys Rev Lett 100:108102.
59. Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349-374.
60. 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.
61. Svirskis G, Kotak V, Sanes DH, Rinzel J (2004) Sodium along with lowthreshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. J Neurophysiol 91:2465-2473.
62. Tchumatchenko T, Malyshev A, Geisel T, Volgushev M, Wolf F (2010) Correlations and synchrony in threshold neuron models. Phys Rev Lett 104:058102.
63. Tetzlaff T, Rotter S, Stark E, Abeles M, Aertsen A, Diesmann M (2008) Dependence of neuronal correlations on filter characteristics and marginal spike train statistics. Neural Comput 20:2133-2184.
64. Theunissen F, Miller JP (1995) Temporal encoding in nervous systems: a rigorous definition. J Comput Neurosci 2:149-162.
65. Tiesinga P, Fellous JM, Sejnowski TJ (2008) Regulation of spike timing in visual cortical circuits. Nat Rev Neurosci 9:97-107.
66. Treisman A (1999) Solutions to the binding problem: progress through controversy and convergence. Neuron 24:105-110, 111-125.
67. Uhlenbeck GE, Ornstein LS (1930) On the theory of Brownian motion. Phys Rev 36:823-841.
68. Victor J, Shapley R (1980) A method of nonlinear analysis in the frequency domain. Biophys J 29:459-483.
69. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446.
70. Wolfe J, Houweling AR, Brecht M (2010) Sparse and powerful cortical spikes. Curr Opin Neurobiol 20:306-312.
71. Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370:140-143.